PROCEEDINGS OF THE 1990 INTERNATIONAL CRUSTACEAN CONFERENCE ———— ea. > yl BRISBANE MEMOIR HE VOLUME 31 1 SEPTEMBER, 1991 QUEENS ee an eae Preface The International Crustacean Conference held in Brisbane from 2-6 July 1990 was attended by more than 200 delegates representing 32 countries. The calibre of the papers presented was extremely high and it is a matter of regret that we were unable to publish all of them in their entirety. We publish here, however, almost all of the papers presented by invited speakers at the ‘plenary’ sessions, and a large number of summaries from those papers presented in the other sessions. They have been grouped thematically in order of their presentation at the Conference, with an alphabetical arrangement for the summary papers. As always, the editing of such a volume as this has been major undertaking and could not have been achieved without the willing and enthusiastic co-operation of many people. Special thanks to the other members of the organising committee: Don Fielder, Jack Greenwood, Peter Rothlisberg, Ken McKenzie, Nigel Preston and John Glaister, who all contributed to reviewing and correcting manuscripts. We are also pleased to thank the many outside referees who also gave of their time to ensure that the final published papers were of the highest quality. At the Queensland Museum thanks must go to: Neale Hall for his expert skills in desktop type-setting; John Short, John Stanisic and Glen Ingram for helping see it through the final stages, and general support; and Lynnette Dickfos, Danielle McDonald and Lisa Bamforth for administrative assistance. Kath Davie and Gillian Quinn are especially thanked for all manner of voluntary assistance with typing, photocopying, checking citations and proof-reading. The Organising Committee is also very grateful to the Queensland Museum, and in particular Dr P.A. Jell, for support throughout the conference and its generous financial assistance to make the publication of these Proceedings possible. P.J.F. DAVIE and R.H. QUINN EDITORS CONTENTS EVOLUTION AND BIOGEOGRAPHY PLENARY PAPERS Schram, F. R. and Emerson, M. J. Arthropod Pattern Theory; a new approach to arthropod PAYNE. sia oi ati et oem a be aide toatl abel ene intel teeeesotefep ite ae gs rJerbhidadegises | McKenzie, K.G. Crustacean evolutionary events: sequences and consequences .,.,.,..,.,.- 19 Dall, W. Zoogeography of the Penseidae ., 6) 6.2 cent ews Crrentetes a8 Newman, W.A. Origins of Southern Hemisphere endemism, especially among 1 marine Cristaces. occu teles wok eb te tepee fe ater Oe ry we Ait bots Booey Dae ap eg Swanson, K.M. Distribution, affinities and origin of the Punciidaa (Crustacea: Ostracoda) ..._ 77 SUMMARY PAPERS Frusher, 5.D., Giddins, R.L. and Smith, TJ. {11 Distribution of mangrove sesarmid crabs (Crustacea: Brachyura) in northeasterm Australia .., 0. 0. c cece ae eee ee aae = 93 Hoffman, D.L,, Bertha, N. and Blom, J.G. Latitudinal variations in seltlement and survival of the pedunculate barnacle, Pollicipes polymerus Sowerby ..,.........--...----+-- 4 Holsinger, J.R. Phylogenetic and biogeographic relationships of the subterranean amphipod genus Bahadzia (Hadziidae) in the West Indian region 2.6 cee eee eee 94 Horwitz, P. The conservation status of Australian freshwater crayfish Ajo thins ehtseghtone'a's{ byelb dees’ 95 Marsden, J.D, and Duncan, K.W. Reproduction in sand dwelling talitrid amphipods: evolutionary adaptation for terrestrial life ..-. 22... ee eee eee 6 Mashiko, K. Diversified reproductive traits among local populations of a freshwater prawn, Macrabrachium nipponense (Palaemonidae: Cavidea; Decapoda) — evidence for a Benet DVHSIS PB scaoide, La eva ape Mate phy Sp whe chat wlule ebePaseletiels Ep dshats toby isttataAabdet sb le rhe oT Murofushi, M,, Nakatsubo, T. and Deguchi, Y. Karyotype analysis of the red swamp crayfish, Procambarus clarku, by cell culture... 6.60 ee ee ee ey OR Stevens, P.M. Molecular divergence and host relationships in New Zealand representatives of the pea crab genus Pinnotheres «2.6... ye ye cee teen eee eb ect tee eteveans 99 Swain, R, and Richardson, A.M.M. Gill arcas and evolutionary relationships in talitrid AMphipods .. 6. cee eee eee bead tote Steve me 2 ee A ce, BOE LOO PHYLOGENY AND SYSTEMATICS PLENARY PAPERS Abele, L.G, Comparison of morphological and molecular phylogeny of the Decapoda _... -- 101 Jamieson, B.G.M. Ultrastructure and phylogeny of crustacean spermatozoa ._.....--...-- 109 Brusca, R. C.and Wilson, G.D,F. A phylogenetic analysis of the Isopoda with some classificatory recommendations . 2.2... 00.0... .0 cece cde cece tee e uu ebeuu ensues 143 Manning, R.B. The irnportance of taxonomy and museums inthe 1990s ....,......-,..+- 2 SUMMARY PAPERS Jones, D.S, New techniques to investigate the ontogeny of scalpellid barnacles, and their phylogenetic implications, ~~~ ~~ <<. cece iii cece cece tape ete tent etn ubep epee 208 Juinio, A,R., Macaranas, J.M. and Gomez, E.D. “Sympatric occurrence of two subspecies of Panulirus longipes Milne Edwards, 1868 (Decapoda: Palinuridac) and biochemical evidence of interbreeding ... 2-2 eee cee c epee edeueneuna ... 209 Lavery. S. Genetic population subdivision in the coconut crab, Birgus latra (Anormura; Coengbilidasy 6. os ans cous ce stetig Stl ba lee Pte t bees dete ae eC AGM hoe Jia 210 Poupin, J. and Richer de Forges, B. New or rare crusiaceans from French Polynesia (Crustacea: Decapoda) . 2.1... eee ce cee nee cen ecaes 211 Shih, C.-t. Phronimidae (Crustacea: Amphipoda; Hyperiidea) of the Eastern Pacific ......., 212 Tavares, M.S. Cladistic analysis and classification of the Gecarcinidac (Crustacea: Brachyura) .,....,. pies tzeriagése CRE Nie 8 Se 213 PHYSIOLOGICAL ECOLOGY AND BEHAVIOUR PLENARY PAPERS Greenaway, P. Nitrogenous excretion in aquatic and terrestrial crustaceans . .... 215 Wolcott, D.L. Integration of cellular, organismal and ecological aspects of salt and water balanee <...., PEST ATE LA AG Se i, late teteie mettiolle pla 229 Morris, S. Respiratory gas exchange and transport in crustaceans: ecological Dotee MIA its .-. 24] Gilchrist, S.L. Behaviour of Crustacea: ecological and social perspectives... ...,.- -,. — 203 SUMMARY PAPERS Hargreaves, P.M. The effect of artificially lighted trawls on catches of crustaceans ......,. 276 Hough, A.R. and Naylor, E. The behavioural basis of crustacean distribution ina tidally MAKE ESMaTY 6. be cle ge epee anne J astteale et etia Tei baer tema Meet 240 Jaros, P.P. Biochemistry and function of crustacean neurohormones ..,.....---..---.-.- 278 Langer, H., Pieper, M. and Henning, U. Photoreceptor membranes and visual pigments in \he apposition cyes of the terrestrial crab, Ocypode ryderi (Ocypodidac), during the GAYE WEA CV Ce. ie ls up nlele ort perce a plgeta rene pairs plese ad vb ode 279 Paterson, B.D, Ventilation activity and gut fullness of the burrowing ghost shrimp, Callianassa australiensis Dana (Decapoda, Callianassidac), during low tide —_...__.- 280 Pavey, C.R. and Fielder, D.R. The influence of size differential on agonistic encounters between intermoull freshwater crayfish in Cherax cuspidatus Riek, 1969 (Decapoda; Parastucidae) -.. 222.2. ee ee eye fe bb otes oe $te4 ti ape bb wah foe 281] Pequeux, A. and Lignon, J.M. lonic permeability of the cuticle and ionoregulation in decapod crustaceans -....2..4.45. trbepeesovartate Po WS ee ee, 282 Richardson, A.M.M. and Swain, R, Pattern and persistence in the burrows of rwo species of the freshwater crayfish, Parasiacoides (Decapoda: Parastacidae), in southwest "Fasordnia 400 Pe i eee erent a awtueetes et tes trite brace aad. 283 Ritz, A. and O’Brien, D.P. Gregarious behaviour in crustacean micronekton: an ecological PEXSPOGUIME: 4-49 oy cy kines coal dpe es S20 hl eTT nye is eT KOT Eh Bo 2 Sheehy, M.R.J. Senescence, fluorescence and crustacean age determination ..,.,...... ve 285 Storch, V. Ultrastructure and function of the stamach of Peracarida and Euphausiacea .,.... 277 Taylor, H.H., Greenaway, P. and Morris, S. Brachial modification of urine and osmoregulation in the land crab, Birgus latro (Anomura: Cocnobilidae) ..-. 2.222... 286 Thorne, M.J. and Fielder, D,R. The red cuticle on the claw of male Cherax quadricarinatus (Decapoda: Parastacidge) .,........ Ba Ae ae open gegin= se trig Aen ete alt 277 Xiang, J.H., Clark, W.H.,, Griffin, F. and Hertzler, P. A study on feasibility of chromosome set manipulations in the marine shrimp, Sicyomia ingentis ....-....----. e040 ccs 287 Xiao, Y. and Greenwood, J.G. Effects of hydrostatic pressure on the tidal vertical movement ol Acetes sibogae Hansen (Crustacea:Deeapoda) ;.........-.--..-2---- =.) a, 284 hepatopancreas in Siberian prawn, Exopalaemon modestus ...5. 6.6564 .55 yea 2 282 LARVAL BIOLOGY PLENARY PAPERS Anger, K, Developmental changes in the bioenergetics of decapod larvae .-..,.,. ry Cre 289 Freeman, J.A. Growth and morphogenesis in crustacean larvae -.-..,....-...)2 2. ..2-- 309 Ross, R.M. and Quetin, L.B, Ecological physiology of larval euphausitds, Euphausia superba (Bupharsigesa) ii: a te ee a ee eee egt cree Ate. ,. 321 SUMMARY PAPERS Forbes, A.T, Origin and behaviour of post-larval penaeid prawns in two estuaries on (he Natal coast of South Africa .-2 2.0... .0..-...0.. mip fhe teat eat feletale ee ass Nitoleretefole eae - Grygier, M.J. Facctotecta (*Y-larvae'): one day's catch in Okinawa, Japan (Crustacea: WRONEDGHOUAD An. tats sfoletonajelassinioocite sw widset tie bie i trade tm laleig met al danthiniete a poy ete apes 335 Kannupandi, T. and Pasupathi, K. Laboratory reared larval stages of a mangrove crab, Sesarma edwardsi De Man 1887 (Decapoda : Grapsidac) ...---, 6.2) 0c. ey eye cae 398 Lavery, S. and Cosgrove, M. Genetic identification of ten species of penacid prawn postlarvae .. 222-22. pee ce ees tomer) 428 Sy tele us pom et Vneraap en’ 288 McConaugha, J.R., Tester, PA, and McConaugha, C.S. Feeding and growth in meroplanktonic larvae of Callinectes sapidus (Crustacea: Portunidae) ...._,-,. -». 320 Moreira, G.S. Metabolic responses of some estuarine crustaccan Jarvae to salinity variation . 334 Rothlisberg, P.C., Helmond, I. and Dall, W. A satellite tracked drifter with a vertically migrating drogue for studies of larval dispersal ....... 0.0... 004 ote Eh eR ne 288 Hi RECRUITMENT AND LIFE HISTORY STUDIES PLENARY PAPERS Staples, D,J, Penaeid prawn recruitment: geographic comparison of recruitment pallerns within the Indo-West Pacific region .-.......--...----.----..-----.----,- -,. 337 Ejner, R.W. and Campbell, A. Spatial and temporal patierns in recruitment for American lobster, Homarus americanus, in the northwestern Atlantic ._... cate weeny ey 349 Jamieson, G.S. and Armstrong, D.A. Spatial and temporal recruitment patterns ‘of Dungeness crab in the northeast Pacific ....-......0. 00. 2.002 one y2iceys See tase ee 365 SUMMARY PAPERS Abellé, P. and Macpherson, E. Life history characteristics of Luhodes ferax (Anomuta: Lithodidae) off Namibia . 2.6.6 oe cc eee ee eee eee eee 364 Armetta, T.M, and Stevens, B.G. Aspects of the biology of the hair crab, Erimacrus isenbeckii, in the eastern Bering Sea (Ceustacea: Decapoda: Atelecyclidae) ....,,. ,.. 383 Armstrong, D.A. and Gunderson, D.R. Unusually rapid growth of coastal 0+ Dungeness crab may lead to strong fisheries... 2 eee re cae vee neues phate cunts 382 Armstrong, J.L., Armstrong, D.A, and Dinnel,P.A. The impact of staghorn sculpin predation on newly settled Dungeness crab .--. 222 ee eee eee 3R4 Briones-Fourzan, P. and Lozano, E. Some biological aspects of the giant isopod, Bathynomus giganteus (A, Mitne-Edwards) (Iscpoda: Cirolanidae), off the Yucatan Pepinerita s! Os, tcutaties 0! po cet eaar bees eth ede) ck eh aptcan pits cdhte ats . 3&5 Bryant, A.D. Growth and reproduction of two species of spider crab (Brachyuru; ‘Majidae) 1 386 Choy, S.C. Life history and biology of Sacculina carcint (Cirripedia: Rhizocephiala) parasitising Liocarcinus holsatus (Decapoda; Brachyura)..--....-...--.-...--.-. ~ 406 Choy, S.C. Distributional ccology of the velvet swimming crab, Necora puber (Decapoda, Brachyura, Portunidae) .. ~~... ..---- scree eter ere e scene phoney enseyapes . 407 Gulati, R.B. Role of filter-feeding crustacean zooplankton in Dutch lakes of varying depth QA APOARY. baits Fy ean Sa aed eRe TE hod tig SE are bolby ate teste (acne betes Waefner, Jr., PA. Natural diet of Callinectes ornatus (Brachyura: Pottunidae) i in Bermuda | - _ 388 Hamre, P. The life histories of the Tasmaniin freshwater crayfishes of the genus asincd (Decapoda: Parastacidac) ..... pce be SO pouea Bhs es ope tae ot oth Cee ee Qe eens 388 Hassan, H.-u. Immigration of Metapenaeus stebbingi, M. affinis and M. monoceros juveniles in the creeks and backwaters near Karachi... 6.0.0. ce eka a eels e eeu cece 389 Jensen, G.C. Gregarious settlement by porcelain crabs, Petrolisthes (Anomura: Porcellanidae) . 0...) 2 np een eget ence eee cence ee bey eee pees ,. 390 Karlsson, K. and Christiansen, M.E. Vertical migration of the edible crab, Cancer pagurtes (Crustacea; Decapoda: Brachyura), on rocky shores of the south coast of Norway ..... 391 Lindberg, W.J., Frazer, T.K. and Stanten, G.R. Spatial structure in a stone crab population Gace ura’ Xanthidae) and the interplay with resource mosaics ......-,----.----,- 392 Maris, Spatial and t¢mporal dispersal and recruitment patterns of decapod Crustacea tn the northwestern Atlantic 6.0.0... cece he eee been ede peed ebeeas 393 Nicol, S., Stolp, M. and Hosie,G.W. Age structure of Antarctic krill (Euphausta superba) populations as determined by age-pigrnent analysis and by size-frequency analysis ... . 394 Norman, C,P. and Jones, M.B. Estimation of growth parameters of the velvet swimming crab (Liscarcinus puber) (Brachyura: Portunidae) at Plymouth, S.W. England , evry 395 Omori, M. Spawning behaviourof Sergia lucens (Hansen) (Decapoda: Sergestidae) _. Sy iches d 396 Pitcher, C.R., Dennis, D.M., Skewes, T.D. and Prescott, J.H. Catastrophic mortality of breeding tropical rock lobsters <4... 06. cs ese y sc ek Se eee cic i ee ee bebe eee es eens 397 Preston, N.P. Replenishment of crustacean associates of coral isolates in the central region of the Gipeol Garr’ Reed ce seen tee ee we xii -gi see aetie pales ie tye 398 Quinn, N.J., Kojis, B,L., Diele, K. and Meischner, U. Reproductive behaviour of Cardisoma carnifex (Herbst, 1794) (Brachyura: Gecarcinidae) at Lizard Island, Great Barrier Reef ......- <5. beens ete bene eines ite teed eis) ate isasetests 399 Rainer, S.F. Food and diurnal behaviour of deepw ater prawns .........-.-...-....----- 400 Reid, D.G., Abello, P.and Naylor, E. Size and assortative mating in the shore crab, Carcinpes ARBEMES | a wee oe S5,S fone Caen eT ener ag erie sane sha pene spies caatpe ts ae 401 Shields, J.D. and Wood, F.E.1. Pathology and fine structure of Ameson Sp. a microsporidian from the blue sand crab, Portunus POMAGICUS «eats tei hdaciiec ede ibieesteactee 403 Shields, J.D. The community ecology of the parasites and symbionts of Portunus pelagicus: evidence for positive and negative interactions 2,-0.0... eee eee eee ees Su, M.-S. and Liao, 1.-C. Life history of the bear prawn, Penaeus semisulcatus, in coastal waters of soulhwest Taiwan .-.......-.,...-. Peay (ube tetat. dilate: (rte are 402 Watkins, J.L., Morris, D.J., Buchholz, F., Ricketts, C. and Priddle, J. Variation in the reproductive status of swarms of Antarctic krill . 2... .....00..202 020-220-220, 404 Wenner, E., Boylan, J. and Knott, D, Daily and monthly settlement patterns of brachyuran megalopae on artificial substrates ..........,-,, Fe wamssiniels at a alas bel yretale ind amt 403 wokpil T.G. and Wolcott, D.L, Microprocessors and field instrumentation for crustacean PORTS wus. an sits tp eae rem fon tet pale din ah sPaaedmo thats pte se yey ee qois fee , 400 Wooldridge, 1H. The response of mysid shrimps to phytoplankton distribution in a high energy surlzone ..-.. 22... ee VoTere re cyan. (bt Aci e4 ! tbe State . 40s FISHERIES AND AQUACULTURE PLENARY PAPERS Smith, P., Kingston, A. and Battaglene, T, The Japanese market for crustaceans ....,..... 400 Hardman, J.R.P., Treadwell, R. and Maguire, G. Economics of prawn farming in Australia 421 Van Eys, S. World shrimp production ....-.. pi bsstehiqny. § Aedes Ceeysbayk ae 435 SUMMARY PAPERS Allan, G.L. and Maguire, G.B. Lethal effects of acidified seawater on Penaeus monodon and the interaction of salinity and pH on sub-lethal effects ~.--.....-.0.000 1 cine. 420 Baelde, P. Analysis of catch statistics from the deep-water prawn (Haliporoides sibogae) fishery off New South Wales, Australia ....-.-._- terete sitter epts rede tes ose 447 hatisuicatus fisheries ---.,-. 0-2 en po gintn a fret ptefitog batt pinot pond a re beeen 447 Conan, G.Y. and Maynard, D.R. Experimental carapace increase in the lobster (Harmarus americanus) fishery on Cape Breton Island, Canada... 2.22.2... ee pe pees 440 Dail, W., Smith, D.M. and Moure, L.E. The biochemical composition of natural food of Penaeus esculentus Haswell (Penaeidae: Decapoda) ........._.. poeerecs loeb A! 448 Deguchi, Y., Sugita, H. and Kamemutou, F.1. Spawning control of the Japanese spiny lobster 449 Deng, J. Management and enhancement of the stock of Penaeus orientalis Kishinouye in the Yellow Sea and the Bohai Sea _.....-.--.....- Se wee eee aay yoyo baa sept. 24s 450 Dredge, M.C.L. and Gribble, N.A. Evaluation of seasonal closures as a means of optimising yield from a multi-species prawn fishery -_.......-.-..... rosthHdarerge oe 451 Gracia, A. The white shrimp (Penaeus setiferus) fishery in he Campeche Bank, Mexico .... 451 Gribble, N.A. and Dredge, M,C.L, Preliminary results from a study of a central Queensland coastal prawn fishery .....- 22. 2-22 eee eee eevee u pees jaded $24 453 Jackson, C.J., Pendrey, R.C..and Rothlisberg, P-C. The Larvatron: a computer controlled apparatus for reating planktonic animals ..--....4..0 222... e045 taxis team its 456 Kennelly, S.J. Consequences of the mortality of discarded spanner crabs (Ranina ranina) ina tangle-net fishery — laboratory and field experiments .-.--..-..-- ~~...) 2.00.0. e- 455 Liu, J.¥., Cui, Y.H., Xu, FS. and Xiang, J.H. Recruitment and stock enhancement of the Chinese shrimp, Penaeus orientalis Kishinouye (Decapoda, Crustacea) -......-..... 4 Maguire, G.B. and Forteath, G.N.R, Commercial recirculating scawater systems for holding rock lobsters in Tasmania, Australia... ... Wiecige ita opi ati ey aD eu dyed oh dy oi nba esctt e 32 internal tags or markings -............ Abie mle ples afta e's bem tebil obits in wets the.b wept ote SO Moriyasu, M. and Conan, G.Y. An alternative stock management for snow crab, Chionoecetes opilio (Brachyura, Majidae), based on the presence of a terminal moult _. 461 Nicol, S. The fishery for Antarctic krill (Euphausia superba)..............,. eye yey 460 Pandian, T.J. and Murugadass, S. Effect of dietary protcin on sexual maturity and egg production in the economically important riverine prawn, Macrobrachium tiabilii ,..., 454 Rippingale, R.J. and MacShane, M,G, A calanoid copepod for intensive cultivalion.,.,... 457 Sanguila, W.M. and Mendoza, N.C. Alternative seration system for intensive prawn ponds . 455 Sarac, H.Z. and Kanazawa, A. Effect of essential amino acid supplementation of casein and sardine powder on the protein requirements of the prawn, Penaeus japonicus ..,.,.. . 458 Turnbull, C.T. Aspects of the biology of commercial penaeid prawns in Torres Strait ,.,... 459 Wadley, V.A. and Morris, §.L. Deepwater fishery for prawns and carids off Western Australia .-......4. Mtr lbe nities pes ee een one ee eee 456 MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ARTHROPOD PATTERN THEORY: A NEW APPROACH TO ARTHROPOD PHYLOGENY FREDERICK R. SCHRAM AND MICHAEL J. EMERSON Schram. F, R. and Emerson, M. J. 1991 0901; Arthropod Pattern Theory: u new approach 10 arthropod phylogeny, Memors of the Queerisland Museum 31: 1-18. Brisbane, ISSN 0079-8835, A review of fossil, morphologic, developmental, and genetic evidence suggests a series of mew and novel hypotheses jo explain the evolution of arthropods. Termed Arthropod Pattern Theory (APT), these hypotheses are: 1, That the biramous limb was formed by the basal fusion of uniramous limbs: 2. Thal a uniramian diplosegment (or paired monoseg- ments) is homologous to a single body segment, or duplomere, of arthropods bearing biramous limbs; 3, Thal suites of segments evolve as units with tagmala transitions. location of gonopores.and anus, and bady terminations occurring at specific points along the body thal are shared among disparate groups. APT requires a complete reassessment of old assumptions aboul segment homologies within articulates. (-] Arthrapeda, Crustacea, Remipedia, Euthycarcinoidea, Drosophila genetics, segment pairing, uniramy, hiramy, phylogeny. Frederick. R. Schram , Seripps Institution of Oceanagraphy, La Jolla, CA 92093-0202, USA; Michael J. Emerson 6 July, 1990. Seldom does the study of fossils cause a complete reassessment of previous assump- tions about evolution within an entire phylum. However, the problematic arthropod, Tesnuse, caris galdicht (Brooks, 1955), from the Late Mississippian of west Texas (Schram and Emerson, 1986; Emerson and Schram, in press) and other fossils reveal some previously umsus- pected features of urthropod anatomy that neces- sitate such a re-evaluation. Brooks was uncertain in his original de- scription of T, goldichi as to the exact aflini- ties of this species, and he compared this fossil with crustaceans such as branchiopods and cephalocarids. Hessler (1969) rejected the latter assignment. and Schram (1983, 1986) suggested possible affinities with the Class Remipedia. The new material reveals the cephalic anatomy of a remipede, but thoracic appendages with most peculiar fea- tures (Fig. 1), Each trunk segment of Tesnu- socaris possesses two pairs of ventrally placed uniramous limbs: a medial pair directed posteriorly and possibly used in sculling, and a ventral pair directed laterally and apparently used in rowing (Emerson and Schram, in press). The significance of these limbs, became apparent when they were compared to other peculiar late Palaeozoic arthropods (Emerson and Schram, 1994). This comparison suggested a novel hypothe- sis for the evolution of the biramous crustacean limb, viz., that biramy evolved by means of the fusion of basal podomeres of udjacent uniramous limbs. We found the above anatomical observa- tions and the concepts they suggested inter- esting. although the stratigraphic position of Tesnusocaris in the Carboniferous. might seem to contradict interpretation of this fos- sil aS an ancestral crustacean. However, we ure not proposing that Tesausocaris is an ancestor, merely that its trunk limb anatomy represents a more primitive condition than that seen in biramous arthropods. Further- more, its stratigraphic position ts unimpor- tant because there appear to be even earlier remipedes in the fossil record (Mikulic eral., 1985, fig. 16). Certainly, one caveat of paleontology is that ‘things are always older than you think they are’, e.g. discoveries of the earliest uniramians (Mikulic er al., 1985; Robison, 1990). Other kinds of arthropods seem to share this distinctive arrangement of trunk limbs, but previously they were not recognised as such because no one had realised the possi- bility of such an anutomical condition. One of the best candidates is the Cambrian Burgess Shale arthropod Branchiaocaris pre- tiosa, Briggs (1976) reconstructed flap-like limbs attached to a ventrolateral ridge on the trunk (Fig. 2B). He noted proximal elements that appeared to extend along the medial a To ~., \¢ was ie, b ir mets A 4) be 7 } ¥ { he \ \} i, A PRS Win, FIG, 1. Ventral reconstruction of Tesnusecaris 2ol- dichi from the Upper Mississippian of Texas (from Emerson and Schram, in press). edge of the flap toward the body midline, Briggs. designated the proximal elements as reinforcing structures or endites along the flaps, but in the text udmitted difficulties im interpreting the fossils and pointed out the tentative nature of his reconstruction of the limbs, However, published camera lucida drawings (Fig. 2A) reveal that these medial clements have a more sagittal position than the lateral (laps. This arrangement, with rami of ut least seven podomeres, simple transverse ar- ticulations between podomeres, and a flipper- like outline, suggests to us that the sagittal elements bear a clear resemblance to those of Tesnusocaris. The flap-like lateral elements on Branchiocaris, therefore, are comparable to the ventrolateral pair of limbs of esnusocaris.. Careful examination of other fossil arthropods MEMOIRS OF THE QUFTRNSLAND MUSEUM may reveal additional examples of (hrs arrange- ment of trunk limbs, The peculiar form and position of the limbs in relation to the Irunk segments of animals like Tesausocaris require a new setof terms to describe appendages and segments in arthro- pods (Emerson and Schram, 1990). The seg- ments of insects and some myriapods are monomeres (or monosegmenty) with each seg- ment bearing one pair of uniramous limbs. The monomeres of many myriapads and the fossil cuthycarcinoideans are paired with the dorsal tergites fused and the ventral sternites free, thus forming diplomeres (or diplasegments). Each diplomere bears two sets of uniramous limbs, one set on cach stetnite, We contend that crustaceans, and by extension other ar- thropods that bear biramous limbs, have completely fused the ventral sternites of adja- cent segment pairs, as well as the dorsal ter- gites, to form duplomeres. Arthropods like Tesnusocaris and possibly Branchiocaris are therefore duplopedous, displaying two sets of umiramous limbs on each duplosegment. The medial pair of trunk limbs on Tesnusocaris are known as the endopedes, the lateral set are the exapedes, Except for the above, most other fossil and living arthropods are biramous, with a single set of branched limbs on each du- plosegment, although secondarily uniramous limbs have reoccurred several times. The Euthycarcinoidea were apparently aquatic creatures that lived from Carbonifer- ous to Triassic time. The most recent review of the group (Schram and Rolfe, 1982) agreed with the suggestion of Bergstrom (1980) that placed the problematic euthycarcinoidcans within the Uniramia, The trunk of these fossils is divided into an anterior limb-bearing region and a posterior limbless area; differences in this regard are the basis for two subgroups (Schram and Rolfe, 1982; Starobogatov, 1988): the Sottyxerxidae (= Sottyxerxiformes) have a long anterior trunk (Fig. 3A), and the Euthyearcinidae (= Euthyearciniformes) possess a short anterior region (Fig. 3B). In both vroups, the trunk is characterised by a serics of diplo- and triplosegments bearing uniramous limbs that are evocative of similar conditions in extant myriapods. The cuthycar- cinoidean head is not well known, bul appears to resemble the hypothetical primitive arthro- pod head of Snodgrass (1952), with an anterior procephalon bearing 4 single pair of antennac and a distinct posterior gnathocephalon bear- A NEW APPROACH TO ARTHROPOD PHYLOGENY SS WA \ASZ: amy vy | SNe a aaAS ae =A=s'= Nie 5 =< Ao i re i) Au= — —_ —= — t ss! a8) FIG. 2. Our interpretation of Branchiocaris pretiosa, from the Cambrian of British Columbia, A, Camera lucida drawing of USNMP 189028. B, Ventral reconstruction of the adult (modified from Briggs, 1976). ing the mouth and a set of rarely preserved mandibles. Comparison of Tesnusocaris, possibly Branchiocaris, and the euthycarcinoideans with the uniramians and crustaceans suggested to Emer- son and Schram (1990) a new interpretation of arthropod limb evolution. However, so unusual is this interpretation that the fossils are insufficient to justify it; confirmation comes from the fields of comparative anatomy, ontogeny, and developmen- tal genetics. The elements of Arthropod Pattern Theory (APT) are considered below. 4 MEMOIRS OF THE QUEENSLAND MUSEUM PIG. 3. Dorsal reconstruction of Euthycarcinoidea from the Middle Pennsylvanian of Mlinois. A, Pieckoxerxes pickoae. B, Kattixerxes gloriosus. (modified trom Schram and Rolfe, 1982). HYPOTHESIS ONE The biramous limb of Crustacea (and probably all arthropods bearing such) evolved by means of the basal fusion of duplopodous, uniramous limbs. In analysing Tesnusocaris, Emerson and Schram (in press) considered the possibility that the two sets of separate uniramous limbs on single trunk segments were only apparently so, ic. that the arrangement of structures seen in the fossils might represent biramous limbs in which the protopods were incorporated, or fused, into the body wall. This would be analogous to a situation in isopods. This alternative was re- jected on both structural and functional grounds. The exopedes and endopedes appear to have functioned in distinctly different ways from cach other and thus likely possessed different muscu- latures; their physical separation on the Tesnuso- caris trunk somites seems too great to have been derived from a single limb pair; the basul seg- ments of both limbs resemble true coxac; and the number of podomeres is more (not less) than would be expected if a biramous limb fused proximal articles into a body wall. We concluded (Emerson and Schram, in press) that the trunk limb analomy of Tesnusocaris Tepresents two separate sels of appendages on each trunk Segment. Furthermore, distinct limb and segment morphologies are recognized among living and fossil groups (Fig. 4), One condition occurs when the tergites of adjacent somites fuse to form diplosegments, while the still separate sternites each bear a pair of uni- ramous limbs. Examples of this condition are noted in diplopodous myriapods and euthycar- cinoideans (Fig. 4A). A second condition occurs in which each monosegment bears a single pair of uniramous limbs. Examples of this condition are seen in geophilomorph centipedes (Fig, 4B) and insect thoraxes. A third condition exists FIG. 4. Ventral views of trunk somites of various arthropods. A, Diplasegment of a generalized euthycarcinaidean with each sternite bearing a pair of uiniramous limbs. B, Two monosegments of a geophilomorph centipede with uniramaus limbs. C, Duplosegment of Tesnusocaris goldichi with two sets of uniramous limbs. D, Duplosegment of ageneralized nectiopodan remipede with biramous limbs (from Emerson and Schram, 1990). A NEW APPROACH TO ARTHROPOD PHYLOGENY 5 furrow FIG. 5. Maxillule of Skara anulata displaying the median furrow on the pratopod (from Miiller and Walossek, 1985), when both tergal and sternal fusion occur to form, what we call, duplosegments. Separate pairs of uniramous appendages give the appear- ance of \wo'sets of limbs on cach duplosegment, The prime example of this is Tesnusocaris (Fig. 4C). We hypothesise that in the final condition the basal podomeres of the separate limb pairs of a duplosegment fuse to form the common pro- (1988) questions whether these fossils are really crustaceans.] Although the interpretation of these furrows. 1s open to speculation, and issues of fossil preservation should not be overlooked, in light of our hypothesis, these furrows could be indications of the remnant of fused medial and lateral elements in the formation of the protopod in animals such as Skara and Bredocaris. A more compelling line of support comes from observations of Ito (1989) who, in comparing the morphology of the copepodan trunk limb to that of nectiopodan remipedes, concluded that the basal podomeres of the nectiopodan exopod and endopod fused to each other to form the basis of the copepodan protopod (Fig. 6). Ito felt that this fusion was. supported by the arrangement of the intrinsic muscles af the appendages of the two groups in question, and by the positional ho- mology of the setose accessory fold found at the base of the exopod in many nectiopodans with the setose lateral arm of the basis in copepods, If a process of segment fusion could have evolved the crustacean basis, then it is possible that an identical process could have produced the coxa. coxa topod of a biramous limb with exopod and en- //// dopod branches (Fig.4D). This is exemplified by crustaceans that bear biramous limbs. trilobites, - and many of the Burgess Shale arthropods. The above may seem startling. Nevertheless, the hypothesis that there was a tendency in the early evolution of crustaceans to fuse basal podomercs gains some support from the study of several fossil and living arthropods. For example, an interesting, but problematic, condition occurs on certain fossils, Distinct fur- rows exist (Fig. 5) on the anterior and posterior faces of the coxae and bases in many of the Cambrian Orsten crustaceans from Sweden (Miillerand Walossek, 1985, 1988). | Lauterbach A FIG. 6. Trunk limbs. A, nectiapodan; B, copepod. Shaded portion designates postulated homologous regions of the proximal podomeres of nectiopodan rami and the copepad basis (from Ita, 1989) 6 MEMOIRS OF THE QUEENSLAND MUSEUM Although the data above suggest only that the crustacean biramous limb could have been formed by the fusion of duplopodous limbs, this process may also be extended to an explanation of the biramous limbs of other schizoramians such as trilobites, various Cambrian Burgess Shale arthropods, and extant and extinct cheliceriforms. Briggs and Fortey (1989) pre- sented a cladistic analysis of the Burgess Shale and other arthropods that suggests that cheliceriforms, trilobites, and their Cambrian al- lies are more derived schizoramians than are crustaceans. We believe that in general their conclusion is valid, but just how the specific interrelationships may sort themselves accord- ing to APT features awaits more detailed development of our own character matrix. HYPOTHESIS TWO A uniramian diplosegment, or two mono- meres, is homologous to a single crustacean (and, by extension, other biramian arthropods) body segment, or duplosegment. The fundamental axiom of comparative anat- omy of articulate invertebrates (arthropods and their allies) has been that all body segments among phyla within this group are homologous. Without any evidence to the contrary, it has never been thought necessary to question this assumption. However, if the origin of the biramous limb is hypothesised to derive from the fusion of duplopodous, uniramous elements, then that basic assumption must now be ques- tioned. We sought support from comparative anatomy. The nervous system of crustaceans provides several excellent examples in this regard. In the central nervous system of the cephalocarids (Elofsson and Hessler, 1990) as well as branchiopods, such as notostracans, anostracans, and conchostracans (Fig. 7C), the paired ventral cords are linked by two commissures in each segment of the head and trunk. Nerve cords in other adult crustaceans and arthropods typically exhibit various degrees of fusion, thus perhaps obscuring a similar pattern. However, in the annelids and uniramians such as centipedes, a single commissure or ganglion exists for each monosegment (Fig. 7A), and in diplopods there is only one fused ganglion per monosegment sternite, i.e. two per diplosegment (Fig. 7B). Where onychophorans fit in this regard is un- clear, since they have multiple commissures along the entire length of the nerve cords but no well-organized ganglia that would mark the seg- ments (Meglitsch and Schram, 1991: 354). In the ontogeny of peracarid and stomatopod crustaceans, there are several instances of the occurrence of double ganglia in segments (Fig. 7D). Transitory anlagen of a second pair of gan- glia occur in the sixth abdominal segments of mysids (Manton ,1928), some stomatopods (Shiino, 1942), tanaids (Scholl, 1963), and isopods (Stromberg, 1967). In addition, a transi- tory furrow occurs in the course of development on the sixth abdominal ganglia of amphipods (Weygoldt, 1958). The traditional interpretation of these phenomena has been that they represent the fleeting appearance of the ganglia of the supposedly ancestral seventh abdominal seg- ment. Although this interpretation could be true, we feel that it is equally likely that these extra ganglia and the furrow may represent the delayed fusion of the second set of ganglia as- sociated with the sixth abdominal duplomere. A similar explanation could be applied to the strange, double arterial supply from the heart to the musculature of the first abdominal segment in certain stomatopods (Komai and Tung, 1931; Siewing, 1956; Schram, 1969). These arteries may not be a remnant of an extra segment in the anterior part of the stomatopod abdomen, as has been suggested, but rather may represent rem- nants within the circulatory system of a first abdominal duplosegment. Reaka (1975, 1979) noted an unusual pattern of moult sutures in stomatopods. The median suture on the sixth, seventh, and anterior half of the eighth thoracomeres connects to a lateral suture on the posterior half of the eighth thoracic and the abdom- inal segments. Rather than indicating, as has been suggested, evidence for an extra monosegment in the anterior abdomen/posterior thorax, the diver- gent sutures within the last thoracomere may mark the separate components of an eighth thoracic du- plosegment. Dohle and Scholtz (1988) studied the early differentiation of limbs in peracarids. Two dis- tinct cell lines give rise to the anterior and post- erior regions of the limbs of the post-oral segments. It is possible that this pattern repre- sents a remnant of the duplosegmental ancestry of those limbs, although an alternative hypothe- sis has been put forth based on the concept of parasegment compartmentalisation derived from work on Drosophila ontogeny (Martinez- Arias and Lawrence, 1985). A NEW APPROACH TO ARTHROPOD PHYLOGENY 7 FIG. 7. Arthropod central nervous systems. A-C, Semi-diagrammatic representations of the paired ventral nerve cord of arthropods. A, Centipede, with one set of fused ganglia per monosegment; B, Diplopod, with one set of fused ganglia within each segmental component (dashed lines) of a diplosomite (solid lines); C, Conchostracan, widely spaced cords with two commissures within each duplosegment (from Emerson and Schram, 1990); D, Nerve ganglia development in Heterotanais oerstedi with last two thoracic and all abdominal anlagen numbered, the last two ganglia interpretable as either the last two of 7 abdominal monosegments (traditional view) or two portions of a 6th abdominal duplosegment (APT view) (from Scholl, 1963). The above examples support our hypothesis that the crustacean segment is a composite, or duplosegment, formed from the fusion of two monosegments. Furthermore, ontogenetic and developmental patterns in uniramians seem to second the view that the segments of insects and myriapods are organized in a fundamentally different way than those of crustaceans. In the ontogeny of Drosophila, the phenotypic expression of repeating monomeres (Fig. 8A) is governed by two types of pair-rule genes (Niisslein-Volhard and Weischaus, 1980; Scott and O'Farrell, 1986), an odd pair-rule type that governs the expression of odd numbered seg- ments, and an even pair-rule gene that controls the even numbered segments. The expression of individual monomeres depends on the interac- tion of both these loci. The discovery of this peculiar mode of segmental patterning was unexpected and startled those working on the genetics of fruit fly development (Niisslein-Vol- hard and Weischaus, 1980: 287). This peculiar 5 MEMOIRS OF THE QUEENSLAND MUSEUM odd-skipped FIG, 8. Diagrammatic representations of gene mu- tants in Drosophila larvae, Pair-rule genes control expression of every other segment, be it odd o1 even. Gap genes control the expression of a series ofsegments (modified from Niisslein- Volhard and Wieschaus, 1980). control of segment development in Drosophila is still difficult to explain under the strictures of traditional views of articulate segmental ho- mology. However, this genetic control is readily accountable in APT by the assumption of an arthropod synapomorphy of segmental pattern- ing organized in units of two as scen in the comparative anatomy of fossil and living forms. The manifestation of pair rules is evident in other extant uniramians as well. Scheffel (1965) noted that in the anamorphic centipedes twa segments at a time are added with each moult stage, and Minelli and Bortolleto (1987) pre- sented strong evidence for segmental pairing based on multiples of two in diplopods that typi- cally add legs during anamorphic growth in units of two or powers thereof. Other epimorphic my- riapods also exhibit some segment pairing in the trunk, viz. lithobiomorph and scutigeromorph centipedes, pauropods, and symphylans. In short, the segmental pairing seen throughout the uniramians, either in the genetics controlling development or the patterns of anamorphic growth and adult morphology, suggests thal this feature was shared with their immediate ances- + Or, In contrast to the segment pairing in uniramian ontogeny, biramian arthropods exhibit no such pattern. Segment budding in the germinal dises of crustacean embryos occurs only one ata time; and, while the appearance of segments in larvae displays no consistent patlern, leg buds in larvae typically appear one at a time (Schram, 1986), Itow (1985, 1986) found that segments appear one at d time during the early ontogeny of limu- lines. Although data are limited and circumstantial, budding of single segments in biramian arthropods instead of segment pairs is exactly what would be expected if a single biramian duplosegment is in fact homologous to two uniramian monosegments. HYPOTHESIS THREE Suites of Segments in arthropods evalve as units, with the transition of tagmata. the location of ganopores and anus, ana the body termination occurring al specific points along the body that are shared between disparate groups. As we initially began our work, comparing nectiopodan temipedes, Tesnusocaris, and the two main groups of euthycarcinoideans, we no- ticed that certain zones along the length of the body seemed to be the focus of distinct anatomi- cal events (Fig. 9), For example, duplomere 6 (de) not only marked the terminus of the head in the crustaceans, but also was the location of an anomalous monosegment in Soltyxerxes miultl- plex (not illustrated here) and was involved in some Way In the appearance of triplosegments in the anterior trunks of all Euthycarcinidac, Furthermore, duplomeres | |—13 marked another region in these animals in which the female gonopore in nectiopodans, segmental anomalies in Sottyxerxidac, and postabdominal termina- tion in Euthycarcinidae occurred. Finally, duplomeres 18-20 marked the location of the male necliopodan gonopore as well as a transi- tion of pre- and postabdominal tagmata in the sottyxerxids. Initially, we viewed these co-occurrences as interesting but coincidental. If the patterning of A NEW APPROACH TO ARTHROPOR PHYLOGENY u arthropod segmentation were under no particular control, We would have expected that the Inea- lion of gonopores, tagmata trunsitions, and hady terminations would have occurred randomly along the arthropod body, However, when we examined other arthropods, we noled thal these same areas consistently marked either the loca- ion of prominent anatomical structures, or (ran sitions of lagmata,or body terminations. We then realized thatthese patierns were nor random atall, We eventually came lo refer lo suites of seg- ments as either ‘fields’ or *nades’ Fields are adjacent duplomeres that are tor the most part legions of taymatic stability, while nodes are suites of somites Where anatomical events Seem to focus (Figs ¥-11). Duplomeres 1-4 (mono- meres 1-8) mark the first field, duplomeres 5.and f (mOnomeres 9-12) are node one, duplomeres. 710 are the second field, duplomeres | !-13 are node two, duplomercs 14-17 are the third field, duplomeres 18-20 are node three, and duplom- eres 21 la the end of the body mark the fourth field, Thus the arthropod body can be divided into an alternating series of 4-2-4-3-4-3-n num- bers of duplosegments (or S-4-5-6-8-6-2n mon- usexments), In addition, secondary nodes appear to focus on duplomere 9 within the second field. in the cuthycarcinid genera Korixerves and Schramixerxes, some maxi llopodan crustaceans, and almost all cheliceriforms, and on duplomere !6 in many crustaceans. As noted above, the nodes are the principle places where gonopores are located, tlagma boundaries occur, and bodies terminate. When shifts in the location of these structures ovcur during the evolution of a group they appear 10 take place in quantum jumps from one node to the next. As with pair-rule genes in patterning of arthropod segment differentiations discussed above, another class of genes that has been studied in insect development, gap genes, seems relevant to understanding the control exerted over the patterning of arthropod body regions, Gap genes (Fig. 8B) govern the differentiation of suites of segments; und futations in these genes result in the deletion of entire segment scries.. Consequently, it is now possible to visu- alize the wpparent movement of anatomical structures forward in the arthropod body, such as gonopores and tagna boundaries, as gap muta- lions interact with regulatory genes to shorten the body and shift structures in quantum jumps within he framework of the underlying 4—2-4-3- 4-3-/) architectural plan of fields and nodes, The Uniramia provide a clear example of pat- fer evoliition (Tahle 1; Fig, 10), Among the centipedes, the longest bodied forms are the ge- ophilomorphs with terminal gonopores, Other centipedes show anterior shifts of the zonopores and body terminus. Scolopendromorphs (Fig. 10) delete node three and the fourth field to shift their anus and terminal gonopores to the end of the third field, and sculigeromorphs and lithobi- omarphs delete the third ficld with the result that the anus and terminal gonopore occur in the last segmenis of node two. In all centipedes, the bexinning of the trunk occurs within node une In the other myriapods, the gonopores open only on monomeres of node one while the anuses and body termini occur in the last monomeres of a more posterior field or node (Pig, 10), Collobog- nathan diplopods bear gonopods and these are found on segments of node two. In the hexapod vranps (insects und upterygotes) the thorax/ah- domen transition is a node one event and gono- pores are Jocated at the end of the second field (Fig. 10), Thus, in uniramians, the location of yonopores and reproductive structures are jo- cated either in nudes or on the terminal segments of the fields just anterior to nodes, This pattern is SO Consistent That it allows us to predict, for example, that the gonopore of the strange fossil myriapod Arthropleura will be found probably in node one, A similar, although more complex pattern can be found among the crustaceans (Table 2: Figs 9, 11). The longest bodied crustaceans with the most posterior location for gonopores arc the nectinpodan remipedes (Fig. 9); the fermale pore is in node lwo, bul the male pore is in node three, We predict that gonopores {nr ihe extinct Tesi socaris, should they be found. will occur in either one or both of those same nudes. With some exceptions, gonopores of other crustaceans occur either in node (wo or node one, The exeep- lions are interesting in their own right in that their occurrence is not random, The Branchiura and Mystacocarida have gonopores on duplomere 9 (dy) of the second field, while duplomere 16 (dry) of the third field is the location of either guna. pores or terminal anuses in several maxillopodan and phyllopodan groups. Both dy and di are bwo duplomeres forward of nodes (wo and three re- spectively, It is tempting to suggest, in light of what we know about gap mutations, that the shifl forward in these animals might be due to a mu- tation that involved the expression in whole orin part of node one fa two duplomere node), The fact that these exceptions in the Crustacea are oot 10 MEMOIRS OF THE QUEENSLAND MUSEUM Crustacea: Remipedia Enantiopoda Nectiopoda Tesnusocaris goldichii Aq F Lasionectes entrichoma Uniramia: Euthycarcinoidea Sottixerxiidae Euthycarcinidae Pieckoxerxes pieckoae Kottixerxes gloriosus ate = PPPS [_mone-sonie 4 a po[ra}ins fro| naff fo fx] s]a]a ||] feolco] fon fen] ee] eo | ns} pg ey eg Pa a) goed Oe ad a Cod ed) leat 7 | Fourth [45] T33 Field [fast | Mra FIG. 9. Diagrammatic representations to illustrate some APT features of remipede crustacean and euthycar- cinoidean uniramian body plans, with APT numeration to the left. The ? indicate uncertainty as to whether monomerous or diplomerous. Small circles = eyes, triangle = labrum, square = mouth, circle = gonopore, inverted triangle = anus, half shaded = predicted location. random, but also conform to a pattern, indicates that some underlying genetic control of pattern formation is operational in the crustaceans. Further confirmation of such field/node archi- tecture is found in the patterns of early differen- tiation of the germinal disc of peracarids (Dohle and Scholtz, 1988). After the egg nauplius stage is passed through, the postnaupliar germ band is re-organised as the teloblasts differentiate. At that point, before the teloblasts begin to pro- liferate body segments, segmental compart- ments for the maxillules, maxillae, and first thoracomeres appear all at once on the germ band. Thus, the initiation of all of the duploseg- ments of the first field and node one in these peracarids are under a different, non-teloblastic control from that of the characteristic teloblastic control of the more posterior fields and nodes. Furthermore, this control is independent of whether the teloblasts are in front of or behind the blastopore, or even if there are teloblasts at all (as in amphipods.) A similar control to that seen in Crustacea is evident in Cheliceriformes (Table 3; Fig. 11), only in this case the possible gap mutation and forward shift is a synapomorphy for the entire subphylum. Cheliceriforms are characterised by an apparent lack of events in node one. The prosoma extends from the first field into the middle of the second field. It is duplomere 9 that is either the site where the gonopores are located, as in chelicerates sensu stricto, or where the abdomen begins, as in fossil and extant pyc- nogonids and the fossils Chasmataspis and Sanctacaris. It is possible that node one was completely deleted by a gap mutation in the ancestry of cheliceriforms, consequently pro- ducing an apparent shift forward of events out of node two into dy. Circumstantial support for such a gap mutation in the trunk region of A NEW APPROACH TO ARTHROPOD PHYLOGENY 11 Chilopoda Scolopendromorpha Field /node 2 E 3 ° 2 oa 3 3 mono-somite Otocryptopus sexspinosa Mn Diplopoda Polyxenus sp. Uniramia Diptera Pselaphognatha Drosophila melanogaster Mx T1 T2 T3 T4 Ts R= = T6 T7 T8 T9 "Zt Fer Field (g7i7] (7 Te TH 4 T12 T13 T14 T15 T16 T17 T1i8 T19 T20 T21 T22 T23 T24 T25 — = a | so ae a als ourth Be Field [46 | Bra 25st ee ae FIG. 10. Diagrammatic representations to illustrate some APT features of living uniramian body plans, with APT numeration to the left. Symbols as in Fig. 9. cheliceriforms might be sought in the cephalic region of these animals. Cheliceriforms are char- acterised by loss of the deutocerebral region of the brain, and we are tempted to suggest that the apomorphies of brain structure and tagmatisa- tion of this group of arthropods are related to some mutation(s) in the regulatory control of development that altered the patterns of ‘normal’ pattern expression by means of gaps in segment development. More typical pattern formation in cheliceriforms seems to prevail in the region posterior to do. In addition to the above animals, various prob- lematic fossil arthropods from the Burgess Shale and other localities appear to conform to APT (Table 4). The patterns among these fossils, compared to those in Tables 1, 2, and 3, lack information on the location of gonopores. In addition some confusion in interpretation arises related to shortcomings in the preservation of these fossils. An example of this is seen with the Cambrian arthropod Sidneyia. This animal has traditionally been interpreted as having a single segment head (Bruton, 1981; Gould,1989). Sid- 12 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. Segmental patterning in Uniramia with reference to fields and nodes. Geophilomorpha Scolopendromorpha Scutigeromorpha Lithobiomorpha Polydesmoidea Ascospermomorpha Juliformia Limacomorpha Colobognatha Oniscomorpha Pselaphognatha Symphyla Pauropoda Arthropleura * ?gp Insecta tx/abd Apterygota fe +eptrgGrerererer et teet a = anus, gp = gonopores, f = female, m = male, ? = unknown but predicted location, t = structure at terminus of region, dn = duplomere, X/Y = transition, + = segments present but otherwise undistinguished, — = portion of or whole region deleted, hd = head, tr = trunk, tx = thorax, abd = abdomen, * = extinct. TABLE 2. Segmental patterning in Crustacea with reference to fields and nodes, Nectiopoda Tesnusocaris Malacostraca Copepoda ¥ disa Mystacocarida . " diga Skara * g ? ta Ostracoda ° " diemgp,a Branchiura id - Ascothoracida ‘ ep,” diga Thoracica - be Lepidocaris * Anostracai Anostracaz Notostraca Conchostraca Cladocera Leptostraca Canadaspis * Cephalocarida * Odiegp ey ++ tte tte ett Abbreviations as in Table 1. ANEW APPROACH TO ARTHROPOD PHYLOGENY 13 Crustaces: Field Malacostraca inode Isopoda Ligia exotica Ay Ag ale/[2|=]=|_mono-somite | Pel] =] duplo-somite Calantica villosa Chelicerata: Maxillopoda Arachnida Thoracica Araneae Biphisteus desultor FIG. 11. Diagrammatic representations lo illustrate some APT features of some advanced crustaceans and chelicerate body plans, with APT numeration to the lefi. Symbals as in Fig. 9, neyia, however, has a rather subtle distinction of limbs that sets off a prosoma of four pairs of uniramous limbs posterior to the mouth from an opisthosoma with five sets of biramous limbs. This transition occurs in node one; the opistho- soma extends through the second field; and a short abdomen (or postabdomen) occupies node two. Under the traditional interpretation, Sid- neyia is notan APT animal; under our interpreta- lion it clearly is, While most of the known problematic arthro- pod genera do display APT motifs in some way, several fossils remain enigmatic. Given the cur- rent state of our knowledge about them, the following taxa do not appear to have any APT features: Burgessia, Marrella, Mimetaster, and Vachanisia. Whether this lack is real or merely due to an inadequacy in our knowledge about incompletely preserved fossils is not known, DISCUSSION In the last 150 years, numerous schemes to explain arthropod phylogeny have been put for- 14 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 3. Segmental patterning in Cheliceriformes with reference to fields and nodes. Sanctacaris * Palaeoisopus * Palaeopantopus* Pycnogonida Synxiphosura * Chasmataspis * Limulus Erypterida * Scorpionida Araneae Solifugae Opiliones Palpigradi Sternarthron * Uropygi Ricinulei Acarina Sy ee OR AP ge aege ae o pr = prosoma, op = opisthosoma, abbreviations otherwise as in Table 1. TABLE 4. Segmental patterning in various problematic fossil arthropods with reference to fields and nodes. Triarthrus Rhenops Naroia Olenoides Agnostus Yohoia Waptia Oxyuropoda Actaeus Alalcomenaeus Habelia Plenocaris Leanchoilea Emeraldella Molaria Sartrocercus Sidneyia Aglaspis Cheloniellon Abbreviations as in Table 1. begin legs begin tr ” hd/tr ” ++ ttteteeetet+ettetyey tr/py i: tx/ab seg. change + + + + leg change + ta ta abd. legs end seg. change ANEW APPROACH TO ARTHROPOD PHYLOGENY 1s ward, but no consensus has been achieved, Fur example, Workers have either focused on development (Anderson, 1973). ur morphology (Snodgrass, 1952; Manton, 1977: Gupta, (979), or tassils (Bergstrom, 1979, T980) and have developed explanations for arthroped evolution narrowly derived from those disciplines. The strength af APT is that it combines inlormation from all these fields of study into one coherent canon, A measure of the effectiveness of a theory ts its ability t) make predictions. Lulike other theo- ties about arthropod relationships, APT offers a predictive framework that attempts to proznos- licate information yet to be derived from future studies, For example, the discovery of a second sct of gonopores in nectiopodan remipedes (Ita and Schram, 1988) corroborated APT becuuse the location of the female gonopores in node Iwo was on the segments that APT predicts. Simi- larly, APT can be tested by seeking gonopares and/or other structural markers on Specific nodal segments on the bodies of the fossil taxa. as indicated in the tables, Another mark of a theory's strength ts how well it incorporales and reconciles apparently disparate clements of previous theories. For ex- ample, Snodgrass (1938) united the insect/myri- apod and crustacean lines as the Mandibulata. Manton (1964. 1977) disagreed with that posi- lion, arguing that mandibles were convergently developed in different arthropod groups. Man- ton’s work was seconded by Anderson (1973) who recogmsed what he felt were fundamentally different patterns of blastomere fates among the three major groups of living arthropods. Various authors (Gupta, 1979) have disagreed with Man- ton and Anderson. A preliminary and very lentative phenogram for arthropods based on APT assumptions (Fig. 12) reveals that these old theorics can cease their warring — all incorporate elements of “truth. The mandibulates, inthe sense of Snodgrass, can be recognized as 4 paraphyletic group near the base of the arthropod lineage, This arrangement accommodates the continuity of blastomere fates of uniramians extending to onychophorans snd chitellate annelids. The unique early ontogenetic patterns so effectively outlined by Anderson for crustaceans and cheliceriforms, can now be seen as autapomorphics for those groups. Mandibles appear to be convergently developed. in the sense of Manton (1964), but this can he accom- modaled within the concept of arthropod mono- phyly, in the sense of many authors in Gupta (1979), ‘The concepts uf Arachnomorpha (Stormer, 1944) and Schizoramia (Hessler and Newman, 1975) alsn have validity, and the posi- Honing of many Burgess Shale arthropods rela- tively high in the arthropod genealogy (Briggs and Fortey, 1989) deserves careful considera- ton, Figure 12 is not a cladogram but merely repre- sents al best a crude first guess of possible rela- liunships within the arthropods, A character matrix for APT features is being prepared. How this will translate into a specific cladogram for dplthropods must await the completion of that work. However, certain broad patterns can be discerned from the above analysis that prompt us woolfer (Pig, (2) a phylogram of arthropod types displaying the distribution of major APT charac- ters and other non-APT features, Essentially. the evolution of arthropods can be sect as a progres- sive serics of events from a diplomerous, uni- Tamous animal through to a fully duplomerous, biramous condition. Some uniramians, such as insects and geaphilomorph centipedes manifest a secondary monomery, and cheliceriforms (as wellas a few crustaceans) manifest a secondary uniramy, Nevertheless, the main thrust of arthra- pod evolution appears to have been focused on progressive control over duplication cycles (Minelli and Bortoletlo, 1987; Jacobs, 1990) such thatdiplormeres were fused to form duplony- eres, and diplo-and duplomeres-were genetically controlled as umit fields and nodes. The end point of this evoluGon was a developmental ane furictional system that allowed for more cffec- tive limb and tagmata specialisations (han were possible in less derived articulates such as an- nelids. A confirmation of sorts for the above scheme comes from the study of molecular sequence data. Among the most controversial analyses of molecular phylogeny is that of the 185 ribosomal RNA sequencing of Field et a/. (1988), wherein metazouns were viewed as polyphyletic, A re- analysis of that data, however, by Lake (1990) reveals a broad pattern of metazoan evolution that is more in accord with traditional interpreta- tions of animal history and a branching sequence for arthropods similar with what we suggest here (Fig. 12), In Lake's analysis, the myriapods and insecis are sister groups to the biramian arthro- pods in a transition series leading to a clade that includes annelids and molluscs, Lake feels the paraphyly of the arthrupods evident in his scheme ts nol strongly supported by the natore of the molecular data available, and that much 6 MEMOIRS OF THE QUEENSLAND MUSEUM Ww a at o £ = o <6 oO ay we v4 aA = 2 tS ow 23 ¢ n 5 € Bp og Bap ne £ s| & 2 o wu & S| fz 2 SS +n & = 26 Ssh ee 8S Se 2 2 ego #5 Sf 2 24 as a Sn > & S mee # 6 a Fea bz usieempus beaay occa monorery FIG, 12. Phenogram of possible arthroped relation- ships according to APT portraying the distribution of various APT and traditional characlers discussed in the text, more data are needed from a variety of arthro- pods before a more definitive answer can be obtained concerning the relationships of protos- tomes. However, his analysis does seem to siip- port both the idea of the uniramians as an carly offshoot of the arthropod lineage, as. we advocate here, and the close relationship of erustaccans and cheliceriforms, as suggested by Briggs and Fortey (1989) and by us. A species is neither completely derived nor completely primitive, each is a mosaic of fea- tures suited to the individual functional needs of that species. The challenge of phylogenetic stu- dies is to sort those features and arrive at same judgment of the relative significance of each. We have approached all arthropod characters with an open mind, and willingly entertained the un- thinkable by treating even old and long cstab- lished assumptions as if they were just newly formed hypotheses. Furthermore, we believe much is to be gained by bridging disparate ficlds of research in an attempt to find common pat- terns. A certain smugness has formed around the idea that fossils can never really make any sub- stantial contributions toward understanding phy- logeny, other than filling in the details of a particular group’s history. For example, Wilmer (1990: 76) bluntly stated, ‘Tt actually seems un- likely...that any one author’s view of metazoan phylogeny has ever been substantially formed, or substantially altered after formation, by refer- ence to the paleontological record.” In contrast. we feel that fossils can make a greai contribution towards understanding animal evolution, as they have in the present case, Furthermore, we cau- tion against too much reliance on the use of exclusive paths to ‘truth’, e.g. such as those represented by molecular data. All lines of re- Search are productive, but theories are not to be viewed as either entirely true or completely false. They are merely useful for a time in organizing, facts and indicating potentially informative lines of research (Wenner and Wells, 1990). ACKNOWLEDGEMENTS The manuscript was critically read by R.C. Brusca and J. Matthews, and J.M. 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MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum CRUSTACEAN EVOLUTIONARY EVENTS: SEQUENCES AND CONSEQUENCES K. G. MCKENZIE McKenzie, K.G. 1991 09 O1: Crustacean evolutionary events: sequences and con- sequences. Memoirs of the Queensland Museum 31: 19-38, Brisbane. ISSN 0079-8835. Crustacean evolution is visualised as proceeding through a space-time continuum in which the Red Queen and stasis have operated. Under these conditions, evolutionary bursts were fuelled by majorenvironmental changes following which the new diversities of1axa. having expanded into any newly available niches, returned to the Red Queen or stasis mode, Afler some polyphyly in the Cambrian, which remains poorly understood, the major radiations in Crustacea seem to conform to such a scenario, particularly from the Hercynian tectonic epoch onwards. Important events follawing this include the initiation of Tethys, Carboniferous—Permian glaciations, peats and coals, Pangaea, Triassic desertic conditions, Mesozoic Tethys, the Purbeckian—-Wealden, break-up of Gondwana, the Danian crisis, origin of the psychrosphere and Palaeogene Tethys, Paratethys, the Mediterranean Messi- nian event, the Central American filler. impingement of India against the Himalayas and of the Australian Block against the Indonesian arc, Pleistocene glaciations. [Mlustrations of the evolutionary effects for crustaceans are given mainly trom the Ostracoda, although examples from other taxa ate also cited. Consequently, after preliminary discussion of such factors as limitations in the fossil record and convergence, new event-triggered phylogenies are derived for the main crustacean classes, maxillopodans and Ostracoda. The role of humans in passive crustacean dispersal is analysed briefly, stressing the importance of history for a proper understanding of this phenomenon. [| Biogeography, palaeontology, evolution, Crustacea, Ostracoda, man. K,G. McKenzie, Geology Department, University af Melbourne, Victoria, Australia 3052; 6 July, 1990. The thesis that evolution is event-triggered is well on the way to becoming a new orthodoxy in evolutionary science. Citing Benson (1985: 35), ‘We are today in the middle of such a change: from the acceptance of continuity as a necessary and sufficient procedural assumption to a con- currence that interrupted stasis is an obvious condition of development.’ Later in the same book Fischer (1985, fig, 7-1) correlated biotic crises with cycles of climatic change, sea level variation and vulcanism for the entire Phanero- zoic (Cambrian—Recent). There is a further modal! constraint upon this paper. Van Valen (1973) propounded an evolu- lionary theory that all groups, ‘go extinctata rate that is constant for a given group’ even in a constant physical environment. This rationale goes under the attractive name of the Red Queen hypothesis- At the court of the Red Queen extinc- lion is inevitable, an entropic effect. Stenseth and Maynard Smith (1984) proposed an alternative hypothesis, that evolutionary stasis would be maintained until the physical environment was disturbed; then they demonstrated mathemati- cally that both the Red Queen and stasis were feasible. This combined mode! is more gener- alised than the Macarthur-Wilson equilibrium hypothesis, in which species number is a dy- namic equilibrium between immigrant taxa and those which become extinct (Webb, 1985), be- cause it allows for the development of new taxa in situ following environmental change and ex- tinction without necessitating stimulation of such evolution by immigrant competitors, al- though this is not excluded. Summarising, crustacean evolution is visu- alised as proceeding through an Barth space-time continuum in which the Red Queen and stasis have operated. Under these conditions, evolu- tionary bursts were fuelled by major en- vironmental changes after which the new diversities of taxa, having expanded into any newly available niches, returned to the Res Queen or stasis mode. The paper first briefly outlines the stratigraphy of crustacean evolution and the contemporary major environmental changes; then develops phylogenies based in the geological record; and finally cautions that pas- sive dispersal of some crustaceans by humiuns can distort biageographic (and any linked phy- logenetic) patterns. 20 MEMOIRS OF THE QUEENSLAND MUSEUM CRUSTACEAN EVOLUTION AND MAIOR ENVIRONMENTAL CHANGES (CAMBRIAN ‘The Cambrian Period is tnghly significant tor the evolution of life on Earth. Although several major groups had appeared in the Ediacaran (latest Precambrian), (heir distribution is patchy; first appearance of widespread, richly diverse and abundant fossils is generally a diagnostic feature of Cambrian sequences. Briggs and Por tey (1989), summarising the carly radiation and relationships of the major arthropodan taxa, pro- vide a cladogram which indicates that crustaceans and crustacean-like animals occupy a primitive position among early biramian ar- thropodans. Their data come [rom the Middle. Cambrian Burgess Shale fauna of British Columbia, Canada, which contains several possible crustaceans of uncertain affinities, in- cluding Waptia, Odaraia, Branchtocaris, Per- spicaris, Plenocaris and Canadaspis. All were extinct by the close of the Cambnan. Boxshall (1983) also refers to the crustacean-like (axa of the Burgess Shale and includes the barnacle-like Prisconsermarinus in his list, Confirmation that the latter is 4 barnacle requires the discovery and description of, ‘identifiable cirriped structures, such as cirri, within the capitulum.’ (Collins and Rudkin, 1981; 1011). Canadaspis was once regarded as the earliest phyllocarid (Briggs, 1978) but this view no longer prevails and Dah! (1987) even thinks that it may not be a crustacean, Similarly, Branchiocaris (Briggs. 1976) seems a plausible early branchiopo- dan but is separated in time from more pencrally- accepted fossil branchiopods by abuul 200 million years. Briggs (1983) is unconvinced of a crustacean affinity and is similarly critical of Waptia, Odaraia. Plenoearis and Perspicaris. Note that the mandible is unkriown for most of these taxa except Canadaspis and Branchio- caris, and that the Branetiecaris mandible is certainly non-crustacean (Briggs, 1976: 11—12), The other Cambrian fauna with major rele- vance for crustatean phylogeneticists is that of the bituminous limestone Orsten of Sweden, The Phosphatocopida (Moller, LY 79a), Skaracarnida (Miller and Walossek, 1985) and Orstenocarida (Miillerand Walossek, 1985) are all preserved jn such complete detail that their assignment to Maxillopoda can be sustained, OF these taxa, Skaracarida and Orstenocarida were apparently extinet by the end of the Cambrian but Phospha- tocopida lingered into the Early Ordovician and seem closely related to Bradoriida, both orders being referrable to the Subclass Ostracoda (Mad~ ducks, 1982; McKenzie, Miller and Gramm, |983). Bradoriids are the commonest, mast diverse and most ubundunt Cambrien crustaceans. They occur in Cambrian rocks al- most everywhere bul their geological succession and geographical distribution has been worked OWL most completely in China (Huo and Shu, 1985; Huo et al., 1989). Huo and Shu (1983, 1985) regard naupliine bradoriids as the earliest crustacean ancestors. The favourable environmental setting for this first evolutionary burst among crustaceans was due to the widespread marine transgression [hat followed a latest Preeambrian glacial epoch of continental emergence. Workers on all fossil groups concur that seas were epicontinental and relatively shallow. There was also a major global climatic change from cold in the earliest Cam- brian to warm in the remainder of the Period (Boucot and Gray, 1987; 33-36). ORDOVICIAN AND SILURIAN During the next two geological periods, the major crustacean diversifications took place among ostracades, Maddocks (1982; 227) notes, ‘This Ordovician burst of adaptive radiation of calcareous shelled types, nearsimultancous origin of the major post-Cambrian orders and rapid disappearance of Cambrian stocks is a common evolutionary pattem in many inverte- brate phyla” Thus, as Bradoniida and Phosphato- copida died out, Leperditicopida, Beyrichicopida, Podocopida, Platycopida and enlomozoacean Cladocopida all evolved. The Silurian saw the initiation of the Halocyprida via Entomoconchacea (Kormecker and Sohn, 19764). No definite Or- dovician Myodocopida are known although, if the phylogeny in Kornicker and Sohn (197hb) is correct, they would have split fram Cladocopida and Halocyprida before these evolved, The most characteristic Lower Palaeozoic groups, huw- ever, were Leperditicopida and Beyrichicopida. The former were an offshaot from the main lincages of ostracode evolution — their in- tralarmellar radial carapace structures are unique within the subclass (Sohn. 1974) — and they include the largest known ostracodes (Abushik, 1979); the latter very often are spectacularly-or- namented (Kesling, 1969). Indeed, Beyrichi- copida were the most abundant Ordovician (Sarv, 1972) and Silurian (Siveter, 1978) crustaceans. Their radiation during these periods was extremely complex, as the rapid evolution of numerous genera went hand in hand with almost equally numerous extinctions (Scott. CRUSTACEAN FVOLUTIONARY EVENTS 21 1961, figs 47, 65). Beyrichicopid systematics were long bedevilled by unrecognised homeo- morphies until Scandinavian workers estab- lished the crucial importance for their classification of sex dimorphic features (Schall- reuter, 1988). The role of homeomorphy in crustacean ¢volution is referred to again in the Discussion section of this paper, Equally important was evolution of the first phyllocarids, beginning in the Early Ordovician with the archaeostracan Ceratiocaris (Rolfe. 1969). The lower Palacazoic Archacostracu are regarded as part of the ancestral stock of all malacostracans by some workers (Dahl, 1987). The initiation of another maxillopodan sub- class occurred during the Late Silurian. Cy- prilepus holmi, of Estonia, was identified as a pedunculate cirriped by Wills (1963), Newman and Hessler (1989, fig, 5) derive the evolution of all Pedunculata and Sessilia from this ancestral! type. Finally, F. R. Schram illustrated a Silurian remipede during his talk at the conference. This is the carlicst known representative of the Re- mipedia, Environmental triggers to the evolution and radiations of as many as seven ostracode orders and Ceratiocaris surely included the widespread tectonism of the mid-Ordovician, Seas remained epicontinental and relatively shallow and ini- tially they were warm. There is evidence for glaciation in Arabia, northern and southern Africa, and South America, dated at near the Ordovician-Silurian boundary (Boucot and Gray, 1987, fig. 3). A good discussion is pro- vided by Fischer (1985). This geologically short- lived global cooling indicates more varied climates at the inter period boundary and was followed by mid-Silurian tectonism. DEVONIAN AND EARLY CARRONIFRROUS It could be convincingly argued that this was the most important geological interval for development of the main crustaccan stocks. The first shrimp-like decapods. — Palaeapalaeman — evolved then (Sturgeon ef al, 1964). Other Devonian malacostracans were no less remarka- ble, including Focaris and Devonacaris of un- certain affinities and the first palaeostomatopod hoplocarids (Brooks, 1969, fig. 157); also 21 genera of archacostracan phyllocarids (Rolfe, 1969, fig. 122), such as Echinacaris (Sturgeon et al., 1964) and Nahecaris. (Bergstrom et al. 1987). The record for olher crustacean classes was even more potewerthy. The first Branchiopoda appeared, via the Spinicaudaja and Lipostraca (note however that Schram has recently il- Justrated a possible Silurian anostracan). Spini- caudata are conchostracans; and they entered the geological record represented by 4 families (Tasch, 1969), Lipostraca were primitive anos- tracgns (Scourfield, 1926), Additionally, acrothoracic barnacles evolved (Trypetesa). The most abundant and diverse Devonian crustaceans, however, remained the Ostracoda, and numerous very rich [unas have been de- scribed (Pokorny, 1950; Becker and Bless, 1974; Tschigova, L967; Jones, 1968; Polenova, 1968. 1974; Adamezak, 1968, 1976; Kesling and Chil- man, 1978: Becker, 1988), While beyrichicopids still dominated, there were also many podo- copids, platycopids and myodocopids; and 15 genera of leperditicopids (Abushik, 1979; Jean Berdan, per. comm. 1981) although the Order became extinct by the Carboniferous. This was also the time for diversification in entomacon- chacean hslocyprids (Kesling, 1954) and for the major radiation in entomozoacean cladocopids (Gruendel, 1962; Gooday, 1978). Devonian climates are summarised in Boucot and Gray (1987: 38-43, figs 6-8) and a plausible palaeogcography is given by Rickard and Belbin (1980), Peats, red beds and marginal marine evaporites were typical on Jand and near the shoreline. Seas were epicontinental and mainly shallow, but reached basinal depths in regions characterised by the Thuringia-facies the most complete discussion of which is given by McKenzie (1987) who cites important prior ref- erences. The general tectonics of the Hercynian epoch are outlined by Carey (1987). Some idea ol the complexity of the movements is given in the team project on the Omolon region, Siberia (Simakov er a/., 1983), li seems that provinesal- ism characterised the Early Devonian whereas Laje Devonian faunas were more widespread. Steiner (1967) linked the mid-Devonian biotic crisis to the dynamics of the Milky Way galaxy; for Fischer (1985) astronomical factors have neither the amplitude nor the frequency lo ac- count satisfactorily for the faunal changes which he believes were. response to a major reversal in climatic cycle, from ‘greenhouse’ to *iee- house stale (Fischer, 1985, fig. 7-1), Note, haw- ever, that the teetonic setting overlapped into the Carboniferous, terminating with the definitive establishment of Tethys, Reappraising the crustacean faunas of the Devonian, it is evident that the radiations and intliatiuns in milacastracans (Phyllocarida, Ha- 22 MEMOIRS OF THE QUEENSLAND MUSEUM plocurida, Decapoda), branchiopods (Spinicau- data, Lipostraca) and Ostracoda can all be ex- plained as triggered by the mid-Devonian crisis. By its close, the Lipostraca apparently had vanished from the geological record. On the other hand, the Early Carboniferous heralded further initiations of major crustacean groups, among them the important remipede Tesnusocaris (Schram and Emerson, 1986). Malacostracan initiations were primitive hoplo- caridan animals (Crangopsis), pygocephalo- morphs (Tealliocaris, Pseudotealliocaris), anthracocandomorph tanaidaceans (Aniiraco- caris), primilive spelaeogriphaceans (Acadio- curis), as well as palaeocaridacean ancestors of the Syncarida (Brooks, 1969, fig. 157; Briggs and Clarkson, 1985; Schram e: al, 1986; Schram, 1984, 1988). Branchiopoda were repre- sented by the earliest Notostraca as well as by spinicaudate conchostracans; pedunculate bar- nacles by Praelepas; ositacode initiations in- cluded cyprellid and rhombinid myodocopids, and the Darwinulacopina (Sohn, 1988). Environments and facies of the Early Car- boniferous have been exhaustively studied. ‘The malacostracan fossils were preserved in shore- line, Uidal flat, brackish-marine, deltaic and near- shore freshwater lake habitats, including coaley and apatite-rich facies (Briggs and Clarkson, 1983, 1988), Many Ostracoda also have been described from similar facies (Bless, 1973, 1983; Bless and Massa 1988; Jones 1989). Further offshore, Thuringia-type faunas persisted (Devolvé and Lethiers, 1986), During the bot and humid climates of the time. limnic basins of thalassogenic type were wide- spread especially in northern continental areas, Ostracoda, in particular, were quick to exploit such niches via a number of families; typical genera included Geisina, Carbonita, Whiplella, Darwinula and Tomiella (Carbone er al, 1988, fig. 25). Their assemblages, and those of the conlemporary conchostracans, were the earlies! widespread continental crustacean faunas. LATER CARHONIFEROUS, PERMIAN AND TRIASSIC The profound changes in crustuccan faunas during the later Carboniferous, Permian and Tri- assic were welltypified by ostracodes. Al the end of the Carboniferous, the following marine groups were extine: beyrichiacean beyrichi- copids: Entomozoacea and Entomocanchacva; the myodecopid families Cyprellidae, Cyprid- inellidae and Rhombinidae; Eridostraca, and Leperditicopida. The Perma-Triassic marine ex- tinctions included Beyrichicopida which had dominated for most of the Palaeozoic, and also the kloedenellocopine platycopids. On land, the crisis was ¢ven more severe with only Dar- winula and one cytheracean genus surviving into the mid-Triassic, Other apparent victims of this series of major biotic crises were palaeocaridacean syncarids, trypetesid barnacles, Acadiocaris, the tremipedes Tesnusocaris and Cryptocaris, and anthraco- catidomorph tanaidaceans such as Bucrypto- caris. But the lineal descendants of these taxa continued fo evolve. Thus, although the earliest isopod ts a Carboniferous phreatoicoid the next fossils. in this group do not appear until the Jurassic. The initiations and radiations were jusi us im- portant. For Ostracoda, there were marine radia- tions in Bairdiacea (Kristan-Tollmann, 1970), 1971; Bolz, 1971) and Healdiacea, and evolution of the family Glorianellidac in brackish environ- ments (Grucndel, 1978); ulso polycopacean cladocopids, thaumutoeypridacean halacyprids and cytherellocopine platyeopids (Gramm, 1968; Kornicker and Sohn, 19762), On land, Darwinulocopina were still widespread but the faunas also included representatives of 10 non- darwinulacopine families and by, ‘the end of the Late Permian, freshwater ostracode associations reached maximum species diversity and geo- graphic differentiation for the Palaeozoic’ (Car- bonel er al,, 1988: 452). Other crustacean initiations during the Per- mian included penacid and astacid Decapoda, cumaceans, stypocaridacean syncarids (Clarke- certs), and perhaps the first leptostracan phyllo- carids (Brooks, 1969; Ralfe. 1969; Glaessner, 1964), The Triassic was marked by the first appearances of mysids, syncaridacean syn- carids, zapfellid acrothoracican bamacles, and glypheoid and eryonoid Decapoda. Several major palacogeographic and climatic changes were associated with these faunal Jevelopments. The continents coalesced form- ing Pangaea, its two main landmasses, Laurasia and Gondwana, being separated by a dominantly shallow Tethys. There was some mid-Cur- boniferous lectonism. Climates were glacial at higher latitades during the Carboniferous—Per- mian nadir of the ‘icchouse state’ cycle (Fischer, 1985, fig, 7-1), but warm and humid in the trop- ics, During the Permian, the continents emerged and there was. 4 salinity ¢risis in the mainly epicontinental seas. Towards the close of the Triassic, on the other hand, although the world CRUSTACEAN EVOLUTIONARY EVENTS had warmed up again, climates were desertic not humid. In marine habitals generally, ostracodes te- mained the dominant crustacean group in the tater Carboniferous and Permian, and were ex- cellent environmental indices in the generally shallow continental shelf seas (Mclynk and Maddocks, 1988; Costunzo and Kaesler, 1987: Bless, 1987); however, Kozur (pers. comm,, 1989) insists on the cecurrence of some tric deepwater facies (deeper than mesubathyal) in the Middle—Late Permian of Tethys. During the Triassic. many Tcthyan facics and faunas were cosmopolitan from Europe through to Asia and even the Americas (Kristan- Tollmann ef al, 1987; Sohn, 1987, Kristan- Tollmann, 1988). Niche-diversification was particularly marked on land, where brackish, Iteshwater and miner- alised lakes were all common, cach with charac- teristic faunas, This. provided opportunities tor many entrepreneurial groups, notably including syncarids and Notocostraca, although the com- monest assemblages by far consisted of spini- caudate conchostracans or ostracodes. By the mid-Triassic many of these ostracodes, (Car- bonel et @/,, 1988, fig. 27) and also the verlexiid Spinicaudata (Tasch, 1969) had died out, pre- sumably victims of the change lo desertic cli- mates. But Kazacharthra (Chen and Zhou, 1985) first appeared in the Late Triassic, JURASSIC AND CRETACEOUS Crustacean diversity in the Jufassie and Cretaceous was cunsiderable in all mayor taxa and in all aquatic environments, continental as well as marine. Thus, in the Jurassic six more decapod superfamilies became established (Glaessner, 1969), along with numerous pedun- culate barnacles (Newman, Zullo and Withers, 1969, table 2), rodgerellid Thoracica; and ap- seudomorph tanaidaceans. Verrucamorph. brachylepadomorph and balanomorph sessile barnacles radiated in the Late Jurassic-Early Cretaceous, but many lepadomorph genera also became extinct in the Jurassic and by the end of the Cretaceous. The Early Cretaccous saw the evolution of tanaidomorph janaidaceans (Schram et al., 1986); and the oldest fossil copepod has been identificd from the Early Cretaceous of Brazil. Ascothoracida (Fadosac- culus) evolved in (he Late Cretaceous. Evolutionary peaks, in what has been called the Mesozoic explosion of the ostracode Cyther- acea, characterised the mid-Jurassic, mid- > ae m t Cretaceous and Late Cretaceous (Whatley and Stephens, 1975). Their initiations and extine- tions clearly express a Red Queen evolutionary pattern (Oertli, 1985, tables 5,6,8). Other initia- lions include the first Macrocyprididae (Mad- docks, 1990), Sigilliacea (Szczechura and Blaszyk, L968); and Punciacea (Herrig, 1988). The Mesozoic—Tertiary distribution via Tethys and Gondwana of entocytherid parasites is linked to the fossil history of their host taxa — phreatoicoids, cirolanids, sphaeromids, gam- manideans. ustacids, parastacids and potamids (McKenvie, 1973). Continental interiors were characterised by large lake systems (including saline lakes) in tectonic depressions and intermontane basins, as in China (Chen, 1987). Darwinule and limnocy- therid cytheraceans were widespread carlier, but by the Purbeckian—Wealdean epoch of allernul- ing (tansgression/tegression cypridaceans had tuken over (Anderson, 1971; Colin and Daniclopol, 1979, 1980; Ye, 1984; Su, 1987). However, most of the characteristic genera of this first continental cypridacean radiation were shori-lived, With respect to canchostracans, {he spinicaudate familics Estheriellidae, Ip- silontidae and Asmussiidae all died out in the Cretaccous but this was balanced by evolution of the order Luevicuudata, World climates were in their ‘greenhouse’ phase according to Fischer (1985, fig. 7-1). Thus, it was generally warm to hot and humid everywhere until the close of the Cretaceous. Valeanic activ- ity peaked in the mid-Cretaceous. High sea- levels characterised the mid-Jurassic, mid-Cretaceous and Late Cretaceous. The mid: Jurassic black marls indicate relatively deep epi- continental marine basins, with Liasina and metacope ostracodes (Oertli, 1963). Summaris ing the Cretaceous history of Africa, Reyment and Dingle (1987) recorded that rifting to open the South Atlantic began in the Late Jurassic bul there were still connections in the Brazil—west Africa region until the mid-Cretaceous as shown by many common astracodes (Malz, 1980), Then the break-up of Gondwana, and provincialism in the Southern Hemisphere, initiated. Marine environments were dominated by the classic Tethys of Suess (1893) which is a mid-Me- sozoic phenomenon, The analysis in McKenzie (1987) demonstrates that Tethys was not broad and uniform, as supposed by some palaeocartographers, but comprised wide continental shelves and siti. ous intervening usually epibathyal deepwater fa- cies, plus some small confined basins. [1 was M4 MEMOIRS OF THE QUEENSLAND MUSEUM affecled by leclono-custatic variations In sca level which were more or less marked according as they were in or out of phase with crustal movements (Reyment and Bengtson, 1955). Thus, along the southem flank of Tethys in northern Africa and the Middle East, Jurassic— Cretaceous facies were transitional from fresh- water to mineralised sabkha to brackish to shallow marine (including bituminous basinal marts) in phase with tectonism and eustasy. Os- iracoda are reliable palacoenvironmental indices (Damotte et af, 1987; Majoran, 1989; Basha, 1985; Rosenfeld and Raab, 1974, 1984; Honig- stein e¢ af., 1989; Al-Abdul-Razzaq and Grosdidier, 1981; Al-Furaih, 1980), The con- temporary deeper-water basinal facies which covered, for example, much of France by the mid-Cretaceuus (Oecertl), 1985) indicate com- mencement ofa change in Tethys, from epiconti- nental to truly oceanic. The tectono-eustatic transgressions of the Cretaceous were well-marked clsewhere in the world, notably in Africa, Australia and the Americas, The characteristic crustaceans of their fossil faunas were usually ostracodes (Dingle, 1984, Kroemmelbein, 1975; Hazel and Brouwers, 1982; Bertels, 19735) or barnacles (Newman and Hessler, LY89) allhough many Late Cretaceous decapod-rich zones oceur in the United States (Bishop. 1987}. Wholesale extinctions that devastated many groups of animals marked the Mesozoic—Ceno- 2oic boundary. The classic study of thisevent has noted a major species level change in Ostracoda and the extinction of numerous marine barnacles (Kaufmann, 1985: 191); many decapod genera also died out (Glacssner, 1964. fig. 251). The enviranmental mode! praposed {6 account for this envisages a major custatic sca level rise associated with active tectonism accompanied by climatic warming during the earlicr Late Cretaceous, followed by sudden and widespread oxygen-depletion in the oceans and marine temperature decline during the Danian; several other possible causes are also discussed, includ- ing an extraterrestrial iridium-rich event (Kauf- mann, 1985). Cenoear The Cretaceous decimations paved the way far development of the modern Crustacea. This. is well brought oul by the suprageneric taxa of Decapoda; Glaessner (1969, Fig. 251) shows that 32 of SL surviving families evolyed in the Tertlary—Recen\. Barnacle genera with fossil re- cords tell ite same story; Newman, Zullo and Withers (1969, table 2) show that 38 of 62 genera evolved in the Tertiary-Recent, and that 27 of these were balanomorphs. For Ostracoda, the Aquitaine Basin, France (McKenzie e¢/ al., 1979) has over 1100 Tertiary—Recent specics; and of the more than 200 genera less than 10% have Cretaceous or earlier records, The initiations of new major groups include 4 of the extant branchiopod orders (Fryer, 1957), There were important adaptive radiations in Copepoda, Isopoda, brachyuran Decapoda and, probably, Amphipoda. Bui many groups have no appreciable fossil record: including Ctenopoda, Onychopoda and Haplopoda (cladocerans); Mystacocarida; Cephalocarida; several orders of Copepoda; Branchiura; Rhizocephala; Bathy- nellacea; Thermosbaenucea; Euphausiacea; and Tantulocarida, This will be discussed below. The Cenozoic also saw important extinctions, among them the rodgercllid and zapfellid As- cothoracica. Further, 26 ostracode genera had disappeared trom the Aquitaine Basin by tne end of the Tertiary (McKenzie e¢ al., 1979: 140). The environmental triggers to such develop- ments had various tectonic, eustatic and climatic components. Very important among these was the origin of the psychrosphere, The estab- lishment of regions of abyssal and greater depths, that is the realm of true oceans, had probably begun in the mid-Cretaceous but the carliest psychrospheric oslracode assemblages have been dated as Eocene, based on Deep Sea Drilling Project cores (Benson, 1975). McKenzie (1987) considered that the ubiquity af new and specialised deep sca ostracode taxa was an indication of the comparative recency of this niche. The figures far crustaceans of the hadal zone are interesting from this point of view. Table 1 has been abstracted from Belvacy (1989). It shows thal by far the largest number of crustaceans living in this deepest zone belong to comparatively young groups such as the [sopoda and Amphipoda, Even in the older groups mest hadal species represent geologically young taxa. e.g. 6 ostracode Conchoecidae (Late Cretacgous— Recent 10 cimpede Scalpellidae, of which genera with fossil records date from the Late Cretaceous or Eocene, and 20 species. of the Recent tan- aidaceun suborder Neotamisomorpha (Belyaey, 1989), During much of the Palaeogene and until the mid-Miocene, Tethys was a world-encompiss- ing ecean in low latitudes that was psy- chrospheric at depth; across its entire extent CRUSTACEAN EVOLUTIONARY EVENTS 25 TABLE 1. Hada] Crustacea (cf. Belyaev, 1989). Tanaidacea Isopoda Amphipoda 57 (20 Neotanaidomorpha oastracode assemblages contained numerous common genera (McKenzie, 1967). Tectonic pulses in the Middle East closed off western Tethys from the Indo-Pacific in the mid-Mio- vene. Two related events then had considerable impact upon Mediterranean faunas (Roegl and Steininger, 1984). First came the establishment of Paratethys and its sometimes linked some- times separate component basins with their highly characteristic ostracode faunas (Pokorny, 1952; Stancheva, 1965; Sheidayeva-Kulieva, 1966; Krstic, 1971; Sokac, 1971; Yassini, 1987) which exhibited an almost 100% turnover as hasinal salinities alternated between marine. brackish and fresh in phase with tectonism and eustasy (Table 2}. Destructive in a faunal sense was the Messinian (Late Miocene) crisis during which the Mediterranean dried out and thick beds of gypsum were deposited — an index for this epoch is the Paratethyan curyhaline ostra- code Cyprideis pannonica. Asa result, when the ncean refilled in the Pliocene, faunas were re- placed from the Atlantic. For crustaceans, the consequences were twofold. Firstly, modern Mediterranean species have almost no links with Indopacific faunas except for a few relicts, and some Lessepsian migrants (Por, 1971) via the Suez Canal filter. Secondly, because of the Gi- braltar Sill only shallow-adapted Pliocene spe- TABLE 2. Ostracode assemblages of the Paratethys in northwest Bulgaria (Stancheva, 1965), showing a near-complete faunal turnover in the same busin al each Stage boundary, subspecies next older Stage | Macotian | 703) | ot | Sarmaiian | 199) | 2 | Badenian | sty) | Sal cies entered from the Atlantic. thus the Mediter- ranean deepwater ostracode fauna differs from that of other older oceans (Bonaduce e/ al., 1983), In the Indo-West Pacific, an important tectonic event was the impingement of the Australian Block against the Indonesian Arc. Unlike the earlier suturing of India with the Himalayas (which closed off a former marine corridor), this event led to faunal mixing and a new burst of marine speciation. McKenzie (1981, 1986) believes that evolution of the ostracode Sub- family Renaudcyprinae and many island assem- blages in the southwest Pacific have resulted as responses to the complex Neogene regional tec- tonics. On the other hand, Newman (1986) ascribes the development of the barnacle fauna of the jsolated Hawaiian Archipelago to long range chance dispersal during and since the Neo- pene. At the western end of Tethys, a critical Neo- gene event was the emergence of the Isthmus of Panama which closed off the Caribbean and Gulf of Mexica from the Pacific seaboard of the Americas. Cronin (1985) and Cronin and Sehmidi (1988) have discussed evolution in the ostracode genera Puriana and Orionina as. an effect of this event, On land, apart from Paratethys, large Cenazaic basins characterised by variable salinities are known from the Amazon region (Purper, 1979; Purper and Pinto, 1985) and China (Yang et a/., 1988), But the most important events were the glaciations of the Pleistocene Epoch. Glaciers covered much of North America, Europe and Asia wiping out all bul a few relictua) faunas. The reoccupation of these niches, following the last retreat of the ice sheets about 11,000 years ago, has been effected especially by partheno- genetic taxa, On other continents, endemism characterises the continental aquatic and also the terrestrial crustacean faunas. This is scarcely surprising piven the long isolation of South America, south Africa, India and Australia from the northern Palaearctic and Nearctic provinces. Thus, Australia has mainly endemic faunas of anostracans, anaspidaceans, phreatoicoids, and calanoid copepods as well as osiracodes, DISCUSSION The detail provided in the foregoing section is clearly sufficient to sustain the thesis that evalis tion is event-triggered. Evidently, the first evo- lutionary burst of Crustacea occurred in 26 MEMOIRS OF THE QUEENSLAND MUSEUM pre-Tethyan early Palaeozoic seas; the second main episode was associated with shallow Tethys, Pangaca, and then the Laurasia and Gondwana landmasses (late Middie Devonian to Middle Cretaceous); while the third main epi- sode relates to the evolution of deep, psy- chrospheric modern aceans and present continental assemblies, beginning around the middle Cretaceous (McKenzie, 1987, 1989).The data are biassed towards Ostracoda because they are the most abundant crustacean fossils. Two recent bibliographies (Kempf, 1980, 1988), both incomplete at their dates of publication by about 10% according to the author, list nearly 5100 taxonomic papers, The preponderance of these papers refer to fossil species. Numbers of de- scribed fossil Ostracoda are not known with certainty butuare in any case over 30,000 and increase by several hundred species a yeur. For many reasons, some of which are dis- cussed briefly below, it is difficult to specify a typical crustacean facies. Nevertheless, the dis- linctiveness of the phylum is generally acknow- ledged, This consensus is due primarily to the work of Manton (1973) who characterised crustaceans as distinct from Chelicerata, Trilo- bitaand Unitamia, Her assessment was vindi- cated on embryological grounds by Anderson (1973), The observation has already been made thal some Recent crustacean orders ate not repre- sented in the fossil record, There are a variety of Teasons for this, most commonly that many groups have a wholly soft anatomy which would not be likely to fossilise except under specially favourable condilions. Other reasons include small size; unsuitable niches such as ephemeral ponds, leaf litters and caves; and inapposile hab- us of life such as the parasitism of rhizo- cephalans, branchiurans and some copepods. Nevertheless, it is not difficult to make rea- sonable statements on the evolution of such taxa based on their morphology, habits and palaeobi- ogeography. Thus, none of the branchiopod orders once classed together as cladocerans are likely to predate the Early Cretaceous, Ha- plopoda (only one genus — Leptodora) are highly specialised marine planktic predators with a restricted Holarctic distribution (Fryer. 1987). Given that the present world ocean with its characteristic psychrosphere only initiated in the mid-Cretaceous and that there was a virtually complete turnover in oceanic plankton during the Cretaceous mass extinctions and, further, the extent of the Pleistocene ice sheets, it is unlikely that Leptodora initiated much before the later Neogene. Similarly, Onychopoda are repre- sented by few genera and although marine spe- cies are distributed worldwide the freshwater Species are Holarctic. Onychopoda are also char- acterised by a Ponto-Caspian radiation of en- demic species (Fryer, 1987). Thus, their evolution possibly correlated with that of Para- igthys in the mid-Miocene, Ctenopoda and Ano- mopoda are certainly older and, for the latter group, fossils are known from the Oligocene and Early Cretaceous (Fryer, 1987; Jell and Duncan, 1986) — Fryer (1987) does not accept the Per- mian fossils described by Smirnov (1970) as anomopodans, Both groups are freshwater in origin. The numerous records of fossil fresh- waler ostracodes and conchostracans from every type of continental habitat make it unreasonable to claim that Ctenopoda and Anomopoda could have evolved much before the earliest accepted anomopodan fossils. Most evolutionists would agree with these conclusions since cladaccrans are generally regarded as neotenic. As further examples, the austral biogeography of the branchiuran Dolops and some continental calanoid copepods suggests that they probably evolved on Gondwana before it fragmemted, ic. before the mid-Cretaccous; but no phylogeny that lam aware of regards these groups as ances- tral maxillopodans. Finally, but importantly, Cephalocarida (Sanders, 1963; Hessler, 1964) also have no appreciable fossil record. Their biogeography indicates wide distribution from the Americas to Asia and New Zealand, always in nearshore marine environments, This suggests that cephalocarids were dispersed via Tethys. They probably initiated prior to the mid- Cretaceous evolution of the intervening Atlantic but after the Late Devonian—Early Carbonifer- ous, because cephalocarid fossils have not been reported from the many suitable Tethyan and other nearshore facies of this interval that would have favoured their preservation if present, The fossil record has much more use for crustacean evolution than the simple provision of initiation times. It also demonstrates clearly That in many groups initiation is soon followed by an adaptive radiation; and as often as nota Red Queen pattern of extinctions follows this phase of diversification. Fig, 1 provides ex- amples from barnacles, decapods and ostra- codes. Further, itcommonly happens inthe fossil record that only one or a few taxa belonging to some particular group survive through a major biotic crisis and this survivor or survivor group CRUSTACEAN EVOLUTIONARY EVENTS 27 may then embark upon a new adaptive radiation or else stagnate in an evolutionary sense. The continental ostracode Darwinula is an excellent example. It evolved in the Carboniferous, radiated and diversified into several genera and even families by the end of the Permian, was the sole survivor of this darwinulocopine diversity after the Permo-Triassic extinctions, stagnated through the Mesozoic and most of the Cenozoic, but may now be at the threshhold of a new adaptive radiation as it is relatively species-rich and virtually euryoecious in modern continental environments and has given off the genus Micro- darwinula (Danielopol, 1968). The fossil record also has examples of groups which became es- tablished early and have maintained a relatively limited diversity ever since. The longest surviv- ing examples of this pattern are the Remipedia; further, the notostracans Triops and Lepidurus had split off from each other by the Triassic and have remained species-poor but persistent since then. A third pattern in the record is that in which a group initiates and then rapidly becomes ex- tinct. A good example is provided by Kazachar- thra (Late Triassic—Early Jurassic). Very useful in the study of evolution is the principle of reductionism, termed oligomerisa- tion by crustacean workers. When we look, for example, at the multi-seg- mented and highly spinose limbs of the Cam- brian maxillopodan orders Phosphatocopida, Skaracarida and Orstenocarida and compare them with the same limbs in podocopid ostra- codes, cephalocarids, and copepods, the modern groups are obviously oligomerised respective to the Cambrian taxa. Exploitation of this principle, however, forms the basis of much crustacean arboriculture (to borrow D.T. Anderson’s felici- tous term). On the other hand, the multiple instances of convergence (or homeomorphy) in all crustacean groups are often very difficult to deal with phylogenetically, as all workers appreciate. Less appreciated are instances of anhomeomor- phy, i.e. of dissimilarities which separate taxa that in reality are monophyletic. Thus, the com- mon characters which formerly united cladocer- ans now have been exposed as instances of convergence between four distinct orders (Fryer, 1987). But the anhomeomorphies between Spinicaudata and Laevicaudata (conchostra- cans) as elucidated by Fryer (1987) should not obscure the stem monophyletic relationship be- tween these two branchiopod orders; the fossil record indicates that Laevicaudata split off from some Spinicaudata in the Early Cretaceous. Permian | | Ordovician unl A Cc FIG. 1. A, normal radiation and Red Queen evalu- tion/extinction in genera of Ordovician to Permian ostracodes, superfamily Drepanellacea (Scott, 1961). B, radiation, Red Queen evolution/extinction and stasis in families and genera of Silurian to Recent barnacles, Lepadomorpha (Newmanetal., 1969). C, radiation and stasis in families of Jurassic to Recent decapods, Brachyura (Glaessner, 1969). Also difficult to cope with is the common occurrence of neoteny, mentioned earlier with respect to cladocerans. The recent description of a punciacean ostracode, Manawa staceyi, sug- gests that it too has several neotenic features to go with its highly-oligomerised chaetotaxy, in- cluding a shallow dome-like univalve in early ontogeny (Swanson, 1989). A further factor which contributes to the com- plexity of elucidating crustacean evolution is the 28 MEMOIRS OF THE QUEENSLAND MUSEUM frequency of mosaic evolution. This is rarely emphasised nowadays in crustacean studies al- though it is a characteristic phase in the evolution of numerous groups (Colin and Danielopol, 1980). Every crustacean is a melange of primitive and derived characters. While this truth is not re- stricted to living taxa it leads to considerable difficulties in arriving at a plausible phylogeny on the basis solely of the Recent fauna. The problem was well aired by Dahl (1963: 13-15, figs 1,2) who warned that the main lines of phylogenies were conjectural,‘for at present we possess no actual evidence demonstrating any case of a group at subclass or higher level being derived from another group.’ (Dahl, 1963 : 13). The value of the punctuational equilibria hy- pothesis in this context lies in the fact that we would anticipate that aspect of phylogeny. On the other hand, constant reference to the fossil record enables the building of a tentative basic phylogeny that is anchored in geological time tather than in a cladistics which ignores this crucial restraint. The reasoning followed in developing a time-oriented phylogeny for Crustacea can be illustrated by reference to two fundamental crustacean characters, the carapace (or headshield) and the antennule. There are only two arguments against the primitive nature of the crustacean cephalic shield. Firstly, some Cambrian fossils which seem to have crustacean affinities lack one, e.g. Yohoia. Considerable new evidence would have to be uncovered before this argument could be sustained. Thus, in Briggs and Fortey (1989, fig. 1), Yohoia lies between the chelicerate-like ani- mals and the trilobites; and all the crustacean- like Cambrian fossils in their cladogram have a well-defined cephalic shield. Parenthetically, these mid-Cambrian crustacean-like taxa seem a polyphyletic cluster; their precise relationships to each other and to Crustacea remaining poorly understood. The second argument contends that Cambrian crustaceans lacking a cephalic shield have not been preserved. This argument fails because the two best known apposite Cambrian faunas, those of the Burgess Shale and the Or- sten, are found in deposits that are highly- favourable to the preservation of soft anatomies: if such forms were present they surely would have been found by now. Further detailed discus- sion on the carapace is provided in Jones and McKenzie (1980). My position with regard to the crustacean antennule is more controversial. Crustaceans have three types of antennule: uniramous, biramous and triramous. Uniramous antennules are typical of Maxillopoda and Branchiopoda; biramous antennules occur in the phyllocarids, eumalacostracans and Remipedia; triramous antennules feature in Hoplocarida. Kunze (1983) proposed recently that, ‘ Hoplocarida and Eumalacostraca evolved independently from separate “phyllocarid-like” ancestors.’ The triramous hoplocarid antennule is a key apomor- phy in her analysis. Recapping, the earliest fossils assigned to Hoplo- carida are Devonian palaeostomatopods. The ear- liest maxillopodans are Cambrian Bradoriida, Phosphatocopida, Skaracarida and Orstenocarida. The oldest-known definite phyllocarids are Or- dovician, but a Cambrian origin for the group is probable. The oldest remipede has a Silurian age; the earliest Eumalacostraca are Devonian. Adap- tive radiations shortly after their evolution certainly characterise the Bradoriida, Phosphatocopida, Phyllocarida and Eumalacostraca. The Skara- carida and Orstenocarida seem short-lived Cam- brian groups. The Remipedia represent the pattern of a long-surviving group with limited numbers. The simplest phylogenetic pathway that is con- sistent with this record suggests that the ancestral forms were Early Cambrian bradoriid maxillopo- dans with an uniramous antennule. Phyllocarids (biramous antennule) branched off in the mid- Cambrian, possibly from bradoriids of the suborder Abdomina (Huo and Shu, 1983). In the Devonian, Branchiopoda (uniramous antennule) split off from the Maxillopoda; but Eumalacostraca (biramous antennule) and Hoplocarida (triramous antennule) diverged separately from phyllocaridan stock (Kunze, 1983). Remipedia (biramous antennule) evolved in the Silurian or earlier, possibly from phyllocarid-like taxa. Cephalocarida (uniramous antennule) may have initiated in post-Permian Tethys as discussed previously, splitting off from as yet unknown branchiopod-like forms (Fig. 2). As a systematic exercise, it elevates Hoplocarida to the same subclass status as Eumalacostraca and Phyllocarida; but Maxillopoda, Remipedia and Branchiopoda retain their rank as classes. Note that subclass and class divergences are attuned to major Palaeozoic events. Given this groundplan, the subdivision of classes and subclasses can proceed under similar chorological and event-triggered constraints. Remipedia are a small group whose biogeogra- phy and subsequent evolution was crucially in- fluenced by the mid-Cretaceous separation of Africa from the Americas (Schram and Emerson, CRUSTACEAN EYOLUTIGNARY EVENTS Em Ho (athoaneious Devonian Silunan Ordovieiin Permian Curbontterous Devonian Silurian, Undovician Cambrian FIG, 2, A, phylogeny of Maxillopoda (Ma). Hoplo- carida (Ho). Eurnalacostraca (Em), Remipedia (Re) and Phyllocarida (Py) from an origin in bradoriid Ostracoda (Ob). B, phylogeny of Maxillopoda (Ma), Cephalocarida (Ce) and Branchiopoda (Br) from an origin in bradoriid Ostracoda (Ob). 1986, lower figure, p. 17). Interrelationships of the orders of Branchiopoda will be published by Fryer; but neither the evolution of Anostraca from Lipostraca, Kazacharthra from Notostraca and Laevicaudata from Spinicaudata nor the timings of these events seem much in dispute. The evolution and relationships of the families of Hoplocarida seem well understood, those of Phyllocarida and Eumalacostraca less so, but all three are beyond my expertise. This leaves Max- illopoda. Maxillopoda were originally defined by Dahl (1956) to include Mystacocarida, Copepoda. Branchiura and Citripedia. Later, the class was redefined to include also Ostracoda, Tantulo- carida and the Cambrian orders Skaracarida and Orstenocarida (Grygier, 1987: Boxshall and Huys, 1989; Miller and Walossck, 1988). The two latter orders, with Bradoriida and Phospha- tocopida (Ostracoda), serve to emphasise the early adaptive radiation of maxillopodans and the equally important subsequent early extinc- tions. Thanks to painstaking work by Miiller (1979a, 1982) and Maller and Walossek (1985, 1988), the anatomies of Phosphatocopida, Skaracarida and Orstenocarida are known in considerable detail, A comparison indicates clearly that the mos! generalised limbs are those of the phospha- tocopid suborder Vestrogothiina in which the antennule is reduced (Falites), the antenna through to the maxilla are biramous and closely similar in morphology, the 6th and 7th limbs are modified from the antenna-maxilla pattern and the Sth ‘limb’ is lamellar (possibly a furea). In Hesslandonina, the antennule is small and uni- ramous, antenna and mandible are biramous and similar, and the maxillule, maxilla, 6th and 7th limbs while differing somewhat fram jhe antenna-mandible pattern are also similar (Miller, 1979a, 1982). The organisation of Skaracarida limbs re- sembles that of Hesslandonina, i.e. uniramous antenule, look-alike antenna and mandible, sim- ilar maxillule, maxilla and maxilliped; but the rest of the body is strikingly distinctive compris- ing 10 circular limbless segments, followed by a telson and 3-segmented furcae (Miiller and Walossek, 1985). Bredocaris, the representative of Orsteno- carida, has differentiated anterior limbs, com- prising uniramous antennule, biramous antenna, mandible with well defined coxal gnathobasce, maxillule; but the maxilla and 7 thoracopods are similar to each other, The body ends in a short abdomen and furcae (Miiller and Walossck, 1988). The earlicst fossils of these maxillopodan orders are Early Cambrian naupliine Bradoriida, the most primitive of which (Shensied/a) seems to have possessed four body segments not in- cluding the telson, indicated by lobe-like expan- sions of the soft and very thin outer surface of the carapace shield (Huo and Shu, 1983: 87). The progressive decrease in lobes through strati- graphically higher beds indicates fusion of the body segments terminating in an unsegmented body (Hanchungella), This ancestral stock then divides into the Lipabdomina (lacking an abdo- men) and Abdomina (with an abdomen). Jones and McKenzic (1980) alsa suggested such a division in Bradoriida but regarded itas evidence for polyphyly. However, the discovery of Nau- pliinae substantiates a monophyletic origin for the order. Fig. 3 presents phylogenies of the carly Max- 30 MEMOIRS OF THE QUEENSLAND MUSEUM Cambrian Ba BI FIG. 3. Phylogenies of the maxillopodan orders and the superorder Thecostraca. Left hand side shows the phylogeny of Skaracarida (Sk), Oerstenocarida (Or) and Thecostraca (Th) from an origin in bradoriid Abdomina. Right hand side shows the phylogeny of the ostracode orders Phosphatocopida (Ph), Leperditi- copida (Le), Beyrichicopida (Be), Cladocopida (Cl), Halocyprida (Ha), Myodocopida (Mo) and Podo- copida/Platycopida (PoP!) from an origin in bradoriid Lipabdomina., illopoda based on an origin in naupliine Bradoriida, On the left, the orders Skaracarida and Orstenocarida split successively from Abdomina; and Thecostraca are interpreted as diverging from Orstenocarida (Miller and Walossek, 1988). On this main branch, Tantulo- carida evolved subsequently from thecostracans (Boxshall and Lincoln, 1987); Branchiura also from Thecosttaca; Copepoda from Skaracarida- like forms; and Mystacocarida from Copepoda (Boxshall and Huys, 1989, fig. 6). Copepod specialists will decide whether or not the Early Cretaceous parasitic species from Brazil is close to the ancestral Copepoda. Based on geological history, copepods probably diver- sified nearshore and on land after the Triassic; profited from the mid-Cretaceous opening of the Atlantic; were exposed to Cretaceous decima- tion; and underwent an adaptive radiation espe- cially in the oceans during the Cenozoic. Mystacocarida, with their interstitial and caver- nicole life habits and longitudinal distribution from Europe to southern Africa, probably evolved from copepod ancestors during the opening of the Atlantic. A possible geological history for some Branchiura was given earlier. The right hand side of Fig. 3 provides a phylo- geny based on Lipabdomina and shows evolu- tion of the ostracode orders. Phosphatocopida diverged via Oepikalutidae (Jones and McKenzie, 1980) in the Midddle Cambrian; Beyrichicopida in the Late Cambrian possibly via Beyrichonidae (McKenzie, Miller and Gramm, 1983); Leperditicopida perhaps in the Late Cambrian (Scott. 1961). Podocopida branched off from Beyrichicopida in the Early Ordovician, and Platycopida possibly from Podocopida in the Late Ordovician; while My- odocopida evolved from Beyrichicopida in the Ordovician, giving rise to Cladocopida and Halocyprida in the Ordovician and Silurian re- spectively, as discussed earlier. The cladistics of the three latter groups is based mostly on Kor- nicker and Sohn (1976b). Kornicker (pers. comm., 1981) accepts the ordinal status of Cladocopida, Lastly, the photograph of an Am- phissites soft anatomy in Miller (1979b) shows that a beyrichicopid origin for podocopids and platycopids is plausible. EPILOGUE History is the biostratigraphy of Homo sapiens, now self-recognised as a rather insensi- tive dominant in the organic world. A main fea- ture of this dominance has been the passive dispersal of thousands of species, usually deliberate but also, on numerous occasions, accidental. Thus, ever since the first human settlements people have transformed their sur- CRUSTACEAN EVOLUTIONARY EVENTS 3] rounding environments by the cultivation of ex- otic but useful plants. The earliest such introduc- tions.can be dated archaeoethnobotanically, but most information on the spread of useful plants is accessed by studying socio-economic history. Many crustaceans have minute dessication-re- sistant eggs that could be transported casily with seeds of exotic cereals and other plants, in soil packed around cuttings; also as dust carried with trade goods, and by travellers and migrating peoples. Both archacocthnobolanical and his- torical records were cited by McKenzie and Moreni (1986) in documenting the role of humans a5 an agent of crustacean passive disper- sa] via useful plants with respect to the many ostracode ospin esteri (foreign guests) of north- ern Italian ricefields. These species origimaled variously, in Africa, Australia, Asia and South America, None of them have been identified in European Tertiary and Quaternary fossil assem- blages. The authors also stressed thal numerous other exotic plants could have been the first vectors for such introductions (McKenzie and Moroni, 1986). Margaritora, Ferrari and Crosetti (1987) found a Far East Moina (cladoceran) in an Italian ricefield which they thought came in with seed exchanges; and Ferrari (pers. comm., 1989) has identified an Oriental calanoid copepod in northern Italy. Marine Crustacea are also susceptible to pas- sive dispersal by humans, the principal vector in this instance being shipping ballast. The earliest ballasts were large stones — clumps of ballast stones can still be seen on atolls, such as Aldabra in the Indian Ocean — and the mud and water associaled with these could harhour small crustaceans, Thus the homogeneity of shallow water ostracode assemblages in island groups of Micronesia (Wetssleader ef al., 1989) may Well be due in part to passive dispersal via frequent inter-island voyages. Sea trade was well established even before Roman times and by the 12th century Islam controlled the Asian sea coutes. With the Chinese invention of bulkheads (Needham, 1971), large ships capable of long oceanic voyages could be built, The Ming admiral Zhung He established a Chinese hegemony in the Indian Ocean early in the 15th century, but this lapsed when later Ming emperors adopted an isolationist policy, In 1492, Columbus discovered America and in 1493 Vasco da Gama sailed round southern Africa to Todia. Soon Portugal, Spain, Holland, France and Britain were colonising and trading directly in Asia and the Americas. When needed, ballast was dredged up by shipboard pumps from har- hour bottoms, This practice continues and now poses 3 serious quarantine problem worldwide. For example, around 60 million tonnes of ballast water are discharged in Australlan Waters each vear; and crustaceans are known to be among the numerous organisms dispersed internationally iy this way (Australian Quarantine and Inspection Service pamphlet, 1990), My own research hes concentrated upon trade in the Mediterranean for which the historical records are excellent, partic ularly those in the Venetian archives (Boredli, 1985), Maddocks (pers. comm,, 1988) has sug- gested thal some unexpected ostracode distribu- tions off Florida may be due to passive dispersal in the ballast of pirate ships during, the 16th to 18th centuries. Many discontinuous distributions of Recent crustacean species and genera are simply ex- plained by passive dispersal in ballast sludge during the past 500 years, Apart from taxa cited in McKenzie (1989), the ostracodes Mungava and Dalerocypria (Wouters, 1987a, 1987b) and lhe harpacticoid Darcythompsonia (Fiers, 1986) could have been distributed passively in such a manner. Obviously, any taxa spread by humans on land or by sea are allochthonous to the geological evolution of Crustacea; and phylogenetic inter- pretalions based upon such distributions are faulty, Because crustacean taxonomy itself is only abou! 250 years old many of these disper sals predate it; but others, particularly of small species, are still oecurting. ACKNOWLEDGEMENTS The literature cited makes clear my profound debt to the generous provision of reprints by many colleagues over many years. T also ac- knowledge gratefully reviews of the draft ms by Professor D.T. Anderson, University of Sydney; Professor J, BergstrOm, Swedish Museum of Natural History, Stackholm; and Professor F.R, Schram, San Diego Museum of Natural History. Some financial support was provided by the Conference Organising Committee. This paper complements that presented a decade ago at the international crustacean conference held in Syd- ney, May 1980, LITERATURE CITED ABUSHIK, A.F. 1979. Order Leperditicopida — mat- phology, classification, distribution, 29-34. In N. Kestic (ed.) ‘Proceedings of the VIT Inter- ay 2 national symposium on Ostracodes’. (Serbizn Geological Society: Beograd). ADAMCZAK, F. 1968, Palaeocopa and Plalycopa (Ostracoda) from Middle Devonian rocks in the Holy Cross Mountains Poland. Stockhalm Con- tributions in Geology 17; 1-109. 1976. Middle Devonian Podocopida (Ostracoua) trom Poland; their morphology, systematics and occurrence. Senckenbergiana lethaeu 37(4/6): 265-467. AL-ABDUL-RAZZAQ, §. 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MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ZOOGEOGRAPHY OF THE PENAEIDAE W.DALL Dall, W. 19910901; Zoogeography of the Penaeidae. Memoirs of the Queensland Museum 31; 39-50. Brisbane. ISSN 0079-8535. The Penaeidae are tropical stenotherms. mostly inhabiting shallow, silly inshore enviton- ments. Their present distnbution appears to be largely determined by a combination of geological history, temperature, ocean currents. ocean deeps and coastal geography. Penaeids are almost six limes more diverse in the Inda-West Pacific Region than in the Western Atlantic, which may be related to continental shelf area or the length of shoreline. Most extant genera probably onginated in the Tertiary, and there is evidence that some species have separated within the last 2 million years. Except for a few pelagic and deep-water species, the penaeid populations of the Indo-West Pacific, Eastern Pacific and Western Atlantic Regions are discrete. Within each region, two or more subregions have been defined, supported by cluster analysis of the Inda-West Pacific Regian. Reasons for these divisions are discussed. particularly the barriers to penaetd movements from the Indo-Malaysian to the Tropical Australia Subregion. These barriers appear to be primarily deep water and unfavourable currents along the steep northern and southwestern coasts of New Guinea. Possible causes of Southern Hemisphere endemism in the Penacidae are discussed, Because of the absence of fossil records extinction hypotheses cannot be tested, bul the apparent absence of amphitropicality in the family and the limited geographic range of many species suggest that evolution within the Southern Hemisphere can account for the endemism of penaeid species there, The unique genera Macrepelasma and Artemesia could be relicts of Miocene. relatively cool-water populations, bul there is no firm evidence to support this, () Periaeidae , zoogeagraphy, tropics, endemism, temperature, ocean currenis, ocean deeps, Indo-West Pacific, Eastern Pacific, Westermt AUlantic W. Dall, Division of Fisheries, CSIRO Marine Laboratories, P.O, Bax 120, Cleveland, Queensland 4163, Australia; 1) July, 1990. The Penueidae is the best-known family within the Penaeoidea in the decapod Suborder Dendro- branchiata. The 171 known species within 17 genera (Table 1) are predominantly tropical and subtropical, About 80% of these species usually live in depths of <100 m; the remainder normally either inhabit deeper water (10 Metapenaeopsis spp.; most Parapenaeus spp.. all Penaeopsis spp.) or are pelagic (all Funchalie spp. and Pelagopenaeus). Many of the deep-water and pelagic species appear to be widely distributed, Funchalia villosa and F. waodwardi, for ex- ample, having been recorded in the Pacific. Atlantic and Indian Oceans. Records of the dis- tribution of these pelagic species are, however, ioo sparse to discuss their zoogeography, so mos of this review is devoted to the better-known shallow-water Penaeidae. All shallow-water Penaeidae so far investi- gated have a planktonic larval phase of about 2-3 weeks, followed by inshore or estuarine early juvenile stages (Dall et al., 1990). Most species prefer soft substrates, ranging from mud to sand, but a number — probably around 25% — (mainly Metapenaecopsis spp.. Heleropenaeus, Trachypenaeopsis), preter harder substrates such as coral rubble. There is one commensal with corals (Meiapenaeopsis commensalis). Both biotic and physical factors are likely to influence the distribution of marine crustaceans such as the Penaeidae. They ate subject to con- siderable predation pressure (Dall er al., 1990); in some areas the papulation density is high and interactions between species may be important. However, while no studies on the effects of such biotic factors have heen made, the physical en- vironment appears to be more important in de- termining the distribution of penaeids. Their life histories suggest there are four principal factors that may affect their distribution : 1. Temperature. As tropical stenotherms they are restricted to the warmer waters of the world. In lower latitudes, cold winds from continental land masses may cool inshore waters or cause upwelling and thus be barriers to distribution; cold currents from higher latitudes may have a similar effect. Conversely, warm currents may extend the latitudinal range of penaeids along a coast. 2, Oceanic larval advection. The pelagic larval 40 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. Genera of the Penaeidae, the world-wide number of species within each genus and the number of species within each region. IWP, Indo-West Pacific; EP, Eastern Pacific; WA, Western Atlantic; EA, Eastern Atlantic; (P), pelagic, probably present in all oceans; number in parentheses, additional spe- cies also present in Western Atlantic. Total Species per region species|IWP EP WA EA Genus Artemesia Atypopenaeus Funchalia Heteropenaeus Macropetasma Metapenaeopsis Metapenaeus Parapenaeopsis Parapenaeus Pelagopenaeus Penaeopsis 4 a, ett 4 (P) (P) (P) (P) Penaeus Protrachypene Tanypenaeus Trachypenaeopsis Trachypenaeus Xiphopenaeus * not including Funchalia and Pelagopenaeus. life makes most species susceptible to the in- fluences of currents flowing in unfavourable directions, such as towards higher latitudes or from inshore to offshore. 3. Oceanic deeps. These constitute a barrier for shallow-water species, especially when they are very close inshore or in conjunction with un- favourable currents. 4. Coastal geography. Since most species live in shallow waters, particularly in the early ju- venile stages, lack of suitable inshore habitats may constitute a barrier. Thus a desert coastline with high inshore salinities, or a very rocky coast with deep water inshore, may restrict the dis- tribution of some species. DISTRIBUTION IN TIME The Penaeidae are an ancient group. Penae- oidea have been recorded in the Mesozoic, back to the Upper Triassic, mostly in various shales of central Europe, the eastern Mediterranean and Great Britain (Glaessner, 1969), with a few in North America (Herrick and Schram, 1978). Crustacea are, however, poor candidates for fossilisation, particularly the thinner-shelled groups such as penaeids (Bishop, 1986). Further, the normal environmental conditions of penaeids are not conducive to fossilisation because of the presence of numerous scavengers and bioturba- tion of the sediment by a large burrowing infauna (Plotnick, 1986). Hence the penaeid fossil record is very sparse. The Penaeidae first appear in Jurassic deposits and become more common in the Cretaceous. Most of these earlier Penaeidae became extinct at the end of Mesozoic, Penaeus being the only surviving genus. Apart from one Penaeus record from India in the early Tertiary, no fossils of more recent origin have been found, so geological evidence of the origins of the re- maining 16 extant genera is completely lacking. The times at which existing genera diverged have therefore to be estimated by other means. Limited data are available from biochemical genetics, supported by palaeogeography (Dall et al., 1990). These authors calculate from geneti- cal data that Metapenaeus could have separated from Penaeus between the early Tertiary and the Pliocene. The genetic distances within these genera indicate that some present species evolved between the Miocene and the Pleisto- cene. While estimates of divergence times from biochemical genetics are imprecise, they can be improved by palaeographical evidence. Separa- tion of the Atlantic Ocean from the rest of the Tethys Sea by closure of the Mediterranean during the Miocene isolated its warm shallow- water fauna (Por, 1986). Although North and South America were not joined during the Oligo- cene—Miocene and the present Isthmus of Panama was not established until the Pliocene (White, 1986), physical conditions in the proto- Caribbean and Pacific had begun to differ by the late Miocene (Keigwin, 1978). Fossil evidence also suggests that the two faunas were distinct at this time (Ekman, 1953). Penaeid genera com- mon to the Atlantic, Pacific and Indian Oceans today were presumably in existence before the separation of the Atlantic. These are the shallow- water genera Penaeus, Metapenaeopsis, Parapenaeopsis, Trachypenaeus and Trachy- penaeopsis. On this basis, excluding the deep- water or pelagic genera (Funchalia, Parapenaeus, Pelagopenaeus and Penaeopsis), seven may have originated since the Miocene. Thus the combined evidence suggests that the ZOOGEOGRAPHY OF THE PENAEIDAE 4) i is a jan: S fet, ' py ( i By Piet agg \ Fa y as Y a ee Ss MV in Fon 0 ir woo 6 Pg SI FIG. 1. Location of 20°C and 15°C minimum winter sea surface temperature isotherms. They correspond with the isocrymal lines (coldest 30 conseculive days of the year) of the Northern and Southern hemispheres. majority of present penaeid genera may have originated in the last 10-15 million years. WORLD DISTRIBUTION The Penaeidae are distributed throughout the world, but their latitudinal distribution is limited by temperature. Most species occur within the isotherms of 20°C minimum winter tempera- tures (Fig. 1). Between the 20°C and 15°C isotherms the number of species falls to about 30% of those within the 20°C isotherms. In these cooler zones, the growth and activity of most species are minimal in winter, but temperatures in summer are usually high enough for them to achieve growth rates comparable with those of fully tropical species. Only two species are abun- dant outside the 15°C isotherms: Penaeus chi- nensis in the Pohai and Yellow Seas and Artemesia longinaris in southeastern South America. Both have adapted to survive tempera- iures down to about 6°C, but, in addition, the adaptive behaviour of P. chinensis enables it to cope with the hostile winter environment. It mi- grates into the deeper waters of the Yellow Sea at the onset of winter and returns to exploit the rapid warming of the shallow waters in spring and subsequent summer temperatures of 25°C (Chang Cheng, 1984). A similar strategy is not available to Artemesia, as water temperatures in the southern half of its range do not rise above 20°C, but winter temperatures are nol as severe as in the Pohai Sea (Angelescu and Boschi, 1959). REGIONAL DISTRIBUTION Ekman (1953) divided the shallow, warm- water marine faunas of the world into Inda-West Pacific, Eastern Pacific, Western and Eastern Atlantic Regions. This classification has been followed by Briggs (1974) for various tax- onomic groups and by Abele (1982) for Crustacea. The Atlantic is clearly separated from other oceans by the Americas and the Afro- European landmasses, and the deep ocean sepa- rates the Atlantic into eastern and western faunas, The Eastern Pacific fauna is separated from the rest of the Pacific by a wide expanse of deep ocean, containing very few islands. East- ward movement of warm-water planktonic larvae js discouraged by the westward Equatorial Current, which is fed in this region by cold currents flowing towards the equator along the west coasts of North and South America. Only species with an exceptionally long larval life can be transported eastward from the Central Pacific (Scheltema, 1988). The fauna of the Eastern Pacific Region does, however, have some affini- ties with that of the central Wester Atlantic, as the final separation of the two oceans did not occur until the early Pliocene and twin species are common (Ekman, 1953). Examples in the Penacidae are Trachypenaeus pacificus - T. similis and Xiphopenaeus riveti : X, kroyert 42 MEMOIRS OF THE QUEENSLAND MUSEUM (western and eastern coasts of the Isthmus, re- spectively). The remainder of the Pacific is not separated zoogeographically from the Indian Ocean and the two are usually grouped together as the Indo- West Pacific Region. Springer (1982), from a study of shallow-water fishes, proposed that the Pacific Plate should be designated as a separate region, but this is not supported by the distribu- tion of corals and echinoderms (Ekman, 1953), nor by that of the Penaeidae (Dall et a/., 1990), Although the number of penaeid genera in the Indo-West Pacific and Western Atlantic Regions is similar, there is great disparity in the number of species (Table 1). Excluding Funchalia and Pelagopenaeus, the Indo-West Pacific contains 73% of known species, compared with 12% in the Western Atlantic. Abele (1982) found simi- lar ratios for other decapod Crustacea (Por- tunidae, Parthenopidae, Sesarma spp. and Alpheus spp.). He also notes that the ratios are due to the large number of congeneric species in the Indo-West Pacific, rather than an increase in the number of genera. Abele (1982) discusses several hypotheses to account for this. Ona small scale there is a positive correlation between hab- itat complexity (e.g. sandy beaches, sand-mud beaches, mangroves, corals and rocky intertidal) and crustacean species diversity, but this does not appear to be valid for zoogeographical re- gions. It would also be unlikely to apply to the Penaeidae, which occupy similar habitats both latitudinally and longitudinally. Briggs (1974) suggests that the number of species of tropical shallow-water marine animals is directly corre- lated with continental shelf area. Abele (1982) obtained a positive linear correlation between continental shelf area and numbers of warm shal- low-water marine crustacean species in the four major regions. He also obtained a positive log- log relationship between Caribbean island per- imeter and number of marine shrimp species (penaeids and carids). Shoreline length may be the reason for the higher penaeid species diver- sity in the Indo-West Pacific, as the factors that tend to isolate penaeid populations are related to the shoreline. SUBREGIONS There are considerable differences in geo- graphical ranges in the Penaeidae, both between and within genera (Dall ef al., 1990). Thus the most ancient genus Penaeus is, with few excep- tions, the most widely ranging. Penaeus japoni- cus, P. latisulcatus, P. marginatus, P. monodon and P. semisulcatus have been recorded in most of the warmer waters of the Indo-West Pacific. In the Eastern Pacific, all Penaeus species are found in both subregions, while in the Western Atlantic they extend through at least two sub- regions, with P. notialis occurring on both sides of the Atlantic. The deeper water genera Para- penaeus and Penaeopsis are also wide ranging, but generally less so than Penaeus. The remain- ing genera are mostly more restricted in range, about 50% of all penaeid species being endemic to one or two subregions. (Some species within these genera with an apparent wide range, such as Metapenaeopsis mogiensis and M. hilarula, may be complexes of species, A. Crosnier, pers. comm.). Dall et al. (1990) define and discuss penaeid subregions within each of the regions. They used the distribution of species with a restricted range, particularly those endemic to a particular area, to define subregions. Geography and temperature data were also taken into account. These were confirmed for the present study for the Indo- West Pacific Region by cluster analysis of the presence-absence data of all species on the basis of euclidean distance with group average hierar- chical clustering (Fig. 2). Bray-Curtis group average hierarchical clustering gave similar groupings, but with Southeast and Southwest Australia separated from the other subregions and closest to the West Pacific. (Reliable cluster analyses for the subregions defined by Dall et al. (1990) for the Eastern Pacific and Atlantic were Average distance co 0.0 —_t E Ss SE SW W_ Arab Sino- Trop Indo- Afr Afr Aust Aust Pac Sea Jap Aust Mal Sub-region FIG. 2. Group average hierarchical cluster analysis of Indo-West Pacific Subregions, using presence-ab- sence data of all species, based on euclidean distance. Abbreviations: E Afr, East African; S Afr, South African; SE Aust, Southeast Australian; SW Aust, Southwest Australian; W Pac, West Pacific Oceania; Arab Sea, Arabian Sea; Sino-Jap, Sino-Japanese; Trop Aust, Tropical Australian; Indo-Mal., Indo- Malaysian. ZOOGEOGRAPHY OF THE PENAEIDAE 43 FIG, 3. Subregions of the Indo-West Pacific Region. 1, Indo-Malaysian; 2, Tropical Australian; 3, Sino-Japanese; 4, Arabian Sea; 5, East African: 6, South African; 7, Southwest Australian; 8, Southeast Australian; ?9, Pacific Oceania; arrows, extension of Malay-Indonesian Subregion (see text for definitions). not feasible because of the paucity of species in these areas). Inpo-WEsT Paciric SUBREGIONS (Fig. 3; Table 2). 1. Indo-Malaysian. This is defined in the south by the oceanic deeps off southern Indonesia, which extend into the Timor Sea, to the west of the Aru Islands, coming close inshore at the neck of West Irian. To the east, oceanic deeps and westward equatorial currents form a major bar- rier, while to the north falling temperatures close off the subregion. There is no obvious barrier in the west, the shallow coastal waters of the Straits of Malacca running without apparent interrup- tion through the Bay of Bengal. However, there is a steady decrease in the diversity of penaeid species diversity from Malaysia to the Bay of Bengal (Dall e7 a/., 1990), as in other faunas (Ekman, 1953). Dall er al. (1990) suggest that unfavourable currents, plus the strongly mon- soonal climate of India may restrict the westward movement of penaeids. The southern tip of India has been arbitrarily selected as the western boundary of this subregion. 2. Tropical Australia. This subregion extends from the southern coast of New Guinea to the 20°C winter isotherm on the east and west coasts of Australia. The significance of the barriers to the northeast and northwest are discussed in detail below. 3. Sino-Japanese. The southern boundary is defined by the 20°C isotherm. The diverse fauna of the Gulf of Tonkin and southern China decreases sharply to the north due to cold conti- nental influences, but the Equatorial Current runs offshore to the northeast, raising the min- imum winter temperature in the Sea of Japan and giving this area a large and distinctive penaeid fauna. 4. Arabian Sea, This subregion, from the south- ern tip of India to Cape Guardafui at the entrance 44 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 2. Total number of specics and endemit species in the subregions of the Indo-West Pacific Region. Indo-Mal, [ndo-Malaysian: Trop Aust, Tropical Australia: Sino-Jap. Sino-Japanese: Arab Sea. Arabian Sea; E Afr, East Attica: S$ Afr, South Africa: SW Aust Southwest Ausiralia; SE Aust, Southeast Australia; O, Pacilic Oceania. Indo- Trop Mal. Aust Total species Endemic species to the Red Sea, has extensive arid coastlines; the hypersaline inshore waters and cold continental winter winds probably act as barriers to less adaptable species. The Red Sea is usually treated ag a Separate subregion because of its distinctive fauna (Ekman, 1953; Briggs, 1974). but the penaeid fauna differs only in having fewer spe- cies and has therefore been included in this sub- region. 5. East African Coast. This extends from Cape Guardafui to Durban. Briggs (1974) regards the coast from the Gulf of Iran to the southern tip of Africa as one subregion, but ihe East African Coast appears to support a more diverse and possibly larger penaeid population than the Arit- bian Sea (Crosnier, 1965). Neither the northern nor the southern boundariesare well detined, but there is a drop in species diversity around the latitude of southern Madagascar. 6, South Africa. This subregion could be jn- cluded in East Africa, except for the appearance of Macrapetasma africanus at Durban. This spe- cies becomes common on the south coast. west of Algoa Bay, where other penacid species are rare, and is unique in that it extends northward along the west coast of southern Africa from Cape Town to Swakopmund, in the cool waters derived trom the Benguela Current. 7. Southwestern Australia. The 20°C isotherm defines the northern boundary of this subregion, which extends across southern Australia because of the influence of the warm southerly Leeuwin Current. There are two endemic specics; Meta- penaeopsis fusca and M. lindae. 8. Southeastern Australia. The 20° C and 15° C isotherms define the northern and southern limits of this subregion. [t has three endemic species, Penaeus plebejus. Metapenaeus ben- nettae and M. macleayi; the first two appear to be siblings of widely distributed species. EAfr S Afr SW Ausi 9. Pacific Oceania. The penaeid population of this subregion appears to be mostly an extension of the Indo-Malaysian fauna; it is therefore doubtful that it is a valid penaeid subregion (indicated by the query in Fig. 3). Two endemic species have been identified: Metapenaeopsis tarawensis and M. comnensalis. both inhabi- tants of coral reefs and the latter a commensal with corals. M. commensualis may be more wide- spread than the published record indicates, WESTERN ATLANTIC SUBREGIONS (Fig. 4; Table 3.) The Western Atlantic Region extends trom Martha's Vineyard, 43"N to Puerto de Rawson, 43°S. The subregions are: |, Caribbean, This extends from southeast Florida through the Caribbean to Sao Luis, Brazil, but stops at the entrance of the Gulf of Mexico, Geographically this area is analogous to the Indo-Malaysian Subregion of the Pacific. It has the greatest penaeid species diversity (16) within the Atlantic Ocean, with three endemic species (Tanvpenaeus caribeus, Trachypenae- opsis mobilispinis, Trachypenaeus similis). The eastern boundary js defined by a marked drop in species diversity, Which appears to be due to a strong westward current, plus a monsoonal cli- mate in eastern Brazil. 2. Fastern Brazil (Sao Luis to Cabo Frio), The southern boundary at Cabo Frio is caused by a cooler-water coastal northerly current meeting the warm southerly Brazilian Currentand divert- ing offshore. There are no endemic species, but the species composition is appreciably different from that of the Caribbean. 3. Gulf of Mexico. This is defined by Penaeus uziecus, P. duorarum and P. seuferus, which are plentiful in the Gulfof Mexico, but do notextend eastwards into the adjacent Caribbean Sub- ZOOGEOGRAPHY OF THE PENAEIDAE 45 FIG. 4, Subregions of the Western Atlantic, Eastern Atlantic and Eastern Pacific Regions. Western Atlantic: 1, Caribbean; 2, Eastern Brazil; 3, Gulf of Mexico; 4, Eastern USA (Carolinean); 5, Southeast South America. Eastern Atlantic: 6, Eastern Atlantic; 7, Mediterranean Sea. Eastern Pacific: 8, Panamanian; 9, Mexican (see text for definitions). region. Also, low winter temperatures in the north of the Gulf reduce the species diversity (7 compared with 16 in the Caribbean). 4, Eastern USA (Carolinean) (Martha’s Vine- yard to southeast Florida). Cape Hatteras is the northern limit of abundant penaeid distribution, but there have been records of Penaeus aztecus as far north as Martha’s Vineyard. 5. Southeast South America (Cabo Frio, Brazil to Puerto de Rawson, Argentina). Penaeus paulensis and Artemesia longinaris are endemic species in this well-defined cooler-water subregion. EASTERN ATLANTIC SUBREGION These are shown in Fig.4 and detailed in Table 3.The Eastern Atlantic Region includes the Medi- terranean Sea, usually considered to be a sepa- rate zoogeographical area. Also, at least five Indo-West Pacific species (Penaeus japonicus, P. semisulcatus, Metapenaeus monoceras, M. steb- bingi, Trachypenaeus curvirostris) have migrated through the Suez Canal from the Red Sea (Les- sepsian migration)(Gab-Alla e7 al, 1990). In the Atlantic, Penaeids normally extend as far north as about 40°N in Portugal, but in the south the cold Benguela Current limits the distribution to about 16°S in Angola. Thus the subregions are: 6. Eastern Atlantic (Lisbon, Portugal, 40°N, to Porto Alexandre, Angola, 16° S). 7. Mediterranean Sea. This subregion has only two of the six species found in the Eastern Atlantic, apart from the Lessepsian migrants. EASTERN Paciric SUBREGIONS (Fig. 4; Table 3) Eastern Pacific Region is reduced Jatitudinally 46 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 3. Total number of species and endemic species in the Subregions of the Western Atlantic, Eastern Atlantic and Eastern Pacific Regions. Car, Caribbean; E Br, Eastern Brazil; GoM, Gulf of Mexico; E US, Eastern USA (Carolinean); S SA, Southeastern South America; E A, Eastern Atlantic; Med, Mediterranean Sea; Mex, Mexican; Pan, Panamanian. Total species Endemic species in both the north and south by cold currents flowing towards the Equator; the continental shelf is mostly narrow and there are relatively few islands to support populations of penaeids. Penaeid species composition changes markedly in the El Salvador region, which has been selected as a boundary between the northern and southern subregions. These are: 8. Panamanian. El Salvador to Punta Aguja, Peru. The unique Protrachypene, Parapenaeop- sis balli (the only Parapenaeopsis in the Western Hemisphere) and three species of Trachy- penaeus define this subregion. 9. Mexican. San Francisco Bay (northern limit of penaeid records) to El Salvador. Here the penaeid diversity is lower than in the Panamanian, with three endemic species Meta- penaeopsis beebei, M. kishinouyei and Trachy- penaeus brevisuturae. BARRIERS TO DISTRIBUTION Low temperature, and thus latitude, has been mentioned as one of the principal boundaries to penaeid distribution. These boundaries may be modified by warm currents flowing away from the equator, or cold currents flowing towards it. Thus the northern boundaries of the South Afri- can, Southwest and Southeast Australian Sub- tegions, and the southern boundary of the Sino-Japanese Subregion, defined by the 20°C winter isotherm, extend outside the tropics (Fig. 1). In all cases there is a marked drop in species diversity outside the 20°C isotherm, with the appearance of one or more endemic species (Table 2). There are comparable subregions in the Western Atlantic. In the Eastern Atlantic and Eastern Pacific, where cold currents flow towards the equator, the north-south extent of the subregions is considerably less than in the Western Atlantic (Fig. 4) and Indo-West Pacific (Fig. 3), In addition, the paucity of species in the Eastern Atlantic does not permit the definition of a possible subregion between Portugal and Cape Verde on the western tip of Africa. Within the tropics, the less obvious limits — ocean currents, oceanic deeps, coastal geogra- phy — appear to be responsible for most of the discontinuities in penaeid distribution. Ex- amples of how these barriers may operate in the Tropical Australian Subregion, which is ap- parently contiguous with the Indo-Malaysian Subregion, are described below and shown in Fig. 5. (The well-known water barriers of Wal- lacia that separate the terrestrial floras and faunas of Australia-New Guinea from southeast Asia are due to long-term movements of the tectonic plate [see review by Whitmore, 1981]; these barriers are not relevant to marine faunas with dispersive planktonic larvae.) The Indo-Malaysian penaeid fauna attenuates along the north coast of New Guinea from west to east. In eastern New Guinea and the Solomon Islands, only 17 species, four of which are deep- sea, are common to the Indo-Malaysian Sub- region, which contains 84 species. All of the 13 shallow-water species are wide-ranging: Penaeus spp. (7); Metapenaeus spp.(4); Hetero- penaeus longimanus , Trachypenaeopsis richtersii. The New Guinea Trench runs close to the steep mid-northern coast of New Guinea, resulting in a very narrow continental shelf (Fig. 5). Further to the east the end of the New Britain Trench comes close inshore. Except for the Sepik River, there are no major rivers along this coast and no extensive marine estuaries. The westward Equatorial Current flows close inshore for most of the year (Lindstrém er al., 1987). The southeast coast of New Guinea is similar geo- graphically to the north coast, but has an along- shore eastward current (CSIRO, unpubl.), which thus discourages westward migration of Penaeidae (such as Metapenaeus affinis and M. anchistus) from the eastern end of New Guinea towards Tropical Australia. To the northwest of Australia the Java Trench extends along southern Indonesia, reaching in the east, past the island of Sumba; deep water ZOOGEOGRAPHY OF THE PENAEIDAE 47 O° Soe FS aE SRO. ‘ ov %, é )* sh x3 fr, 1" BANDA sEA © eo apseicne es >, 1¢ou0h 10° Java Trench qe iat 20° 120° 130° Ne “A vt Suing, we 4 > NS RO EE G —~ f 3 : 2 a —_—_,—— ave_lrench = Thy nO ose, 7; sor * Te = ~\ Urey 209, [CORAL SEA 150° 140° FIG. 5. Geographical features that tend to isolate the Tropical Australian Subregion from the Indo-Malaysian Subregion. Arrows indicate surface currents. continues to the northeast as the Timor Trough, followed by the Aru Basin, coming close inshore at the neck of New Guinea (Fig. 5). Here the continental shelf is very narrow, which probably inhibits coast-wise migration of penaeids. The Banda and Aru Basins are fed by southerly in- flows from the Pacific Ocean and this water then flows southwesterly through the Timor Trench (Van Aken et al., 1988; Postma and Mook, 1988). Thus the net flow of intermediate and deep water is towards the Indian Ocean. In addi- tion, from April to October the southeasterly trade winds produce a northwesterly shallow- water flow, which appears to cause upwelling and lower water temperatures (Fleminger, 1986). This cold water then joins the surface currents flowing to the northwest, carrying any penaeid larvae away from the extensive shallow coastal regions of southern New Guinea and Australia. The effects of the November—March monsoon season on shallow-water movements do not ap- pear to have been documented for this area. In open waters the winds tend to be northwesterly during this period, which would enhance migra- tion of penaeid larvae towards Australia. But the discontinuity between Indo-Malaysian and Tropical Australia faunas indicates that some kind of year-round barrier exists. (This barrier is, of course, only partial; there are many species common to both subregions.) The western end of New Guinea is geographically complex, with mountain ranges from 1000 m to over 4000 m high. Winds originating in the north-northwest and flowing across the neck of New Guinea (about 1000 m high), could be deflected by the much higher mountains in the east, resulting in local southerly, or even south-westerly winds crossing the south coast. Such winds would probably be cool and could produce further in- shore upwelling. Also, Fleminger (1986) re- viewed evidence that, during the Pleistocene glaciation, water temperatures in this region may have been unusually cool for the tropics, due to cool prevailing winds and upwelling; this cool- ing may have acted as a barrier to tropical stenotherms. Dall et al. (1990) point out that during the maximum of the Quaternary Glacial Period the lowered sea levels would have re- sulted in most of the sea between New Guinea and Australia becoming dry land. There would have been a steep coast, with virtually no shallow 48 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 4. Apparent sibling species in the temperate subregions of southern continents and their more widely-ranging, usually tropical ‘parent’ species. Subregion Southeast South America South Africa Southwest Australia M. fusca M. lindae M. insona Metapenaeus bennettae Penaeus plebejus Southeast Australia water, connecting the two subregions, probably eliminating the migration of shallow-water penaeids during the last glacial period. The mi- gration of penaeids towards the northern Australian area from Indonesia, appears, there- fore, to have been restricted since the Pleisto- cene. The northwest coast of Australia, which is arid, with hypersaline inshore waters also appears to be unfavourable to penaeid colonisation. Of 36 shallow-water species in northern and north- eastern Australia, only 18 also occur in the far northwest of the continent. SOUTHERN HEMISPHERE ENDEMISM IN THE PENAEIDAE The Northern Hemisphere has only one sub- region (the Sino-Japanese) outside the tropics that includes endemic species, whereas in the Southern Hemisphere the South African, South- west Australian, Southeast Australian and the Southeast South American Subregions all con- tain endemic species (Tables 2, 3). Some of these are closely similar to more widely distributed tropical species and may be sibling species (Table 4), but there are also three Southern Hemisphere species which do not have any close affinities. Metapenaeus macleayi in Southeast Australia is distinctive within its genus, but Mac- ropetasma africanus in South Africa and Ar- temesia longinaris in Southeast South America are more exceptional. Both are monospecific genera, they are quite different from one another and from other genera, both fossil and present, of the Penaeidae. Artemesia and, to a lesser extent Macropetasma inhabit waters cooler than is usual for the Penaeidae. Newman and Foster (1987) conclude that en- demism of barnacles in the Southern Hemi- sphere is due to: Sibling species Penaeus paulensis Metapenaeopsis scotti M. insona Parent species ?P. aztecus 2M. philippii M. quinquedentata M. barbata 2M. acclivis M. quinquedentata M. moyebi P. latisulcatus 1, Extinction processes (either at low latitudes or of Northern Hemisphere counterparts). 2. Evolution of long indigenous taxa. Unlike barnacles, the Penaeidae have a very poor fossil record and extinction hypotheses can- not be tested, but as a predominantly tropical group, extinction within the tropics is probably less likely than in more widely ranging groups. There do not appear to be any clear examples of amphitropicality in the Penaeidae. There are Northern or Southern Hemisphere endemic spe- cies, but no matching pairs of species, nor are there any species with a clear break in distribu- tion in the tropics. P. aztecus and P. paulensis in the Western Atlantic may be amphitropical spe- cies, but the affinities of the Western Atlantic complex of grooved Penaeus species needs further research. Metapenaeopsis acclivis and M. lindae in the Indo-West Pacific may also be amphitropical, but there are significant morpho- logical differences between them and this genus also needs further research. The most usual sit- uation is for a northern or southern endemic to have a closely related species, which could be a parent, in the adjacent tropics (Table 4). The uniqueness of Macropetasma and Arteme- sia suggests that they could be relict species from much more widely ranging populations. Dall et al. (1990) examine the possibility that they could be Gondwana relicts, but find this hypothesis to be untenable. Macropetasma is unique among the Penaeidae in possessing photophores; Ar- temesia superficially resembles some deep- water Penaeoidea. Thus they could be relicts of a deep-water, possibly amphitropical group, but there are no similar extant deep-sea genera to support this hypothesis and wholesale extinction would need to be invoked. Alternatively, they could have been once widely distributed in the cooler conditions of the Miocene and sub- sequently became extinct in the tropics (Valen- ZOOGEOGRAPHY OF THE PENAEIDAE 49 tine, 1984). Although plausible, in the absenee of any supporting data, this hypothesis mustalso remain pure conjecture. However, the rate of evolution of penacid genera. discussed earlier, suggests that Macro-petasma and Artemesia could well have evolved since the middle Tertiary. (Protrachypene is another unique monospecific genus in the Eastern Pacific Region that has presumably evolved since the Caribbean fauna became separated from thal of the Eastern Pacific in the Miocene). Meiapenaeus macleayi and the sibling species listed in Table 4 could have evolved more recently. Dall ev al. (1990) estimate fram genetical evidence that the sibling species Metapenaeus bennetiae and Penaeus plebejus in Southeast Australia probably evolved in the last two million years. This urea was separated geographically from the rest of the Indo-West Pacifie during the last glacial epoch. The cold-adapted Penaeus chinensis must also have evolved from the closely similar and geo- logically ancient P. merguiensis - indicus group since the last glacial epach; the shallow Pohai and Yellow Seas would have been isolated lakes or dry Jand at the height of this period. Dall er ai. (1990) point out that the lowering of sea-levels in the late Tertiary and Quaternary would have produced extensive land bridges in former shal- low seas; these would have acted as effective barriers and thus enhanced penueid speciation during this period. The limited range of many species af Penaeidae also point to such processes in the evolution of the family. In summary, in the absence of fossil evidence to the contrary, evolution of pre-existing laxacan account for the endemism of the Southern Hemi- sphere Penaeidac. Macropetasma and Ariemesia may be excep- tions and are relicts of widely-ranging Miocene populations, but further evidence is needed to support this hypothesis. LITERATURE CITED ABELE, L.G. 1982. Biogeography. 241-304. In L.G Abele (ed.), ‘The biulogy of Crustacea, 1. Sys- tematics, ihe fossil record. and biogeography’. (Academic Press: New York and London), ANGELESCU, V. AND BOSCHI, EE, 1959. Estudio biologico pesquera del langostino de Mar del Plata en Connexion con fa Operacion Nivel Medio. (Servicio de Hidrografia Naval, Secretaria de Marina, Republica Argentina, Pub- lico H. 1017, Buenos Aires). BISHOP_G.A. 1986. Taphonomy of the North Amer- ican decapods. Journal of Crustacean Biology 6: 326-355, BRIGGS. J.C. 1974. *Marine zoogeography’- (McGraw Hill Ing,: New York).476p. CHANG CHENG, Y. 1984. The prawn (Penaeus orientalis Kishinuuye) in Pohai Sea and their fishery. 49-60. In J.A. Gulland and B.J. Rothschild (eds) ‘Penaeid shrimps — Their bi- ology and management’. (Fishing News Books: Farnham). CROSNIER, A, 1965, Les crevettes penaeides du plilewu continental Malgache; élal de nos con- naissunces sur leur biologie et leur peche in Septembre 1964, Caters ORSTOM, Oceanag- raphic Supplement 3(3); 1-158. DALL, W., HILL, BJ., ROTHLISBERG, P.C, AND STAPLES, D.J. 1990, ‘The biology of the Penacidae’, Advances in Marine Biology 27. (Academic Press" London) 489p EKMAN, S. 1953. “Zoogeography of the sea’. (Sidg- wick and Jackson: London).417p FLEMINGER, A.,1986. The Pleistocene equatorial barrier between the Indian and Pacific Oceans und a cause for Wallace's Line. UNESCO Tech- nical Papers in Marine Science 49: 84-97. GAB-ALLA, A.A.-F.A.. HARTNOLL, R.G,, GHOBASHY, A-F. AND MOHAMMED, S.Z. 1990, Biology of penaeid prawns in the Suez Canal lakes. Marine Biology 107: 417-426. GLAESSNER, M.F. 1969. Decapoda, 399-533. In R.C. Moore (ed,) “Treatise on invertebrate paleon- tology’, Part R, Arthropoda 4, VoLIL (Geological Sociely of America; Boulder, Colorado, and the University of Kansas Press: Lawrence). HERRICK, E.M. AND SCHRAM, F.R. 1978. Malacostracan Crustacea of the Sundance For mation (Jurassic) Wyoming. American Museum Novitates 2652: 1-12. KEIGWIN, L. D, 1978. Pliocene closing of the Isth- mus of Panama, based on biosiratigraphic evi- dence from nearby Pacific Ocean and Caribbean sea cores, Geology 6; 630-634, LINDSTROM, E., LUKAS, R., FINE, R., FIRING, E., GODFREY_ 5S., MEYERS, G. AND TSU- CHIYA, M, 1987. The Western Equatorial Pacific Ocean Circulation Study. Nature 330: $33-537. NEWMAN, W,A. AND FOSTER B.A, 1987. South- ern Hemisphere endemism among the barnacles, #xplained in part by extinction of northern mem- bers of amphitropical taxa? Bulletin of Marine Science 41; 361-377. PLOTNICK, R.E. 1986. Taphonomy of a modern shrimp: Implications for the arthropod fossil re- cord. Palaios !: 286-293, 50 MEMOIRS OF THE QUEENSLAND MUSEUM POR, F. D. 1986. Crustacean biogeography of the late Middle Miocene Middle Eastern landbridge. 69-84. In R. H. Gore and K. L Heck (eds) ‘Crustacean biogeography’. (A.A. Balkema: Rotterdam). POSTMA, H. AND MOOK, W.G. 1988. The trans- port of water through the East Indonesian deep- sea basins. A comparison of Snellius - I and Snellius - IT results. Netherlands Journal of Sea Research 22; 373-381. SCHELTEMA, R.S. 1988. Initial evidence for the transport of teleplanic larvae of benthic inverte- brates across the east Pacific barrier. Biological Bulletin, Marine Biological Laboratory Wood's Hole, Massachusetts. 174: 145-152. SPRINGER, V.G. 1982. Pacific plate biogeography, with special reference to shorefishes. Smith- sonian Contributions to Zoology 367: 1-182. VALENTINE, J.W. 1984. Neogene marine climate trends; implications for biogeography and evo- lution of the shallow-sea biota. Geology 12: 647-650. VAN AKEN, H.M., PUNJANAN, J. AND SAIMIMA, S. 1988. Physical aspects of the flushing of the east Indonesian basins. Nether- lands Journal of Sea Research 22: 315-339. WHITE, B.N. 1986. The isthmian link, antitropicality and American biogeography: distributional his- tory of Atherinopsinae (Pisces: Atherinidae). Systematic Zoology 35: 176-194. WHITMORE, T.C. (ed.) 1981. ‘Wallace’s line and plate tectonics’. (Clarendon Press: Oxford).91p MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM, ESPECIALLY AMONG MARINE CRUSTACEA WILLIAM A. NEWMAN Newman, W.A, 1991 09 01: Origins of Southern Hemisphere endemism, especially among marine Crustacea. Memoirs of the Queensland Museum 31: 51-76. Bnsbane. ISSN 0079-8835. There are a number of hypotheses to explain the high endemism above the species level in the Southern Hemisphere. The separation of Gondwana from Laurasia by the Tethys Sea during the Mesozoic and the subsequent breakup of Gondwanaland evidently explains some of the terrestrial and freshwater endemism. Marine endemism is not generally explained by these events however, but rather by late Mesozoic and Tertiary reliction of tropical forms, or by extinction of Northern Hemisphere portions of amphitropical forms. Amphitropicality apparently can result from dispersal across the tropics. But it can also result from exclusion of an earlier biota from the tropics. Exclusion often involves replacement by more advanced forms concomilant, ai leas! since ithe Miocene, with wurming and compression of the tropics. Areas of endemism in both hemispheres can be relatively localised and this provides insights into why a number of older taxa have survived there while going extinct elsewhere. Areas of marine endemism in the Southern Hemisphere are presently more evident in southeast Australia, Tasmania, and New Zealand than in other Southern Hemisphere outposts apparently because much of it has developed in the western Pacific since the breakup of Tethys. [J Crustacea, Southern Hemisphere, endemism, Gondwana, Tethys, relictian, amphitropical, dispersal, vicariance, William A. Newman, Scripps Institution of Oceanography, LaJolla, CA 92093-0202, USA; 22 February, 1991. There is a high degree of endemism in the Southern Hemisphere, compared to the Northern Hemisphere, on land and fresh water and, per- haps surprisingly, in the sea. While itis generally most pronounced in Australia, New Zealand, and islands of the southwest Pacific, some extends around the Southern Hemisphere, to oceanic is- lands as well as the southern parts of South America, Africa, and India. No one hypothesis explains the situation, al- though the breakup of Gondwanaland, after its long separation from Laurasia by the Tethys Sea, is apparently the best explanation for many of the freshwater and terrestrial forms that are suffi- ciently old and lack propagules capable of long range, trans-oceanic dispersal. The marine situa- tion is less clear since most farms have, or had, significant dispersal capabilities, and many of the Southern Hemisphere endemics are too young to have been part of Gondwanaland (McDowall, 1978; Newman, 1979). There is a growing consensus that much of the apparent endemism in the Southern Hemisphere is due to the extinction of Northern Hemisphere counter- parts rather than its having evolved there (Eskov and Golovatch, 1986; Newman and Foster, 1987). In the present paper some crustacean distribu- tions will be examined for endemism, especially in the Southern Hemisphere. But before getting to them, a brief discussion of climatic change, the development of tropical provincialism fol- lowing the breakup of Gondwanaland and Tethys, and examples and hypotheses relevant to the matter of Southern Hemisphere cndemism, ate in order. Some marine molluscs will be used as examples because, by and large, they have a good fossil record. BREAKUP OF GONDWANA AND TETHYS, AND CONCOMITANT CLIMATIC CHANGE it has long been recognised that the marine climate was equably warm up to relatively high latitudes im the late Mesozoic (Murray, 1896). but it is only in recent years that we have come to accept that in the Late Cretaceous, approxi- matcly 100 million years betore present (MY BP), the super continent Pangea was being split into Laurasia and Gondwana with the tropical sea known as Tethys in between (Kennett, 1982: Windley, 1984). A Tethyan marine biota was not only distributed throughout this sea, it included a $2 MEMOIRS OF THE QUEENSLAND MUSEUM large pantropical clement that circled the globe via oceanic currents and islands of Panthalassa, the present day Pacific (Hamilton, 1956). With continued continental drift, the Adantic began to open up and Gondwana to fragment. Both processes led io the breakup ol Tethys and, hence, to the tropical provincialism we see today (Ekman, 1953). Significant events in the breakup of Tethys included the northward movement of Africa and its contact with Eurasia in the lower Miocene, about 18 MYBP, followed by the clo- sure at Suez, virtually cutting off the tropical Indian Ocean from the Atlantic in the Middle Miocene, 12-14 MYBP (Kennett, 1Y82; Wind- ley, 1984). Likewise, New Guinea-Australia moved north to contact southeast Asia, thereby diverting the North Equatorial Current from the Indian Ocean to the North Pacific in the Upper Miocene, approximately 7 MYBP (Kennett ef al., 1985). The Panamic closure separated the widening Atlantic from {he tropical East Pacific in the Pliocene, (3. 1- 3.6 MYBP [Rosenblatt and Waples, 1986]), With the onset of the Tertiary, the shallow equuble seas of the Mesozoic began to cool and retreat, al low as well as high latitudes (Shackle- ton, 1984). This trend persisted throughout the Paleogene, about 25-30 MYBP. Then a new trend, correlating with the establishment of cir- cum-Anlarctic deep-water circulation near the end of the Oligocene, set in (Van Andel, 1979). It is noteworthy that, while the poles continued io cool, the tropical regime reversed and began to warm to the extent that for the most part, the lropics are warmer loday than they were at the close of the Cretaceous (Shackleton, 1984), As will be discussed below, this warming phenom- enon was used by Valentine (1984), in lieu of the biological factors af Théel (1911), in explaining amphitropical reliction via exclusion from the deep tropics. These two hypotheses stand in marked contrast to migralion across the tropics, especially during the Pleistocene, utilised by Darwin (1859) tn explaining amphitropicality. HYPOTHESES RELEVANT TO SOUTHERN HEMISPHERE ENDEMISM Five hypotheses relevant to the origin of Southern Hemisphere endemism are identified here, and they can be divided between three categories, The categorization is not intended to be precise; rather, itis simply to give us areas on which to focus, The hypotheses, listed here, are claborated upon below: T) Centres of origin. Il) Dispersal ta the Southern Hemisphere [ol- lowed by extinction in Northern Hemisphere (includes one form of amphitropicality, cf. If B, 2 below). If) Vicariance: Relict and relic biotas!; in- volves two processes (A and B), the second and sometimes the first being followed by extinction in the Northern Hemisphere: A.The breakup of Pangea and/or Gondwana. B. The breakup of Tethys. Relicts and relics of Tethys fall into two principal types: 1.Those resulting from division of the tropics. 2. Those resulting from exclusion from the tropics (second form of amphitropical- ity). I. CenTRE OF ORIGIN The taxon in question evolved in the region where il is found (Fig. 1). Species can certainly be found at or near their place of origin, but the probability decreases with the age of the species, and that higher taxa evolved where they are presently found decreases dramatically with tax- onomic tank. Therefore, a centre of origin hy- pothesis is risky unless one has an excellent Stralignaphic record. The hypothesis can often be falsified by the discovery of a single fossil or living population in the “wrong place’ and there- fore it should be proffered with caution. In order to emphasise this point, we cun now look at some examples of molluscs that would have fallen under a centre of origin hypothesis had it not been for the fossil record. Scattered populations of a gastropod, Nerifep- sis radula, range across the Indo-West Pacific, from islands off East Africa to the Hawaiian Archipelago. One might conclude that the pre- sent distribution includes the centre of origin. However, approximately 100 fossil species of Nerilopsis are recognised and N. radula, the sole surviving member of the Neritopsidae, is ilself known from the Eocene of the Paris Basin (Bat- ten, 1984). Hence, it is a Tethyan relic at the familial as well as generic and specific levels; u relic par excellence. Another Tethyan relic is the bivalve molluse Neotrigonia represented by six extant species found around Australia. They are the last surviv- A ‘relict’ population is one separated from a parent population by some vicariant event while a ‘relic’ population consists of the last survivors of an an- cient radiation. ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM 53 SOUTHERN HEMISPHERE ENDEMISM Hypothesis 1 - Centers of Origin *K Origin — West Wind Drift Dispersal (WWDD) %* Oceanic islands — 140* 100° FIG. 1. Hypothesis 1 — Centre of Origin. The origin of a hypothetical Southern Hemisphere endemic has been arbitrarily placed in southeastern Australia (large asterisk). The taxon may subsequently disperse, in this example, via the West Wind Drift (Fell, 1962) to South America, South Africa etc. (arrows) and involving oceanic island stepping stones (small asterisks; stippling indicates presence of established populations). Presence on oceanic islands is evidence for post-Gondwanan long-range dispersal (Newman, 1979a). The hypothesis can be falsified by fossil evidence from other continental sediments of Gondwanan age, or by appropriate evidence from the Northern Hemisphere. ing members of the Trigoniidae which became largely extinct at the end of the Cretaceous in the North Pacific and Europe (Stanley, 1984). Un- like the Indo-West Pacific Tethyan relic Neritop- sis, Neotrigonia is a Southern Hemisphere endemic as well, by virtue of having gone extinct in the Northern Hemisphere. The commonness of this latter pattern is illustrated by the following three relic gastropod molluscs of the Southern Hemisphere: 1) Campanile symbolicum of southwestern Australia, the sole surviving spe- cies of the Campanilidae which flourished in Tethys of the early Tertiary (Houbrick, 1984a); 2) Diastoma melanoides of southern Australia, the sole surviving species of the Diastomatidae which flourished in the Eocene of Tethys (Hou- brick, 1984b); and 3) Gourmya gourmyi of New Caledonia, New Hebrides, the Chesterfield Is- lands and Marion Reef of the Coral Sea, the sole surviving species of the genus which traces back to the Eocene of the Paris Basin, Tethys to the end of the Miocene, and the Pliocene of Japan (Houbrick, 1984c). As well as emphasising the value of the fossil record, the foregoing gives some perspective. While the course of extinction that led to these Southern Hemisphere endemics apparently had its roots in the Paleogene, it apparently did not become highly restrictive until the Neogene. These examples demonstrate how readily a centre of origin hypothesis can be falsified (Eskov and Golovatch, 1986; Newman and Foster, 1987) and the issue will be taken up shortly concerning some crustaceans. {I. DisPERSAL TO SOUTHERN HEMISPHERE Immigration from the Northern to the South- etn Hemisphere, with subsequent extinction in 54 MEMOIRS OF THE QUEENSLAND MUSEUM SOUTHERN HEMISPHERE ENDEMISM Hypothesis 2 - Dispersal A. Dispersal from the northern hemisphere to the southern hemisphere from mid-latitudes teSulting in amphitropicality. B. Extinction in northern hemisphere resulting in southern hemisphere endemism with or without WWDD, (ao* 90" \ao* 140° 100" so eo or 20 FIG. 2, Hypothesis 2 — Dispersal and Extinction. A, Dispersal of Northern Hemisphere propagules (stippled, planktonic or benthic) to the Southern Hemisphere, whereby the taxa involved become amphitropical (Darwin, 1859). Immigration is most easily accomplished where eastern boundary conditions exist (arrows), beneath a shallow thermocline and/or during cool periods such as the Pleistocene. B, If Northern Hemisphere amphitropical counterparts of Southern Hemisphere immigrants go extinct (crosses), the immigrants become Southern Hemisphere endemics. Southern Hemisphere immigrants may disperse via the West Wind Drift (arrows). Evidence needed to falsify hypothesis 1 generally supports this and subsequent hypotheses to one extent or another. the Northern Hemisphere, is a simple and been by way of high mountains for terrestrial straight forward way of explaining both am- forms, or across equatorial waters for marine forms phitropicality and Southern Hemisphere en- (Darwin, 1859). It is of course also possible to go demics (Fig. 2). Migration during the beneath tropical waters, especially under eastem Pleistocene, across the tropics, could have boundary conditions where the thermocline is GRIGINS OF SOUTHERN HEMISPHERE ENDEMISM 55 shallow and upwelling prevails (Ekman, 1953: Hubbs, 1952). The foregoing molluscan examples are nol envisaged as falling into this category because they were apparently originally wide-ranging Tethyan populations. Thus it may be difficult to decide berween this hypothesis and that covered under I!l B, 2 below, since both are two-step processes involving extinction in the Northern Hemisphere. But because the present hypothesis involves migration across the trapics rather than exclusion from the tropics in establishing am- phitropicality, the distinclion is important to our understanding. LL. VicaRIANCE Such hypotheses for the origin of Sauthern Hemisphere endemism involve two processes: A) the breakup of Pangea and Gondwanaland (Fig. 3); and, B) events included in and following the breakup of Tethys (Figs 4 and 5). A., Relicts and relics of Gondwanaland seem to be linvited printarily to terrestrial and fresh- water bjotas and examples among the freshwater crustaceans will be taken up shortly. B., Tethyan relicts und relics (I! B), on the other hand, include many marine forms. Two palterns can be identified and they need to be distinguished here. The first (Fig. 4) involves retreat of warm seas of the world, since the Cretaceous, towards centres of distribution. The second (Fig. 5) involves splitting of primarily Paleogene tropical populations into amphitropical populations beginning in the Oligocene (Kennett, 1982; Newman and Foster, 1987). Both processes may ultimately lead to hemispheric endemism, commonly in the Southern Hemisphere and espe- cially in the southwestern Pacific. AMPHITROPICAL DISTRIBUTIONS Examples of molluscs given above (the bivalve, Neovtrigonia, and the gastropods Cam- panile, Diastoma, and Gourmya) are all South- ern Hemisphere endemics with Tethyan histories. They appear to be a subset of the Indo- West Pacific relict pattern, a pattern also ob- served al bathyal depths by Ameziane- Cominardi et al, (1987) and Richer de Forges (1990). However, these authors do not explore the possibility of their once having been am- phitropical. Therefore we can move on to am- phitropical distributions and their role in the origin of Southern Hemisphere endemism. There are numerous examples of amphitropi- cal distributions (cf. Good, 1964; Van Balgooy, 1971; Randall, 1981, Springer, 1982; Briggs, 19872. b), and hypotheses regarding their origins were recently reviewed (Newman and Foster, 1987). There were pwo noted above deemed rel- evant to marine forms — that of Darwin (1859) involving migrations across the tropics espe- cially during the Pleistocene (Fig. 4) and that of Théel (1911) and Valentine (1984) involving the splitting of a previously tropical biota into north- ern and southern populations (Fig. 5). Darwin's (1859) hypothesis involved cooling during the glacial epochs whereby some terrestrial and marine plants and animals could have ranged across the tropics to become amphitropical wher the cool period abated. This hypothesis has heen popular with marine biogeographers studying fish and plankton, especially those working with plank- ton or under eastern boundary conditions such as along the shores of the tropical East Pacific, or elsewhere where upwelling occurs (Hubbs. 1952; Brinton, 1962; Van der Spoel and Heyman, 1983; Fleminger, 1986). Although the tropical East Pacific can become relatively warm during El Nifo period (Ramage, 1986) it is generally cool com pared to the same latitudes in the West Pacific due to prevailing currents from the north and especially the south, and the upwelling associated with them. From deep-sea drilling results, it is known thatthe belt was much narrower during the last glacial period, 18 000 YBP, than itis today (Moore ev af, 1980), Amphitropicality, established by migration actoss the tropics at such times, would then be followed by extinction, generally in the Northem Hemisphere whereby the Southern Hemisphere populations become endemic at some level, n the other hand, Théel’s (1911) hypothesis for the origin of amphitropicality concerns split- ting of tropical populations; that is, peripheral reliction through replacement in the deep tropics by more advanced forms via competition. Valen- tine (1984) looks as well to the physiolagical impact of warming of the deep tropics noted above under climatic change?, These two hy- potheses seem to go hand in hand since many modern forms (structurally more advanced and often known to be geologically younger) cam- monly dominate the deep tropics while some . Briggs (1987a) dismisses Shackleton’s eartier {emperalure curves for high and low latitudes over the past 100 MY because of a difficulty with the method due to water tied up in glacial ice. How- ever, he does nol cite Shackleton (1984) where the difficully is apparently taken into account. 56 MEMOIRS OF THE QUEENSLAND MUSEUM SOUTHERN HEMISPHERE ab aa = Hypothesis 3 - Vicariance SP Go ee EAS POR : (Relicts of are ie RF % : . Ry $i + & ; “a Oo : ; 1D ~ , India é a 1 2, Australia Bs : : 3, New Zealand ee 4, Antarctica ; Gig t+ +o 5, Africa ai cle an - 6, South America « A Lower Cretaceous (modified from vs Howarth 1981). i S ee Ree Paleogene (modified from Adams 1981) tas fe, FIG. 3. Hypothesis 3 — Vicariance. Relicts and relics of Gondwanaland. A, Contiguity of the six Gondwanan continents and the extent of Tethyan and adjacent epicontinental seas (stippled, modified from Howarth, 1981). Tethys virtually separated Gondwana from Laurasia during the Mesozoic, up through the Cretaceous. During this time, tropical Tethys formed a significant barrier to dispersal between Laurasia and Gondwana for terrestrial and freshwater forms. On the other hand, cosmopolitan elements of the Tethyan marine biota girdled the earth during this period via currents and oceanic islands of Panthalassa (Hamilton, 1956). B, Positions of the six Gondwanan continents by the Palaeogene (modified from Adams, 1981). The breakup of Gondwanaland apparently explains the distribution of many terrestrial and freshwater forms endemic to the Southern Hemisphere. ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM 57 older forms tend to be peripheral (Théel, 1911; Newman and Foster, 1987). Since temperature is presently apparently the primary factor in main- taining the separation between some amphitropi- cal populations, the current hypothesis is classified as vicariant. It is instructive in this regard that in situations such as the East Pacific some populations have not been split completely (Ekman, 1953) and these have been termed ‘par- amphitropical’s. THE METHOD USED FOR ANALYSIS The material covered in the foregoing introduc- tion includes areas of historical geology and clima- tology as well as considerations of present day distributions of some marine molluscs having a significant fossil record. These data were inte- grated to varying degrees into hypotheses involv- ing the origins of Southern Hemisphere endemism. This background can now be applied to the dis- tribution patterns seen in a number of freshwater as well as marine crustaceans. The question is often whether the present distribution of a given taxon is more or less as far as the radiation reached, or is the result of reliction of a once much wider pattern. Obviously to have been wide ranging, a taxon would have to have radiated at one time or another, but the place of origin and the direction of the radiation are usually lost in antiquity. Likewise, the course of a subsequent reliction is also often diffi- cult if not impossible to document. Distributions are plotted where appropriate, and inspected for the patterns noted above, plus other patterns such as amphi-Atlantic distributions in forms having no obvious means of dispersal. Patchiness, disjunctions, and latitudinal and longi- tudinal ranges are also very important, but above all there are the areas of endemism. Indications from the fossil record are also plotted if appro- priate. The patterns observed can then be checked against available hypotheses for Southern Hemi- sphere endemism; namely, origin, migration, Gondwanan and Tethyan relictions, and am- phitropicality. 3 The term ‘paramphitropical’ identifies transtropi- cal species, genera or even higher taxa that show preferences (relative abundance, condition, habi- tat, emergence etc.) for the higher portions of their latitudinal range (Newman and Foster, 1987; see Lyreidus tridentatus in the West Pacific, and Cancer in the East Pacific and elsewhere at bathyal depths in the tropics, in the following discussion). What little evidence there is, such as one im- portant fossil locality for the brachyuran Cancer (Miocene of Java) or two extant localities for the cephalocarid, Hutchinsoniella, is often taken at face value. This is certainly open to criticism but the conclusions drawn are generally falsifiable. Therefore, as long as the pitfalls are known, there is no harm in this approach since it appears to be capable of generating testable hypotheses having predictive value (Ball, 1975). CRUSTACEAN DISTRIBUTIONS Abele’s (1982) discussion of the biogeography of Crustacea includes some aspects of paleogeo- graphy, patterns of species richness, migrations and morphology. It also provides distributional information on the Cephalocarida, Branch- iopoda, Remipedia, Ostracoda, Mystacocarida, Branchiura, Copepoda, Cirripedia, Leptostraca, Hoplocarida, Syncarida, Pancarida (Ther- mosbaenacea), Mysidacea, Cumacea, Spelaeo- griphacea, Amphipoda, Isopoda, Tanaidacea, Euphausiacea, Amphionidacea and some De- capoda. This informative material includes bio- logical aspects such as habitat requirements, life history and dispersal capabilities. However, the single distributional chart given includes the Cephalocarida, Anaspidacea, Spelaeogriphacea, Mystacocarida, and Pancarida (Ther- mosbaenacea); a montage that is not particularly informative. Schram (1986) adds to this back- ground, in good part by plotting the distributions of a number of crustaceans on separate charts, some of which illustrate amphitropicality and/or Southern Hemisphere endemism. While both authors note the classical freshwater relicts of Gondwanaland such as Anaspidacea, Para- stacidae and Phreatoicidea, neither notes South- ern Hemisphere endemism among marine forms. RELIcTs AND RELICS OF GONDWANALAND Since Gondwanan distributions should be rela- tively easy to identify, and since this paper is primarily involved with the origin of Southern Hemisphere endemism among the crustaceans, some apparent Gondwanan examples will be given first. Abele (1982) reviews the situation for the branchiopods and argues that while pas- sive dispersal may occur, the distribution of genera may be more the result of continental movements. Likewise, Tasch (1987) concludes that the distribution of conchostracans between the five Gondwanan continents was by non- marine dispersal in the Palaeozoic or Mesozoic. sh MEMOIRS OF THE QUEENSLAND MUSEUM ‘These findings do nat precludes long-range dis- persal, but if it is taking place now it is not particularly evident. Much the same has been said for other fresh water groups; the Branchi- uran genus Dolops, the phreatocid isopods, par- astacoid astacurans, and anaspidaccans. According to Abele (1982), Dolops only occurs in Tasmania, South America and Africa, but itis parasitic on freshwater fishes whose distribucion is beyond the scope of the present paper. Perhaps the strangest cases can be made for the phreatoi- cids (Fig. 6A; India, Australia, Tasmania, New Zealand, and Africa but, curiously, wor South America), and parastacids (Australia and New Guinea, Tasmania, New Zealand, South Amer- ica, and Madagascar but not Africa or India) (Williams, 1974; Holthuis, 1986). The anaspidaceans apparently descended [rom the Palaeocaridacea, marine forms present in both the Northern and Southern Hemispheres from the Carboniferous into the Permian (Europe, North and South America; Schram, 1986). Since fossil anaspidaceans are known from only the Triassic and Cretaceous of Australia, we are left with the conclusion that they evolved there from marine forms. Gond- wana was essentially intact al the time and there- fore the occurrence of stygocaridids in New Zealand and South America as well as mainland Australia is consistent with (he hypothesis, It should be noted however that a rather well developed nauplius is passed through in the egg of Anaspides tasmaniae. This suggests that anas- pidaceans are not too far removed from having had larval stages and, judging from other malacostracans, this mdicates that they are not too far removed fram the marine environment. Therefore it is possible that the occurrence of stygocaridids in New Zealand and South Amer- ica in addition to Australia is a West Wind Drift distribution (WWDD, Fell, 1962) ra(her than # Gondwanaland pattern per se. This is much the explanation given by Feldmann (1986) for the caglid decapods of fresh waters in southwestern South America, except (hat {heir apparent ances- tor went extinct in New Zealand. Reuicts awp Reucs or TeTeys Molluses were used above in exploring Indo- West Pacific and southwestern Pacific ende- mism because their past distributions were well documented in the fossil record. All were Tesh- yan, yet some remained tropical while others, probably having had an .amphitropical compo- nent, became Southern Hemisphere endemics, There are numerous crustaceans that appear to be Tethyan relicts, but the degree to which these are documented by the fossil record varies con- siderably. There are some caridean shrimp, in- cluding Procaris, that are relicts without a Lossil record. They are particularly interesting because they are largely restricted to refugial hypogeal and anchialine habitats and then frequently on oceanic islands of the Atlantic and Inda-West Pacific Oceans (Abele, 1982; Maciolek, 1983; Hart er a@l., 1985; Schram, 1986). The refugial aspect of oceanic island cannot be over emphasized, as illustrated by the distribu- tion of some other shallow water crustaceans of the Indo-Pacific and Atlantic; namely, the acorn barnacle Tesseropora (Oligocenc—Recent) anda species each of the burrowing barnacles (Dev- onian-Recent) Lithoglyptes and Kochlorine (Newman and Ross, 1977; Schram, 1986, re- spectively). Both of these groups are more re- stricted in the Atlantic than in the Indo-Pacific, so thatifreliction continues one might expect the Atlantic populations would go extinct first. While there is evidently a greater diversity of Tethyan relicts in the Indo-Pacific than in the FIG. 4, Hypothesis 4 — Vicariance. Deep tropical relicts and relics of Tethys, A, Contemporary configuratiun ofthe world with the approximate limits of the tropical bell (stippled). Barriers to transtropical dispersal that Jed to the tropical provincialism We see today include: 1, the Australiane-New Guinea/southeast Asia closure (Upper Miocene) blocking equatorial currents between the Pacific and Indian Oceans; 2. the East Pacific Barrier or islandless track between the black bar and the Americas; 3, the Pananiic closure (Pligcene) separating the East Pacific from the western Atlantic; 4, the opening up of the Atlantic (cf, Fig. 3); and 5, the closure at Suez (Miocene). B, Decline of Tethyan tropical elements concomitant with evoling al the poles and warming of the tropics, the latter beginning in the Miocene (Shackleton 1984) and the formerculminating in the Pleistocene. Principal relict areas initially in; 1, the West Pacific; and 2, the western Atlantic, but also 3, in Europe/North Africa apparently due to the Gulf Stream, Deep tropical elements belonging to this class had pretly much gone extinet jn the East Pacific and most of the eastern Atlantic, concomitant with the loss of coral reefs"there (Newell, 1971), C, Further decline of this class of relicts included extinction im the Northern Hemisphere and much of the Southern Hemisphere, except for the Indo-West Pacific, Of particular interest here are West Pacific endemics, some of which became restricted to the southwest Pavific as Southern Hemisphere endemics. ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM Atlantic, there are some crustaceans at high tax- onomic levels that appear to be endemic to the Atlan- tic; mamely, the Remipedia. Pancarida, Spelaeogriphacea, and the Mystacocarida (Pancarida and Mystacocarida have recently been discovered elsewhere). These groups are restricted to anchialine. oF tags 1o0* /aor Hypothesis 4 - Vicariance (Relicts of Tethys) A = SOUTHERN HEMISPHERE ENDEMISM 59 brackish, fresh water hypogeal and marine interstitial refugial habitats, Unlike the shrimp just noted, they are blind and otherwise have life histories that are apparently not conducive to long range dispersal. The Remipedia, known from the Caribbean and allied ta Tesiusocaris from the middle Car- o* 2 ud zor IN : 1, Australia-N.G./Asia closure, U. Mio. |? 2, East Pacific Barrier, islandless track from line to shore. , Pamic closure, Plio. Opening of Atlantic, Cret. 5, Red Sea closure, Mio Principal relict areas: tert Decline of early Tethyan especially in Northern Hemisphere. “ - Extinction in northern hemisphere and further restriction in W. Pacific resulting in S. Hem. endemism. - HHH A tropical elements, 1, Western Pacific _ 2, Caribbo/ W. Atlantic 60 MEMOIRS OF THE QUEENSLAND MUSEUM boniferous of Texas at the time of Abele (1982), have since turned up on the opposite side of the Atlantic, in the Canary Is. (Schram, 1986, fig. 3-3; Schram et al., 1986, fig. 39). Likewise, the Spelae- ogriphacea, known to Abele (1982) from fresh- water caves in South Africa and from the Carboniferous of Canada, is now known from freshwater in Brazil (Pires, 1987). 100" 140° a0" iE lehd SOUTHERN HEMISPHERE ENDEMISM Hypothesis 5 - Vicariance (Amphitropical licts of Tethys) Pancarids were originally known from various ground waters around the Mediterranean, from anchialine situations in the Caribbean, and fresh- water caves in Texas (Stock, 1976; Bowman and lliffe, 1988; Schram, 1986, fig. 17-3). Abele (1982) summarises the explanation of Stock (1976) and previous authors for their amphi-Atlantic dis- tribution; namely, Tethyan relicts ‘stranded’ in- of 1, Endemics shared by Hawaii and the 3, Occasional occurrence of member of S. | S.E. Pacific. 2, Endemics shared with Hawaii and the | *“) SE. Pacific. ¢1, Hem. endemic group in N. Hem. i CaS § |. 4, Ndi | C. Extinction of most northern hemisphere amphitropical counterparts. ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM 61 land by changes in sea level during the Miocene. But it needs to be recalled that the Miocene Atlantic was nearly as wide as it is today, and Schram (1986), citing Macquire (1965), favors plate tectonics as the vicariant event. Pancarids co-occur with remipeds in the Caribbean (Bow- man and Iliffe, 1988) which also occur on both sides of the Atlantic, as does one species of cephalocarid to be taken up below and the spelacogriphaceans in fresh water noted above. Thus, the situation for pancarids is evidently better explained by a tendency to enter ground water and other refugia prior to the opening up of the Atlantic. This is especially attractive when it is noted the Texas locality appears to be on the edge of the Mississippian embayment. That there are insome respects more primitive representatives in marine situations in the Caribbean (Bowman and lliffe, 1988) is not at all incompatible with an explanation involving reliction via opening up of the Atlantic unless one is willing to speculate that Monodella evolved independently on both sides. Schram (1986) noted that the distribution of pancarids was congruent with that of certain copepods, mysids, isopods and amphipods on both sides of the Atlantic, and that representatives of the last were also known from the Indo-Pacific. Thus, these groups are Tethyan relicts. That the Pancarida was also in fact once a wide-ranging Tethyan group was recently revealed by the discovery of a species in Cambodia (Cals and Boutin, 1985). Until recently, the mystacocarids presented an enigma to me because they could be envisaged either as having extended their range from the Atlantic around the southern ends of South America and South Africa into the southern ex- tremes of the Indo-Pacific since the Cretaceous (Schram, 1986, fig. 34-4, a centre of origin hy- pothesis), or as having been excluded from oceans of the world except the Atlantic. The latter, a reliction hypothesis, received some sup- port in the fact that their present distribution is apparently amphitropical and that the South American species belong to a distinct genus, Ctenocheilocaris (Hessler, 1988), whereby di- versity is greater in the Southern than in the Northern Hemisphere. Since this symposium, R.R. Hessler has shown me a photomicrograph of a mystacocarid B. Knott sent from Western Australia. Therefore, as far as the present pattern is concerned, the centre of origin hypothesis has been falsified. But, as with virtually all groups, we still do not know when or where the mysta- cocarids originated. AMPHITROPICAL DISTRIBUTIONS Schram (1986) plots a number of distributional patterns, several of which, including that for the mystacocarids just noted, can be observed to have an amphitropical component. One involves the bathysquillid hoplocarids which apparently have Jurassic affinities. They are known from the Caribbean, and also from the Indo-West Pacific where they are amphitropical (Schram, 1986, fig. 5-7). Then there is the asellote isopod, Nan- noniscus, dubbed by Schram (1986, fig. 12-6) as ‘ubiquitous’ but actually as far as it is known strongly amphitropical, especially in the Atlan- tic. Another of this group might include a wood- boring amphipod, Chelura terebrans, of the North Atlantic, South Africa, S.E. Australia and New Zealand had it not been inferred that the FIG. 5. Hypothesis 5 — Vicariance. Amphitropical and paramphitropical relicts and relics of Tethys: A, Contemporary configuration of the world with the approximate limits of the tropical belt (stippled, cf. Fig. 4A for fuller explanation). Tropical forms are not equally steno- or eurytopic, nor do they have identical temperature optima. Consequently there are patterns within such a uniformly stippled area reflecting these and other characteristics, such as substrate or water mass preferences. B, Evolution of advanced, presumably more competitive tropical forms (Théel, 1911), and/or warming of the tropics beginning in the Miocene (Valentine, 1984), excluded many older elements from the central and deep tropics. Thus a distinct class of Tethyan relicts known as paramphi- and amphitropicals was produced (stippling), Paramphitropicals tend to occur under eastern boundary conditions, as indicated by the stippling in the East Pacific. The eastern Atlantic could also be stippled, but examples of paramphitropicality are apparently uncommon there. These patterns can be detected to varying degrees in both oceanic and coastal forms. C, With further reliction, many Northern Hemisphere populations become extinct, whereby their Southern Hemisphere counterparts become endemic. The fact of extinction in the Northern Hemisphere is based on the fossil record, although some quasi Southern Hemisphere endemics (widely distributed populations in the south but with some Northern Hemisphere representation) can be interpreted as belong to this class. Remnants of previous connections with the Northern Hemisphere include 1, endemics shared between Hawaii and the South Pacific, 2, endemics shared with the East Pacific as well as Hawaii and the South Pacific, and 3, endemics having representation elsewhere in the Northern Hemisphere such as in the northeast Atlantic as indicated here (Newman ,1986; Newman and Foster. 1987). 62 species had been introduced to the Southern Hemi- sphere (and to Califomia) by ships. Abele (1982) and Hessler (1984) review and Schram (1986) plots the distribution of cephalo- carids (Fig. 7A), but none attempts to analyse the overall pattern. [t can he argued the distribution is poorly known and likely too incomplete to allow an analysis. Afterall, there are but four genera, nine jane A. ISOPODA™= & Uilehd ace VAY Phreatoicidea, U. Carb. (Penn.)-Recent_ 3.1 Amphisopodidae, Trias.-Recent Nichollsiidae, Recent Phareatoicidae, Recent MEMOIRS OF THE QUEENSLAND MUSEUM species and about eleven localities in the world to work from, At first glance the pattern may appear little more than random, but on close inspection and the application of biogeographical principles, patterns be- come evident. The first cephalocarid genus, Hutchinsoniella, was described some 40 years ago. Itis still monotypic and known only from the Adantic where, instructively, ES a 2, Australia | | 3, Tasmania + = eo 4, New Zealand ee : 5, S. Africa ‘ + Palaeophreatoicidae, Penn. - Permian ['B. ANASPIDACEA (Trias. - Recent) sro 2578 a —— j 6 < = t/ 1 . Stygocarididae , Koonungidae Anaspididae Psammaspididae |go* | bs A 2 \ r Palaeocaridacea, Carbo. - Perm. oar 20° o 7 ORIGINS OF SOUTHERN HEMISPHERE ENDEMISM 63 it is amphitropical (Fig, 6A), The second genus, Lightiella, discovered jn California at about the same time, is now known by twa species from the Caribbean and one from New Caledonia (a relatively isolated southern outpost). It is there- fore at least Tethyan as well as amphitropical in distribution, Likewise, species of Sandersiella, a genus first described from Japan, have turned up on both sides of South Amenca, with that from the east coast (southern Brazil) also occurring on the southwest coast of Africa (Namibia), Thus, not only are all three of these genera wpparently amphitropical, two are Tethyan, and the last as amphi-Atlantie (Hessler and Sanders, 1973) at much the same latitudes as the Spelueogrphacea noted above. And finally, there ts the monotypic New Zealand genus Chiltonella, whose dis- covery makes the diversity of cephalocirids greater in the Southern than in the Northern Hemisphere. Along with the species of Livsir- iella from New Caledomia, these taxa have a geographical refugial aspect to their distribution in addition to their minuscule size and habitat, Abele (1982) notes that there has been little local differentiation among cephalocarids and therefore concludes that they are specialists rather than gencralists as suggested by Hessler and Sanders (1973), There is no question that they are specialised in size and structure for the refugium afforded by floeculent sediments, and it is probably characteristic of forms so limiled, like the mystacocarids in interstitial waters, to show little subsequent diversification. But there is also no question that while specialised, cepha- locarids have retained printitive traits known in ray other living crustaccans, such as uulising the antennular gnathobases for feeding, multiple ontogeny stages, and second maxillac which are almost indistinguishable from thoracic limbs (cl. Miiller and Walossek, 1988). Furthermore, the cephalocarids had to evolve from something not too dissimilar, and there is nothing living from which they can be derived (Hessler and New- man, 1975), Th Consideration of this wand therr highly relict geographical distribution, it ts clear that the more generalised ancestor of cephalo- carids entered this refugium a long time ago (Hessler and Sanders, 1973), likely before the breakup of Pangea and certainly belore the breakup of Gondwanaland. Ostracod biogeography is reviewed hy Abele (1882) who cites previous. authors who have noted, for example, some freshwater forms with Brazil West African affinities daltable to conti- Hental conpections during the Early Cretaceous. He goes on to note that arguments for passive dispersal via birds etc. cannot be excluded, as they so readily can for other trans-Atlantic en- demics including the species of Sandersiella and the spelaeogriphaceans noted above whose amphi-Atlantic aspects could well date back to the same epoch. Schram (1986) plots two distributions (Fig. 7B, C) displaying amphitrapicality, one fromthe fresi- water isocypridine ostracods, the other for the marine genus Saida, the latter being the most rele- vant here, The fossil record for Saida begins in the Cretaceous and ends in the Paleogene in northem Europe (Fig, 7C), It also begins in the Cretaceous of Australia where it survives today, Until recently the genus was thought to have gone extinct in the Northern Hemisphere whereby it was considered a Southern Hemisphere endemic. Mowever, there are now (Whatley, pers. comm,) several additional Reeent localities known in the world (on the Morida Slope and in the South China and the South Scotia Sea: Fig. 7C). Thus, the genus may presenily be puaramphitropical. Whatever the case, the &x- ample of Saide appears to be close to, ifnata subset of, Fleming's (1979) observation that much of the manne fauna of New Zealand (and hence at leas southeastern Australia) had its roots in northern Europe where it died out in the Miocene, If it were not for the fossil record, we would FIG. 6A, lsopada, Phreatoicides, Known from uur of the six Gandwanan continents ineluding India. While the Phreatoicidae and Nichollsiidae (stippled) wre Recent, the Amphisopudidae are known as fur back as [he Triassic. This is strongly indicalive of a Gondwana distribution, especially since they are freshwater forms, However, their northern hemisphere counterpart. the Palaeophreatoicidae (crosses). are sufficiently old (Pennsylvamun-Permian, Schram. (986) tu make them relics of Pangean as well, B, Synearida, Anas- pidacea; The distribution of anuspidaceans cenlery on southeastern Australia, wilh one of the lour families ranginy cast (6 New Zealand and southern South America. Known from fresh witer as far back as the Triassic, their closest relatives, the Palueoearidaces (Cerhonilerous—Pernmian), are known from marine depastts in North and South America as well as Europe (crosses, Schram, (986), Like the phreatuicids, conventional wisdam is that anaspidaceins are Gondwanan telicls af Pangea. Flowever, their closese ancestors, the palaeocaridaceans, Were marine, and 4 Well developed mauplius is passed through in the ege af at least Anaspides. Therefore, the ncvurrence of one family in New Zealand and Sourh Ameriva could have been by West Wind Drift dispersal ralher hun via the breakup of Gondwanaland, 64 AA any anaceatli}) ANIL, # bisexual Q, 1 1, Cretaceous 2, Paleogene 3, Neogene 4, Recent after McKenzie 1973 40) ALOCARIDA . socypridinae %*& parthenogenetic C.OSTRACOD MEMOIRS OF THE QUEENSLAND MUSEUM OUI nibrook suggested, consider the punciids as re- lict, a shadow of their former selves, the Kirkbyacea —the assumed ancestral stock of the Punciacea (Swanson, 19894) — whose more re- eent (IS MY — Beira day) distribution (Fig. 1) ina series of isolated, Widely-distributed pockets is the remains of a diversive/dispersive event which chmuaxed some three ta four hundred mil- lion years ago. MUSCLE SCARS In ostracod taxonomy, muscle scars are an extremely useful tool. Most specimens (fussi! and living) of punciid ostracods display a full complement of well-preserved sears; in contrast, Tépresentalives af the Palagozoic Kirkbyacea, although nearly always. presenting the charac- teristic ‘kirkbyan pit’ externally, more often than not have the internal muscle scar detail oblit- crated as a result of imperfect preservation (G. Becker, pers, comm.), In his description of the central muscle scar ficld of one group of kirkby- aceans, Sohn (1954) concluded ‘...ceven the best preserved specimens show only one knob on the inside of the valve without any trace of areas of attachment of accessory muscles’. Results of a recent re-examination of a number of Sohn’s types indicate a variety of muscle scar types as diverse as that expected for ‘modern’ padocopid ostracods. The cumplete muscle scar pattern for punciids was first described by McKenzie and Neil (1983) from the carapace of a new genus Promanawa. \t consists of a central adductor group Of six sears arranged biserially, two dorsal scars (the larger occurring on an elevated node) and a single mandibular scar. Frontal scars were considered absent. Such a pattern, they can- cluded, indicated the punciids were benthic crawlers with a mandibular coxale capable of a transverse biting action (Swanson, 1989b), The kirkbyid pattern, assuming Aurikirkbya worden- sis (Hamilton, 1942) is representative, also possesses two dorsal scars and a weakly developed mandibular scar (Becker, 1989). In contrast however, the central adductor area con- sists of an undifferentiated node and a frontal scur is also present. Becker (1989) concluded that this species was probably a nectobenthic filter-feedér, Ostracods generally exhibit a variety of often quite complex central muscle scar patterns. Thus, it seems probable that an apparent lack of differentiation in the kirkbyid node reflects imperfect preservation rather than some anatomical peculiarity. Contrasts in the central muscle sear fields, as they are presently understood, cannot therefore be used reliably as evidence againsta kifkbyacean-punciacean con- tinuum. Additionally, as noted by McKenzie and Neil (1983), Promanawa uustraliensis does have a well developed *kirkbyid pit’ externally; other members of the Punciidae do not, presum- ably because they have a much weaker reticulum FRILL ‘The punctid selvage is at least an analogue of the velar ridge in Beyrichicopida and might well be homologous with it’ (McKenzie and Neil, 1983), This is not supported by my work on Manawa which indicates that the ventral lunettes are structurally and functionally (2) quite dis- tinct. From the outset, discussion on the relation- ship between the extant Punctidae and a possilic Palacozoic predecessor has invariably been dominated by the presence/absence of ho- mologous structures in the frill, “In summary, then, | see no objective basis to separate Punoia and Manawa from the Palaeozoic Beyrichiidae, which as [ understand them include Palaeozoic straight-backed ostracods, with both cardinal an- gles well defined; a marginal frill typically ex- tends adjacent to the free margins from cardinal angle to cardinal angle; the frill is doubly walled and has inner partitions corresponding to exter- 80 MEMOIRS OF THE QUEENSLAND MUSEUM PUNCIID OSTRACODS 81 nal radial striae; in general, dimorphic pouches are formed by swelling of the frill, but such pouches are unknown in several early, primitive genera’ (pers. comm. from F.M. Swartz to N. de B. Hornibrook). In most respects our assessment of the Palaeozoic ostracod frill remains un- changed, acknowledging that ‘the ability of forming adventral extensions has been acquired independently in different, remotely related groups of Palaeocopa’ (Jaanusson, 1957). With the availability of modern analogues/homo- logues (Puncia and Promanawa), it is now possible to compare and contrast this unique structure in detail. The total number of chambers in each frill is quite variable: 35 in Coronakirk- bya hamori, (Kozur, 1985), noting the specimen is fragmented; 37-38? in Coronakirkbya krejci- grafi, fragmented; 31 in Aurikirkbya sp. A also fragmented (Becker, 1978); 55 in Coronakirk- bya fimbriata (pers. comm. G. Becker). This pattern is repeated in the Punciacea: 28 in Puncia goodwoodensis, (Hornibrook, 1963): 40 in Promanawa australiensis, (McKenzie and Neil, 1983); 42 in Puncia novaezealandica, (Horni- brook, 1963); 43 in Puncia sp. A (Fig. 2E). In Puncia and Promanawa the septa which divide the frill into approximately 40 chambers are not radial pore canals (Swanson, 1985); addition- ally, access to the domicilium via these chambers is prevented by a thin, calcareous (?) wall or membrane (Fig. 4B). At the ventral edge of the frill, each chamber may be completely or only partially sealed, the latter resulting from in- complete calcification (Fig. 4B). A similar situa- tion occurs in most Kirkbyacea, in the hollinacean Oepikium and in eurychilinids (Jaanusson, 1957), noting however that in these Palaeozoic taxa most chambers are circu- lar/ovoid in section rather than rectangular. Al- though some specimens give an indication that the kirkbyid frill is composed of a row of distinct tubules, I suspect that this is an artefact of pre- servation/extraction and that in life the gaps be- tween individual chambers were closed by a thin calcareous bridge. Ventral chamber exits, where present, were also extremely small since in many instances the ventral extremity of the calcareous bridge is tapered to a fine edge (Becker, 1978, pl.3, figs 17a—c, 18b). Determination of the func- tion of the frill must await the discovery of living specimens of Puncia or Promanawa, however the possibility that these structures performed a dual role as both benthic support and gas-filled floatation-aid cannot be excluded. Adamczak (pers. comm.) has also found some form of mem- braneous (?) closure in the crumen of the Ordovi- cian genus Craspedobolbina; this he felt could indicate a ballast/brooding function for that structure. Although McKenzie and Neil (1983) suggested the punciid frill did not appear till quite late in ontogeny (‘until after the develop- ment of the anlages of reproductive characters in the soft anatomy’), evidence from imperfect ontogenetic sequences for Puncia (Fig 2A — E), Aurikirkbya and Coronakirkbya (Becker, 1978, pls. 3, 4) indicate that it is carried by ‘early’ juvenile stages as well. PORES AND SETAE Marginal pore canals with their associated setae, as found in most podocopid ostracods, do not occur within the Punciidae. Okada (1982) observed that in some taxa (Bicornucythere bisanensis) ‘no pore runs along the marginal zone, though many pores appear to run radially in the marginal area of the carapace when ob- served from the lateral side with a light micro- scope’. One may conclude that in some podocopids the so called marginal pores are in fact wrongly identified. The stratigraphic record of ostracods gives clear evidence that the contact margin between the two valves has been a zone of considerable evolutionary innovation. In- creasingly, workers on Palaeozoic assemblages are recognising a wealth of structural detail in the calcified inner lamella and it is now established that the lack of a duplicature is not a determinant of the ‘palaeocopid’ condition (Gramm, 1988; Schallreuter, 1988). In Manawa and Puncia the upper surfaces of the carapace are pierced by evenly-spaced, small, simple sensillia or ‘nor- mal’ pores. The sole’ of the manawan valve FIG, 2. Scale bar = 200 um unless otherwise stated. A-E, incomplete ontogenetic sequence for Puncia sp.A. Cavalli Islands, New Zealand, 17 metres. Note progressive reduction in sub-dorsal protuberance towards adulthood. F, Coronakirkbya fimbriata juvenile paratype, Lower Permian, West Texas. USNM 118486. Scale bar = 300 um. G, Puncia sp.B. Cavalli Islands, New Zealand, 17 metres. Juvenile? Compare and contrast sub-dorsal nodes with Figs B and H. Scale bar = 100 um. H, Puncia novaezealandica Cavalli Islands, New Zealand, 17 metres. Note sub-dorsal spines. Scale bar = 100 um. I, Promanawa exposita Upper Cretaceous erratic, Insel Riigen, Jasmund, Germany. Scale bar = 100 um. J, Puncia levis Upper Cretaceous erratic, Insel Rigen, Jasmund, Germany. Scale bar = 100 um. MEMOIRS OF THE QUEENSLAND MUSEUM PUNCTID OSTRACODS 85 displays an inner (close ta the contact margin) and outer row of pores from which moderately long sensory setae exit (Figs 3C, 4F). A single row of between 12-15 equivalent pores and setae may be found on the proximal edge of the upper surface of the sole (Fig, 3A). Examination of the carapace of Puncia between the frill and the contact zone clearly indicates thal the manawan pore pattern is repeated in this genus (Fig. 4A, Significantly, the outermost row of sctae on the ventral (when the carapace is gaping) surface of the frill are extremely long (equal to the total width of the frill in most cases). The flexibility of these setae (Fig, 4A) suggests 4 sensory role within the cavity created by the frill and the substrate, rather than one associated with the lateral extremities of the frill, Clearly, as the carapace gape is increased the distance between the contact margin (and therefore the animal) and the substrate is reduced to a point where such setae would no longer drape; in fact during am- bulatory excursions if rs likely thal they are drawn across the substrate. I? the punciids are capable of dispersal by floatation, itseems likely that the animal would then assume a pas- sive/defensive role, i.c, the carapace would be closed; during such times extreme selal length in an afea surrounding the carapace opening would obviously be advantageous. Details of pore Lypes and their distribution for Palacozoic ostracods remain scanty, although pores have been used as stable ‘landmarks’ in a recent study of evolutionary change in species of Amphissites from the Lower Carboniferous of Australia and Upper Caroniferous of Texas (Jones, 1988), From my examination of micro- graphs of Coronakirkbya fimbriata | see no evi- dence of pore exits similar ta [hose found an the underside of the punciid frill (Pig, 4A). In all instances, however, specimen/detectar angles ' Examination of the contact margin to determine the existence of a duplicalure and its relation to the gules lamella have not been undertaken. Note however the structural blue-print for the sale is established with the carapace of the nauplius. were not optimal for such a search. One row of assumed pore exits (Fig. 4D) does.clearly dupli- cate that found on Puncia close ta the contact margin (hig. 4+C). Because of their position close to the contact margin/sole, these may be con- sidered analogues of ‘modern’ podocopid margi- nal pores which penetrate the carapace between the outer Jamella and the duplicature. There is some evidence to suggest that the oldest ‘ostra- cads’ (see discussion Swanson, 19894) were also open-gaped with pore exits concentrated on the carapace sole in a fashion similar to thal ex- hibited by Manawa. The setal arrangement in Puncia therefore could represent an evolutionary intermediate step appropriate to a wide-gaped ostracod, in which a domiciliar ‘early warning’ system is afforded by the frill and extremely lonz setae. In extant benthic podocopid ostracods, because of their vertical orientation, carapace shape and narrow gape, the greatest concentra- tion of the longest and most diverse sensory receptors (marginal pores and their setae) occur around the valve periphery near the contact mur- gin. Lopes In both the Kirkbyacea and the Punciidae some representatives carry externally near their dorsal margins structures ranging from “lobes” (used adyisedly since Jaanusson, 1957 considered lohes as external expressions of internal relief) as in Auridirkbya and Coronakirkbya to bulbs, ridges und spines, as in Puncia (Figs 2 E, G, H). An incomplete developmental sequence for Puncia sp, A (Figs 2A —E) clearly illustrates the progressive reduction in relief of two perforated, mid-dorsal, admarginal ridges. Although equiv- alent hollows are found on the interior of the valves, they are poor reflections of the extemal condition, especially in juvenile valves. Struc- tural duplicates (for which subsurface and inter- nal carapace detail is not available) in the Kirbyacca show a similar developmental pattern through ontogeny. In species of Puncia, the shape of these admarginal lobes is extremely vanable; elongate, bulbous and spinose forms all occurring in the New Zealand assemblage (Figs FIG. 3. Scale bar = 100 ym unless otherwise stated. A, Manawa tryphcna Cavalli Islands, New Zealand, & metres. B, Manawa stacey Cavalli Islands, New Zealand, 17 metres. Entire carapace in life position. CL Manawa staceyi Cavalli Islands, New Zealand, 17 metres. Entire carapace in life position inverted to expose soft anatomy. D, Manawa staceyi Cavalli Islands, 17 metres. Nauplius, Note slight bending of carapace. E, Manawa staceyi Cavalli Islands, 17 metres. Naupliar carapace. Arrow indicates double-walled nature of sale. F, Manawa staceyi Cavalli tslands. {7 metres, Metunaupliar carapace. G, Melometasus syliensis Ordovician, Isle of Sylt, North Sea. Geologiseh - Paldontologisches [nst(tii der Universitat Hambure (GPTH 2223), Oblique view of “larval'’ carapace. H, Vertical view, specimen as for 3€7. S OF THE QUEENSLAND MUSEUM MEMOIR 84 PUNCIID OSTRACODS BS 2A; 3G, H). Alternatively, in Manawa (Fig. 3A, B), Promanawa (Fig. 21) and Puncia (Fig. 21) lobate surface-swellings may occur in zones equivalent ta Li and L3 on paleocopids. Functionally, the more compact and defined ridges, knobs and spines remain a mystery. The fact that theif surface expression is more pro- nounced earlier in ontogeny suggests some form of Jarval aid, noting that the subsurface detail in adults has not been investigated. Shape does not appear lo influence the basic pattern of the com- ponents making up the larval admarginal ‘lobe’. The dome or roof js always smooth and, unlike the rest of the carapace, unperforated; the lobal floor has a tough texture which suggests the epiculicle envelopes the entire structure, Lastly, the basal periphery of the lobe is interrupted by a number of portals in which the carapace per- forations are organised in a roughly semi-circu- lar pattern (Fig. 4G). INTERNAL STRUCTURE Earlicr (Swanson, 1989a), I gave an indication that the internal structure of the punciid carapace also warranted further investigation, In both Manawa and Puncia, numerous, small (2—S,um) ‘ducts’ perforate the carapace wal) perpendicu- lar ta the external surface, excluding lobes und frills. or their equivalents (Fig. 4B,1; Swanson, 1989a, pl.2, fig. 10). In benthic podocopid ostra- cods, the calcified partion of the carapace con- sists of a reticulate chitin fabric the interstices of which are filled with fine crystals of calcium carbonate; in those ostracods (c.g. pelagic my- odocopids) for which flexibility and/or low weight seem a priority a lamellar chitin structure similar to that found in decapod Crustacea oc- curs (Bate and East, 1972, 1975), The carapace of most podocopid ostracods is also piereed by small’ normal’ pores which display an enormous variely of form. Generally. such structures pra- vide (a) exits for sensory setae and (b) accam- modation for basal accessories of such setuc. Both Manawa and Puncia do have normal pore exils bul these are easily distinguished from the perforations presently under discussion (Swan- son, 1989a, figs 2,3, 9, 10; Fig. 4F, 1) by the fact that the latter do not have setae. They may he densely-packed, simple, vertical tubules (Pre- cia, Fig. 44, B, G) or larger countersunk forms in which the external nm is either papillate (Manawea staceyi, Swanson, |989a, figs 3, 5) or spinose (Manawa tryphena, Swanson, 19894, fig. 2). Both manawan types of duct are ex- tremely complex internally with ‘epicuticular’ lining forming 2-3 continuous, membraneeus bridges across each duct. Studies of the calcified portions of the ostra- cod carapace clearly indicate that such structures are an economic solution lo an architectural problem. ‘The carapace is impregnated with massive layers of calcite during the molting and consequent growth process (unlike phyllopods- and cladocerans). The result is a heavily ar moured animal. There have existed through ge- ologic lime as many 4s Wwenly to thirty thousand species, all representing experiments.in carapace design. As unlikely as the basic body plan may stem, if has obviously been successful’ (Benson, 1981). As could be anticipated, therefore, the carapace of benthic ostracods is internally coher- ent with few breaks (normal pores) interrupting “that continuity and often with external beams and ridges providing additional strength at a FIG. 4. A, Puncia sp.A, Cavalli Islands, New Zealand 17 metres, Internal surface of frill (lef{= ventral) showing pore exit and seta (arrowed). Scale bar= 20 jim, B, Puncia sp,A, Cavalli Islands, New Zealand, 17 metres Longitudinal section of frill showing exposed chamber and septa {upper surface = ventral). Note break is slightly oblique therefore top of next chamber also exposed, Arrow indicates ‘caleareous” membrane which closes the damicilum to the frill. Note also imperfect caleilicution of frill at distal (right hand) extremity. Seale bur = 20 pn. C, Puncia sp.A. Cavalli Islands. New Zealand, 17 metres, Frill and external ventral periphery of domicilium. Note pore exists and sétue (arrowed) below curapace sole. D_Coronukirkbya fimbriata Lower permian, West Texas. USNM 118488. Ventral periphery of domicilium showing assumed pore exists (arrowed), Scale bar = 30 um. E, Corenakirkbya fimbriaia Lowet Permian, West Texas. USNM 118488, Ventral view of entire carapace, contact margin at top of picture, Seale bar = 300 gum, F, Manawa stacey! Cavalli Islands, New Zealand, 17 metres. Contact zone or sole of left valve showing two rows of pores ancl associated setae. Scale bar = 20 um. G, Puncia sp.A, Cavalli Islands. New Zealand, 17 metres, Subdarsal protuberance. Note carapace perforations continue under postal (arrow) and contrasting texture of external carapace surface and protuberance floor, Scale bar =20 pm, H, Aurikirkbya wordensis. Middle Permian, West Texas, USNM 110232a. Partial view of surface reticulation. “Membranous” closure (partial) al base of sach reticulation arrowed. Seale bar = 60 jam, |. Manawa siaceyé Cavalli Islands, New Zealand, 17 metres, Note “equivalent” partial closure of one rericulation (arrowed), Scale bar = 4 um. 86 MEMOIRS OF THE QUEENSLAND MUSEUM PUNCILD OSTRACODS 87 minimum cost physialogically (Sylvester-Brad- ley and Benson, 1971, figs 1-3: Bate and East, 1972, fig. 2; Okada, 1982, text-figs 1, 16). Why have the punciids taken the development of carapace perforations fo such extremes? One possible answer lies in the unique gait of the animal. Whilst walking, both valves are carried aloft and extended, supported by relatively thin and poorly chitinised cephalic and thoracic ap- pendages. I have already indicated thata pivotal, side to side rocking motion for Manawa slaceyt as it walks (Swanson, 1989a) would suggest that the weight loss, resulting from a densely per- forated valve, provides a partial solution to some locomotory problems, The felatively high den- sity of perforations in Manawa may be used also as additional evidence to indicate the value of ihe frill of Puncia as a buoyant balancing aid. Al- most all Kirkbyacea present a punctate pattern externally which duplicates that described for the punciids. Whether these negative carapace features penetrate the entire thickness of the carapace wall in the Palaeozoic forms is un- known. In some kirkbyids, however, the internal ex- pression of the reticulum (if it exists) could be masked by a very thin ‘calcified’ membrane which may tepresent an extension of the inner lamella (H. Kozur, pers, comm.). Such a mem- braneous layer is commonly encountered in specimens of punciid ostracod and although ex- (tremely thin and transparent is sufficiently elec- tron dense to obscure structural detail below (Swanson, 1989a, fig. 14, top right hand third of micrograph). Becker (1989) has also described subsurface closures of puncli in the kirkbyid Aurikirkbya wordensis which parallel those found in Manawe (Fig. 4H. 1), Lam unaware of the existence of equivalent structures in other extant ostracods. Sort ANATOMY It is not my intention in this paper to discuss homologisation of manawan appendage seg- ments, but detailed histological and scanning electron microscope examinations of their development through ontogeny are proceeding, One must acknowledge that whatever the result- ing interpretation if will inevitably not meet with universal acceptance. ‘Although the terms ex- opodite, endopodite, epipodite and the like are applied to ostracode limbs by various authors (not always harmoniously) in fact it is yery dif- ficult to homologise the individual parts of ostra- code limbs with those of other Crustacea’ (Maddocks, 1982). Previously, I suggested that the punciids have only three cephalic append- ages (antennule, antenna and mandible) and four pediform thoracic legs. This condition (the pos- s¢ssion of four thoracic segments) had also been proposed for Cambrian bradoriid ostracads (McKenzie and Jones, 1979). This is clearly at odds with the generally accepted limb/tagma formula for ostracods. “I-seems clear thal the first four limbs belong to the cephalon and the last two to the thorax, but the fifth limb has been claimed for both’ (Maddocks, 1952). Anderson (1965, 1967) acknowledged that embryological studies of post-mandibular seg- ment formation is of little value in assessing phylogenetic affinities amongst non-branchi- opods because the possibility of paraphyletic derivation can never be excluded. Equivalent studies may prove uscful in some areas of pun- clid biology (segmental origin of limbs) und phylogeny. The fundamental difficulty as- socisted with the concept of a specific group of limbs allocated to specific tagma is haw does one prove it and fo what end? In most Crustacea, the mesoderm of the post-naupliar region even in its earliest stages gives evidence of differentiation into somite rudiments of post-maxillulary seg- ments; i.c., differentiation of some mesodermal tissue into cellular clumps from which thoracic elements are derived is initiated during the naupliar slage, Consequently, i] would be diffi- cult to divide such a developmental sequence: when it is effectively 4 continuurt, FIG. 5. Scale bar = 100 ym unless otherwise stated. A, Manawa staceyi Cavalli Islands, New Zealand, 17 metres. Posterior of body (male) including thoracic/abdominal elements and right valve. Scale bar = 40 pm. B, Manawa staceyi Cavalli Islands, New Zealand, 17 metres, Ventral oblique view of abdominal segments and furca. Anal flap arrowed. Scale bar= 2) am. C, Cytherella sp.A. West Coast South Island, New Zealand 500 metres. Posterior-mosi abdominal segments and furca (male), Note anal flap and faecal pellet (arrowed). Scale bar = 40 um. D, Cytherella sp,B, Olt Kaikoura, South [stand, New Zealand, 380 metres. Trunk showing segmentation and genital lobe, gravid female. E, Cyrhere/la sp.B, Off Kaikoura, South Island, New Zealand, 380 metres. Trunk showing abdominal and thoracic (incomplete) segmentation and hemipenes. male. F, Cytherella sp.C. West Coast South Island. New Zealand. 910 metres, Ventral oblique view of furea, trunk and hemipene. 88 MEMOIRS OF THE QUEENSLAND MUSEUM PUNCIID OSTRACODS 89 In terms of ‘phylogenetic’ studies, Anderson (1965, 1967) gave indication of a embryological developmental progression from that of the cephalocarids in which ‘mesodermal segmenta- tion precedes ectodermal segmentation in the primitive manner’; to the derived malacostracan condition in which & mesoteloblasts ‘....bud off successive rows of 8 cells which form the somite rudiments of individual segments, and a corre- sponding row of ectotcloblasts bud off ectoderm which lies outside the somite rows and becomes segmentally associated with them’. Embryologi- cal studies of ‘primitive’ and ‘modern’ ostracods may give some indication of polarity within Anderson's sequence and asa result confirm or refine present concepts af ostracod phylogeny and relationships with other Crustacea. ABDOMEN Ostracoda are generally regarded as non-seg- mented and cephalised (McKenzie, 1983), and their trunk and abdominal reduction, as a result of segmental loss, is the most extreme of any crustacean. Nevertheless, after a study of the chitino-skeleton of several living taxa, Schultz (1976) concluded that ostracods had abdominal segmentation earlier in theit phylogeny. On the basis of this evidence and the possession of other ‘primitive’ limb and carapace characters, at least ive groups of ostracods are repeatedly utilised as providing examples of bauplans (acknow- ledging such constructions only as indicalions of what is possible) from which ‘modern’ ostracods. may have evolved, | have excluded the Poly: copidac from this discussion because they have fewer segments in the trunk (Fig. 6D, E). Sai- panettid ostracods will be discussed only in a general sense because detailed electron micro- graphs were nol available for study. As noted by Maddocks (1982), Schulz considered Saipanesta ta represent a phylogenetic intermediate be- tween the ancestral Platycopina und descendant Podocopina. On the basis of the carapace detail Schallreuter and Jones (1984) included the Pun- ciocopa (Kirkbyacea and Punciacea) in the ex- lant Platycopa. Discussion of morphological aspects of the abdomen of the platycopid Cy- therella is warranted because superficially, at least, it appears to resemble that described for Manawea stacey! (Swanson, 1989a). The trunk of male cytherellids is dominated by paired hemipenes which are attached to the body on or near segments 5 to 7 (Figs SE, F, 6A—C). Chitinous skeletal elements of the abdomen are produced anteriorly to provide what may be structural support for cach hemipenis and genitil lobe (in females), From the present study the precise origin of each hemipenis could not be determined; what is encouraging however is (a) its Structural variation between taxa and (b) the existence of ‘segmentation’ (Fig. 5E, F) indivat- ing # potential source of important taxonomic and phylogenetic information. The anlage of the hemipenis appears quite early in ontogeny (A-3 or A-4), as does abdominal segmentation (Fig. 4c), Kornicker (1975) argued that the position of ihe furea relative lo the anus should be given more emphasis in ostracod classification. Schulz (1976) figured the cytherellid trunk as being composed of ten segments, a telsan and furca: according to him the anus was located between the tenth segment and the telson, dorsal to the furca, Kornicker (1975) also placed the cytherel- lid anus dorsal to the furca but behind the telson. Scanning electron microscope examination of a number of critical-point dried specimens of Cy- therella confirms Kornicker’s view. The anus occurs after the Jast full sezment and an anal fap is present (Fig. SC). Also of interest is the pre- sence ofa ‘faecal’ pellet composed of coccalith remains which may indicate that cytherellids operale as ‘collectors’ (Kornicker, 1975; 41) rather than as efficient benthic filterers (Cannon, 1933). Note also that the posterior-most (in life position) ventral elements of the furca may also function as ‘housekecping” accessories (Fig. SF). Members of the Punciidae also have ten trunk segments with a poorly understood “reproduc- live’ element between segments 5 and 7. Bath Cytherella and Manawa carry paired lamcl- FIG. 6, Scale bar= 100 um unless otherwise stated. A. Cydterella sp.b. West Coast South Island, New Zeakand 320 metres. Ventral oblique view of male abdominul segments, lurca and hemipenes. B, Cytherella sp.£, West Coast South Island, New Zealand 320 metres. Hemipenes and abdomen (male). C, Cyrhere/la sp.B. OFF Kaikoura, South Island, New Zealand 380 metres. Trunk and hemipene of juvenile male. D, Palycope sp. Inside Crayfish Reet, Kaikoura, South Island, New Zealand, 14 metres. Entire adult enclosed in right valve, abdominal segments arrowed, E, Pelycope sp. Inside Crayfish Reet, Kaikoura, South Island, New Zealand, 14 metres, Entire juvenile enclosed jn right valve, abdominal segments arrowed. F, Manawa xtaceyi Cavalli Istatids, New Zea and. 17 metres. Metanauplivs 3, anal segment and furcal anlage. Scale bar = 10 am, 90 MEMOIRS OF THE QUEENSLAND MUSEUM liform furcae, the setae of which differ numeri- cally (more in Cytherella) and structurally (derived ?). The anal position in Manawa dupli- cates that found in Cytherella although in the former the anal flap occurs after the ‘telson’ (Fig. 5B). Both Kornicker (1975) and Schulz (1976) indicated that in Saipanetta the anus exits dorsal to the furca. This was seen by Kornicker (1975) as confirmation of the podocopid status of the saipanettids, since members of the Myodocopida (with which Saipanetta has some furcal similar- ity) have the anus ventral to the furca. The fact that Saipanetta has six trunk segments and a telson shows that its abdominal condition is more derived than that of platycopid or punciid ostracods but less than that of most extant ostra- cods. Abdominal evidence for a direct punciid-platy- copid link (Schallreuter and Jones, 1984) is not convincing; when combined with substantial contrasts in anatomy and carapace structure it seems unlikely, I suggest that segmentation of the trunk and abdominal configuration as found in Cytherella and Manawa is the plesiomorphic condition for ostracods. This does not exclude the possibility that both lineages developed in- dependently. CONCLUSIONS 1. As indicated by Hornibrook (1949) and confirmed by the present study, the carapace of the Punciidae is unlike that found on any other extant ostracods. 2. On the basis of detailed comparison of a number of key carapace characters it is con- cluded that punciid ostracods are the only living representatives of the predominantly Palaeozoic Kirkbyacea. 3. Similarities in abdominal soft anatomy of platycopid and punciid ostracods probably re- flect the plesiomorphic ostracodal condition; contrasts in other aspects of soft anatomy and the carapace suggest that the inclusion of Puncio- copa in the extant order Platycopa is unwar- ranted. 4. The position of some Cambrian bradoriid ‘ostracodes’ in which the abdomen is reduced or absent should now be reassessed. ACKNOWLEDGEMENTS I wish to thank Dr K.G. McKenzie and the Organising Committee of the 1990 International Crustacean Conference for giving me the oppor- tunity to present my findings to a wider audience. Drs G. Becker (Geologisch - Palaontologisches Institute, Frankfurt) and E. Herrig (Ernst- Moritz-Arndt-Universitat) generously provided reference material and some of the micrographs used in this text. Dr R. Scallreuter (Universitat Hamburg) kindly brought to my attention the existence of Melopetasus, an important element in my discussion. To all ostracodologists who attended the meeting in Frankfurt (August 1989) a sincere thanks, their discussions and comments have assisted punciid research immeasurably. The continued interest and support of Dr N. deB. Hornibrook (N.Z. Geological Survey) is appre- ciated. Mrs Joan McTurk expertly typed the manuscript. Finally I thank my wife (Christine) and daughter (Zina) who again accepted a sec- ondary role during the writing of this manuscript. LITERATURE CITED ANDERSON, D.T. 1965. Embryonic and larval development and segment formation in /bla quadrivalvis Cuy. (Cirripedia). Australian Jour- nal of Zoology 13: 1-15. 1967. 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Carapace sculpture in Amphissites (Kirkbyacea: Ostracoda). 259-273, In T, Hanai, N. Ikey# and K. Ishizaki, (eds) ‘Evolutionary biology of Ostracoda’, (Elsevier, Amsterdam), KORNICKER, L.S. 1975, Antarctic Ostracoda (My- adocopina) Part 1. Smiihsonian Contributions to Zoology 63; 1-374. KOZUR, H. 1985. Biostratigraphic evaluation af the Upper Palaeozoic conadonts, ostracods. and holothurian sclerites of the Bikk Mis. Part Ul: Upper Palaeozoic osiracods. Acts Geologica Hungarica 28 (3-4); 225-256. MADDOCKS, R.F. 1982. Evolution within the Crustacea. Part 4; Ostracoda 221-239. In 1..G. Abele (ed.) ‘The bivlugy of Crustacea 1. Sys- tematics, the fossil record and biogeogra- phy*.(Academic Press; New York), MCKENZIE, K.G. 1983. On the origin of Crustacea. In J,K, Lowry (ed.) ‘Papers from the conference on the biology and evolution of Crustacea’. Australian Museum Memoir 18; 21-43. MCKENZIE, K.G, AND JONES, P.J. 1979. Partially preserved soft anatomy of a Middle Cambrian bradoriid (Ostracoda) from Queensland. Search 10(12); 444-445, MCKENZIE, K.G. AND NEIL, J.V. 1983. Prom- anawa Gen. Nov., an Australian Miocene Pun- clid ostracode from Hamilton, Victoris. Proceedings of the Royal Society (Victoria) 95(2): 59-64. MULLER, K.J. 1982. Hessiandona unisulcata sp. noy. with phosphalised appendages from Upper Cambrian “drsten” of Sweden, 276-304, In R.H_ Bate, E. Robinson and L.M. Sheppard (eds) ‘Fossil and Recent ostracods’. (Ellis Horwood: _ Chichester), MULLER, KJ, AND WALOSSEK, D, 1986, Arthro- pod larvae from the Upper Cambrian of Sweden, Transactions of the Royal Society of Edinburgh: Earth Sciences 77: 157-179. 1988. External morphology and larval develop- ment of the Upper Cambrian Maxillopod, Sreda- caris admirabilis. Fossils and Strata 23: 1-76), NOHARA, T. AND NAKASONE, N. 1982. Sexual dimorphism of the paleocopid ostracod genus Manawe from Okinawa, Japan. Transactions and Proceedings.of the Palaeontological Soctely of Japan N.S. 127: 364-367. OKADA, ¥. 1982, Ultrastructure and pattern of the carapace of Bicornucyihere bisanensis (Os- iracoda, Crustacea), The University Museum, University of Tokyo Bulletin 20: 229-255. SCHALLREUTER, R. 1979. Ordovizische problem- alica, 1. Melopetasus gen. Paliontologische Zeitschrift 53 (1-2); 129-135. 1988. Homeomorphy. phylogeny and natural classification; case studies involving palaeozoic ostracads. 1041-1049. In T. Hanai, N. Lkeva, and K. Ishizaki (eds) ‘Evolutionary biology of Ostracoda’. (Elsevier: Amsterdam). SCHALLREUTER, R. AND JONES, C.R, 1984. A new Ordovician kirkbyacean ostracode. Newes Jahrbuch flr Geologie und Palaontolgic Mh (H,7):416-426, SCHRAM, FR, 1982. The nature and limits of the crustacean fossil record, 94-147, In 1G. Abele, (ed.),.°The biology of Crustacea. 1. Sys- tematics, the fossil record and biogeogra- phy’ (Academic Press: New York). SCHULZ, K. 1976. *Das chitinskellet der Podocopida 92 MEMOIRS OF THE QUEENSLAND MUSEUM (Ostracoda, Crustacea) und der frage der met- amerie dieser Gruppe’. Unpublished Ph.D. The- sis, University of Hamburg. SOHN, I.G. 1954. Ostracoda from the Permian of the Glass Mountains, Texas. United States Geo- logical Survey, Professional Paper 264(A): 1- 111. SWANSON, K.M. 1985. The discovery of living pun- ciid ostracodes in New Zealand. New Zealand Geological Survey Record 9: 87-89. 1989a. Ostracod phylogeny and evolution — a manawan perspective. Courier Forschungsin- stuit Senckenberg 113: 11-20. 1989b. Manawa staceyi n.sp (Punciidae, Os- tracoda) soft anatomy and ontogeny. Courier Forschungsinstuit Senckenberg 113: 235-249. 1990. The punciid ostracod — a new crustacean evolutionary window. Courier Forschungsinstuit Senckenberg 123: 11-18. SYLVESTER-BRADLEY, P.C. AND BENSON, R.H. 1971, Terminology for surface features in ornate ostracodes. Lethaia 4: 249-286. WALOSSEK, D. AND MULLER, K.J. 1989. A sec- ond type of A-nauplius from the Upper Cam- brian “drsten” of Sweden. Lethaia 22: 301-306. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 93 DISTRIBLTION OF MANGROVE SESARMID CRABS (CRUSTACEA: BRACHYURA) IN NORTHEASTERN AUSTRALIA Sesarmid crabs have been shown to be an important com- ponent of mangrove ecosystems in tropical Australia (Robertson. 1986; Smith, 1987). Despite their dominance in mangrove forests (Jones, 1984) there is litile information on the distribution of sesarmid crabs bewh between and within estuaries of tropical Australia, P, Davie (Queensland Museum) is Working on the taxonomy of the group and ts describing the new species discussed in (his paper. Materials and Sampling Sites Pitfall traps were used lo determine crab abundances. Within estuary sampling was undertaken a! Hinchinbrook Island, Murray River and Cape Ferguson (Fig. |). Between estuary sampling was undertaken in the Endeavour, Morgan. Claudie, Escape and Wenlock Rivers (Fig, 1). Opportunistic hand collections of crabs were also available tram the Fly Raver. Results Five species accounted for over 90% of crabs captured al Hinchinbrook Island, Murray River und Cape Ferguson, At the moutlrof these estuaries, in high salinity regions, Sesarma semperilongicristutiam dominated in the low intertidal adja- cent to the mudflat. This species was replaced by 5. messa which dominated catches in the intertidal region up to the terrestrial mangrove interface where S. fourmanvir] domi- nated. In the medium and lower salinity regions of estuaries the mangrove region is reduced to normally less than 3Um., As such, the dominant crab distributions showed no dilter- ence with intertidal position. §. messa dominated the medium sulinily regions of the mangrave forests, giving way to S. brevipes in the low salinity regions. §. brevicristanim was sub-dominant in the medium and low sulinity regions. The Endeavour, Morgan and Claudie Rivers had within estuary crab distributions similiar to those described above. The Wenlock River had 4 completely different sesarmid fauna to the northeast coast rivers. S. darwinensis dominated high salinity Jow intertidal regions and was co-dominaot with Sesarma sp. nov. 2 in the mid- to high intertidal regions, In ihe low salinily regions Sesarma sp, poy- 1 dominated. The Escape River could only be sampled in the medium and high salinity regions. Within estuary crab distributions reflected both east coast aid Wenlock River distribuons. 8. semperi longicristatum and S. messa distributions were similiar to the other east coast rivers and §. sp, nov, 2 replaced §. four- manoiri as well as being co-dominant with S. esse in the medium salinity rogions. In the Claudie River S. sp. nov. 2 was noliced adjacent to a large population of §, fourmaneirt, S.messa and S. sp. nov. 2 were bath collected from the lower reaches of the Fly River, Fig. 1 shows the distributions als. messa. §, fourmanoiri and S sp. nov. 2 found in these surveys. Discussion Davie (1985), in trying to explain the apparent segregation af northern coast endemic species (o westwards of he Torres Strait region, suggested that current flow westwards through Torres Strait could effectively prevent northern derived spe- — — a? SSS Bee rte / , whit Fic | h- Taveee oo ores Vi tone eae te — \ pres ume Wem fiero : rT * " iat A — whe we j vee | =. \ (mony te eos - - 1 +t ee as , on / I —e i “ “ e rv on cies from colonizing eastern Australia, but that tropical east coast fauna could be swept via larvae or adults onta northern coasis, The present study shows that Torres Strait is nol a barrier for at least one typical northern species, §, sp. nov, 2, which is able lo penetrate some distance south along eastern Cape York Peninsula and onto the coast of Papua New Guinea. The existing distribution patterns of the dominant sesarmid crab fauna associated with mangroves in NE Aus- iraliadnd SW PNG can only partially be explained by simple physical coastal oceanographic features. As Davie (1985) suppesied, further studies are needed to elucidate larval/adult disinbution patterns for these species. If the dominant sesar- mid species are “keystone species’, then knowledge of the colonization factors which determine distribution is impor- (ant. As the tropical littoral zones come under increasing pressure through urbanization, development and subsequent pollution, logether with the predicted effects of the 'green- house phenomena’, a correct Understanding will be impera- live when the biological components of these littoral ecosysiems are forced to adapt and alter distribution patierns, Literuture Cited Davie, PLP. 1985. The biogeography of littoral crabs (Crustacea: Decapoda: Brachyura) associated with tidal wetlands in trepical andsub-tropical Australia. 259-276, In J. Chappell, J.D.S. Davie, and C. Woodrotfe(eds.) “Coasts and lidal wetlands of the Australian monsoon region’. Proceedings of a conference held on 4-11 November 1984, Darwin, N_A.R.U. Monograph Series. Jones. D.A. 1984. Crabs. of the mangal ecosystem, 89-109, in F.D, Por and 1. Dor (eds.) “Hydrobiology of the mangal (W. Junk: The Haguc). Robertson, A.!. 1986, Leal-burying crabs: their influence on energy Mow and export [rom mixed mangrove forests (Rhizophora spp.) in northeastern Australia, Journal of Experimental Marine Biology and Ecology 102: 237- 248, Smith, Tu, 1]f, 1987, Seed predation ia relation to tree dom- inance and distribution in mangrove forests, Ecology 68(2): 266-273. §.D. Frasher, RL. Giddins and TJ. Smith 11, Australian Institute ef Marine Science, PMB No. 3, MC Townsville 4810, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 94 MEMOIRS OF THE QUEENSLAND MUSEUM LATITUDINAL VARIATIONS IN SETTLEMENT AND SURVIVAL OF THE PEDUNCULATE BARNACLE, POLLICIPES POLYMERUS SOWERBY The pedunculate barnacle, Pollicipes polvmerus. has a broad distribution range along the West Coast of North America, from British Columbia, Canada, to Punta Abreojos. Baja California, Mexico. Brooding activity indicates two geographically disparate races corresponding to the cold and warm water temperature zones north and south of Point Conception, California (34° 16° 12" N) (Cimberg, 1981). Settlement and recruitment were monitored on two Cal- ifornia populations that corresponded to these two races: a southern race from La Jolla (32° 52° 12" N) and a northern race from Bodega Head (38° 18° 30" N). The cyprid larvae of Pollicipes settle preferentially on the peduncles of adult conspecifics facilitating settlement and Tecruitment measurements. The index of settlement is de- fined as the mean number of spat/adult; spat being individu- als <1 mm rostro-carinal (R-C) length. Recruitment is defined as the mean number of juvenile barnacles in the 1-9 mm R-C length. Generally barnacles this size remain at- tached to the adult peduncles. From observations off La Jolla, growth of barnacles in newly established aggregates is quite rapid reaching mean R—C lengths in less than one month. By five months a mean R-C length of almost 15 mm is attained (Hoffman, 1989), PHYLOGENETIC AND BIOGEOGRAPHIC RELATIONSHIPS OF THE SUBTERRANEAN AMPHIPOD GENUS BAHADZIA (HADZIIDAE) IN THE WEST INDIAN REGION As presently known, the subterranean amphipod genus Bahadzia is composed of 7 species: 4 from anchialine caves in the Bahamas and Turks and Caicos Islands, | from shallow (mostly freshwater) wells in southeastern Haiti, and 2 (de- scriptions in prep.) from anchialine caves on the Yucatan Peninsula and the nearby island of Cozumel. A cladistic analysis of the genus, using PAUP, suggests that nested subsets of species correspond closely to geographically sep- arate areas. The geographic distribution of Bahadzia is nearly congruent with the distributions of 4 other small, monotypic subterranean crustacean genera, including the remipede Speleonectes, the thermosbaenacean 7ulumella, the cirolanid We define survival as the mean number of juvenile/adult divided by the mean number of spat/adult from the preceding month’s sample. The rationale being that the spat grow quickly reaching the juvenile size range during their first month of existence. Although settlement occurs year round off La Jolla with peaks (133-290 spat/adult) occurring during the early spring, the percent survival from spat to juvenile peaks (19°) during the late autumn-early winter months. At Bodega Head, settlement occurs trom April through January peaking during the early summer (22.6 spat/adult) and early winter (26-37 spat/adult). Survivorship in the northern popu- lation peaks (37-64%) during the summer months. It is proposed that the lower survivorship in the La Jolla race may be due to desiccation and/or temperature stresses exerted on the recently settled spat along the warmer and drier southern California coastline. Literature Cited Cimberg 1981. Variability in brooding activity in the stalked barnacle Pollicipes polymerus. Biological Bulletin. Marine Biological Laboratory, Woods Hole 160: 31-32. Hoffman, D.L. 1989. Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymerus Sowerby, off La Jolla, California. Journal of Experimental Marine Biology and Ecology 125: 83-98. D.L. Hoffman, N. Bertha and J. G. Blom, Department of Biology, Bucknell University, Lewisburg, PA. USA. isopod Bahalana, and the decapod shrimp Agostocaris. Pre- liminary track analysis and observations on natural history suggest that Bahadzia and these other stygobiont taxa, have shared a similar distributional history. A second cladistic analysis, which compares Bahadzia with most other hadziid genera in the greater West Indian region, strongly supports the possibility suggested previously that Bahadzia is more closely allied phylogenetically with the freshwater genus Mayaweckelia and its sister genus (description in press) from caves on the Yucatan Peninsula, than with any other genus or group of genera in the family Hadziidae. John R. Holsinger, Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 95 THE CONSERVATION STATUS AUSTRALIAN FRESHWATER CRAYFISH Ina recent review of the conservation status of Australian freshwater crustaceans (Horwitz 1990), relevant issues deal- ing with the freshwater crayfish fauna of Australia were included; this paper summarises that information. Twenly five species have been included in a provisional list of threatened crayfish species and these include; i) three species of smooth freshwater crayfish belonging to the genus Cherax, indications are that the impact of aquaculture and commercial and recreational fishing has resulted. or may result. in declines in the population numbers, genetic varia~ bility or distributional ranges for these species. ii) thirteen species of spiny crayfish: ten of these belong to the genus Euastacus and are confined to highland rainforested regions along the eastern seaboard of Australia where their habitat is continually (hreatened by agricultural and forestry activity and where only a few of the species are adequately reserved, Three very large species belonging to the genera Euustacus and Astacopsis are subjected tw pressure resulting from et- fectively unrestrained recreational fishing and habitat altera- tion: and iii) nine species of burrowing crayfish belonging to the genus Engaeus; this genus can be characterised by a few species with broad distributions and many species with very restricted distributions, The listed species are potentially threatened by agricultural activity and again not all are adequately reserved. Taxonomic problems have prevented proper assessments being made for species in al least four genera (Tenuibranchi- urus, Geocherax, Parastacoides and Engaewa). even though populations for each of these are known ty be threatened or have become extinct already. Three major habitat types are important because they harbor distinctive freshwater crustaceans and because they are threatened in Australia, These habitats which either in- clude crayfish in their faunal assemblages or require crayfish OF to create the microhabitat conditions necessary for other crustaceans, include: i) caves and mound springs, which are subjected to pressures resulting from habitat alteration (eutrophication, trampling by cattle, off-road vehicles etc.) and the effects of water drawdown; ii) highland rainforested areas in eastern Australia; and iii) other subterranean habi- tals, crealed by crayfish, including their burrows in per- manent water. in seasonally inundated areas, or even on hill-slopes. Crayfish burrows harbour a distinctive faunal assemblage (termed “pholeteros’); pollution and the allera- tion of water table levels are the most likely areas which might affect both the crayfish which create the habitat, and the assemblage itself. The above issues would be al least partially resolved by improving the reservahon status of identified species and habitats. Furthermore. as we increase our knowledge base we will need to modify the status given Lo species and habitats. The most urgent information required to update these find- ings must be the precise effects on species of a wide range of potentially (hrealening processes (effects of pesticides, heavy metals, sedimentation, swamp drainage. changes in nutrient concentrations, introduction of exotic diseases etc), With this data, status could be reviewed on a regular basis to remove any impeding effect that outdated listings mighl have on appropriate developments. Literature Cited Horwitz, P. 1990. The conservation status of Australian freshwater Crustacea, Australian National Parks and Wildlife Service Report Series I4. (Canberra: Australia). 121 p . Pierre Horwitz, Department of Geography and Environmental Studies, University of Tasmania, GPQ Box 252C, Hobart, Tasmania 7001, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 96 MEMOIRS OF THE QUEENSLAND MUSEUM REPRODUCTION IN SAND DWELLING TALITRID AMPHIPODS: EVOLUTIONARY ADAPTATION FOR TERRESTRIAL LIFE Within the Amphipoda reproductive potential can be eval- uated by measuring a number of factors including longevity. egg size and brood production. Some previous workers have suggested that mean brood size (number of egys) is related to habitat, decreasing from marine through supralittoral to terrestrial amphipods. Supralittoral talitrids include two eco- morphological groups (Bousfield, 1982) - the beach fleas with well described patterns of reproduction and the beach hoppers investigated here. Brood characteristics were measured for three species of sandhoppers from Maine, USA (Platorchestia platensts, Talorchestia megalophthalma and Talorchestia longicornis) and two species from New Zealand (Talorchestia quoyana and Talorchestia cookii), The results were combined with literature values lo provide a comparison of 10 sandhoppers. ranging in body length from 2 to 21 mm (Williams. 1978: Morino, 1978; Venables, 1981; Van Senus, 1988). Some species, for example P. capensis, show a good correlation between brood size and female body length whilst others, including P. platensis and T. quoyana, are more variable. The combined results suggest no obvious relationship between average female length and brood size, which varied between 2 and 24 eggs. For T. quoyana from New Zealand, females of 17 mm body length (minimum rostrum to telson distance when animal was straightened) had the highest brood numbers (mean = 24.0; SE = 2.0) and the egg size was large (mean = 1.33 mm maximum diameter, SE = 0.12). Brood mortality was low over the four developmental stages. Similar patterns were seen in other genera and species of supralittoral sand- hopper. The overall reproductive potential of sandhoppers is less than subtidal amphipods (Fenwick, 1984) and aquatic gammarids (Steele and Steele, 1975). They are, however, within the range recorded for beach fleas and euterrestrial amphipods (Duncan, 1969; Wildish, 1979; Friend, 1980). Recent studies on the physiological ecology of sandhop- pers show they are well adapted for aerial existence and are able to withstand greater water loss during desiccation than many marine and terrestrial species (Marsden, 1989). The sand beach habitat is physically demanding and amphipods may be exposed to vigorous wave and tidal action. In addi- tion, storm events cause massive and rapid substratum move- ments and overturn. Most sandhoppers have evolved a thick and tough cuticle to resist these crushing and abrasive events and as a result their cutaneous respiration is low. Mating strategies and behaviour patterns of sandhoppers most likely provide increased brood protection. The consistency of brood size between sandhoppers of a wide size range may indicate phylogenetic constraints on reproduction. The evolution of larger eggs allows the release of larger hatchlings which are more tolerant of desiccation in the strand line habitat. The life history strategies of sandhoppers are well adapted for the biotic and physical factors operating within the sand beach ecosystems. Compared with other talitrids, sandhop- pers have achieved a larger body size, have high resistance to desiccation and have complex behaviour patterns to avoid being displaced by the tide. It is concluded that sandhoppers have evolved reproductive strategies for exploiting sand beach habitats. These are not seen necessarily as an integral part of the colonisation of truly terrestrial habitats. Acknowledgements We wish to thank the University of Canterbury for granting study leave to one of us (IDM) during 1989, and the Depart- ment of Marine Resources, Boothbay Harbour, Maine, for providing laboratory and study facilities, Literature Cited Bousfield. E.L. 1982. The amphipod superfamily Talitroidea in the northeastern Pacific region. 1, Family Talitridae: Systematics and distributional ecology. Publications in Biological Oceanography, National Museums of Canada, 11:1-73. Duncan, K.W. 1969. The ecology of two species of terrestrial Amphipoda [Crustacea: Family Talitridae] living in waste grassland. Pedobiologia 9: 323-341. Fenwick, G.D, 1984. Life-history tactics of brooding crustacea. Journal of Experimental Marine Biology Ecology 84: 247-264. Friend, J.A. 1986. Biology of terrestrial amphipods, Annual Review Entomology 31; 25-48. Marsden, I.D. 1989. An assessment of seasonal adaptation in the beach hopper Talorchestia quoyana. Journal of Ex- perimental Marine Biology Ecology 128: 203-218. In Press. A comparison of water loss and gill areas in two supralilttoral amphipods from New Zealand. Hydrobio- logia. Morino, H. 1978. Studies on the Talitridae (Amphipoda, Crustacea) in Japan. III. Life history and breeding actiy- ity of Orchestia platensis Kroyer Publications Seto Marine Laboratory 2-4; 245-267. Steele, D.H. and Steele, J.J. 1975. The biology of Gammarus (Crustacea, Amphipoda) in the northwestern Atlantic XI. Comparison and discussion. Canadian Journal of Zoology 53: 1116-1126. Van Senus, P.W, 1988. Reproduction of the sandhopper Talorchestia capensis (Dana) (Amphipoda, Talitridae). Crustaceana 55: 93-103. Venables, B.J. 1981. Aspects of the population biology of a Venezuelan beach amphipod, Talorchestia margaritae (Talitridae) including estimates of biomass and daily production and respiration rates. Crustaceana 41; 271- 285. Wildish, D.J. 1987. Reproductive consequences of the ter- restrial habitat Orchestia (Crustacea, Amphipoda). In- ternational Journal of Invertebrate Reproduction 1: 9-20. Williams, J.A. 1978. The annual pattern of reproduction of Talitrus saltator (Crustacea: Amphipoda: Talitridae). Journal of Zoology, London 184; 231-244, 1.D. Marsden and K.W. Duncan, Department of Zoology, University of Canterbury, Christchurch, New Zealand. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 97 DIVERSIFIED REPRODUCTIVE TRAITS AMONG LOCAL POPULATIONS OF A FRESHWATER PRAWN, MACROBRACHIUM NIPPONENSE (PALAEMONIDAE: CARIDEA: DECAPODA) — EVIDENCE FOR A GENETIC BASIS Varied egg and clutch sizes among local populations of the freshwater prawn Macrobrachium nipponense (de Haan) in Japan have been previously reported i.e. laying many small eggs (0.05 mm* in single egg volume) each spawning by estuarine populations, a few large eggs (0.1 mm’) by inland freshwater populations, and a moderate number of medium- sized eggs by coastal lagoon populations (Mashiko, 1990). Such populations with different reproductive traits were oc- casionally found even within a single water system for in- stance, the Sagami River, central Japan (Mashiko. 1983a. b). The present study examines the genetic grounds for the different reproductive traits in this species. Materials and Methods Two groups of individuals, one spawning large eggs (0.100 mm* in mean egg volume: large-egg population), and a second producing small eggs (0.051 mm”: small-egg popu- lation) were collected from the upper basin, and the estuary respectively of the Sagami River in 1988. The two sexes were reciprocally crossed between them, and viable F1 individuals were obtained as noted previously (Mashiko, 1984). A de- finite number of the F1 individuals were raised under the same defined conditions and the size and number of their eggs were examined when they bred the next year. As a morphological characteristic, the number of upper marginal teeth on the rostrum was also investigated for both of the laboratory raised and field-collected individuals. Results and Discussion Fl individuals produced by crossing the female of the small-egg population and the male of the large-egg popula- tion (S? x Ld) and by crossing the two sexes in inverse combination (L? x Sd), laid eggs of 0.071 and 0.075 mm respectively. These egg sizes were intermediate between the large and small eggs of their parental populations. On the other hand offspring produced by crossing within the large- egg population (L2 x Ld) and the small-egg population (S 2 x So) laid eggs of 0.102 and 0.051 mm’, respectively - practically unchanged from the eggs of each parental popu- lation. Thus, the different egg sizes in this species is con- sidered to be genetically controlled as a quantitative character. Similarly the results of crossing experiments sug- gested a genetic basis for different clutch sizes between the two populations. The mean number of the upper marginal teeth on the rostrum differed significantly between the two populations in the field — 11.8 + 0.8 (SD) and 12.5 + 0.9 for individuals with large and small eggs, respectively (P concentrations us in other (errestrial taxa, Literature Cited Boustield, E.L. 1984, Recentadvances in the systematics and biogeography of landhoppers (Amphipoda: Talitridae) oft the Indo-Pacific region. In F.J. Radovsky, P.H. Raven und $.H. Somer (eds) “Biogeography of the tropical Pacific’. Bishop Museum Special Publication 72: 171- 210). Friend, JA, 1987. The terrestrial amphipods (Amphipoda: Talitridae) of Tasmania: systematics and zoogcography, Records of the Australian Museum Supplement 7; |~85. Moore, P.G. and Taylor, A.C, 1984. Gill area rélationships in an ecological series of gammaridean amphipods (Crustacea). Journal of Experimental Marine Biology und Ecology 74: 179-186. Spicer, J.1., Moore, P.G. and Taylor, A.C. 1987. The physi- ological ecology of land invasion by the Talitridae (Crustacea. Amphipoda). Proceedings of ihe Royal Sociely of London, B, 232: 95-124, Spicer, J.J, and Taylor, A.C. 1986. A comparative study of the gill area relationships in some talitrid amphipods. Journal of Natural History 20; 935-947. Roy Swatn and Alastair M.M. Richardson, Department of Zoology, University of Tasmania, GPO Box 252C, Hobart, Tasmania 7001, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum COMPARISON OF MORPHOLOGICAL AND MOLECULAR PHYLOGENY OF THE DECAPODA LAWRENCE G. ABELE Abele, L.G. 1991 09 01: Companson of morphological and molecular phylogeny of the Decapoda. Memoirs of the Queensland Museum 3b; 101-108, Brisbane, ISSN 0079-8835, Decapod phylogenies based on morphological and molecular data are similar in topology for the taxa in common: both trees recognise a dendrobranchtate lineage, a caridean lineage (including procaridids), a stenopodidean lineage, and a replant lineage. The two trees are compared with respect to homaplasy levels using consistency indices, hamoplasy excess values, and bootstrap values for the various nodes, In all cases the molecular data exhibit considerably less homoplasy. It is suggested that moleculat and morphological data be viewed as complementary because in many cases comparative morphology has suggested the research question. Significant questions on decapod phylogeny remain with the reptant infraorders. (_] Decapoda. phylogeny, morpholagy, molecular data, nucleotide sequences, ISS ribosomal RNA. Lawrence G, Abele, Department of Biological Science, B-142, Florida State University, Tallahassee, FL 32306, USA; 20 March, 1997. Decapods are among the best known of the crustaceans, although their phylogenctic rela- tionships are poorly understood, Recent reviews of decapod phylogeny (Burkenroad, 1963, 1981: Glaessner, 1969; De Saint Laurent, 1979a; Fel- genhauer and Abele, 1983: Abele and Felgen- hauer, 1986) have resulted in recognition of a fundamental division of the decapods into two groups, the Dendrobranchiata (penacid shrimp and their relatives) and the Pleoevermuta (all other decapods). This division is based on the fact that all pleocyemates incubate their embryos on the pleopods, with eclosion occurring at a zocal or Jater larval stage, in contrast to dendro- branchiates and euphausiaceans, which release embryos free into the sea with eclosion occurring ata naupliar stage. Furthermore, dendrobranchi- ates have a unique gill morphology consisting of a central branchial axis and paired lateral branches each with subdivided secondary rami (= the dendrobranchiate condition), The male petasma might also be a unique dendro- branchiate feature as Burkenroad (1963) sug- vested that this structure is not homologous to that found in euphausiaceans and some reptants, All other morphological characters generally cited for dendrobranchiates are either found in other taxa or are pleisiomorphic and uninforma- tive relative to the Decapoda. The above analyses and diagnoses were based an morphology, while the analysis of Kim and Abele (1990) used nucleotide sequences of 18S ribosomal RNA in a phylogenetic study of selected decapods. Here [briefly review the clas- sification and phylogeny of the Decapoda and, using new sequence data for a dendrobranchiale, several carideans and a brachyuran crab, com- pare molecular results to those obtained from morphological data, MATERIALS AND METHODS A summary classification of the Decapoda is given in Table 1 along with a list of the decapod axa used in this study. Kim and Abele (1990) provided details on sequencing methods and alignment of the sequences, and all molecular data have been deposited in GenBank. The list of morphological characters is given in Appen- dix I (derived from Abele and Felgenhauer, 1986, figs 2~5). Phylogenetic analyses were per- formed using PAUP 3.0 (Swofford, 1990), A dendrobranchiale shrimp, Penaeus aztecus, Was used as the outgroup for the molecular data while Euphausia sp. was used as the outgroup for the morphological data. RESULTS MOoLvecuLAR ANALYSIS Maximum parsimony analysis yielded a single minimum-length tree (Fig. 1a) of 432 steps with a consistency index of 0.692 based on 195 phy- logenetically informative characters. The two dendrobranchiates are joined by a node (A) that is 35 steps from the node (B) joining the pleocye- mates (Penaeus aziecus 1s 17 Steps from the node (A) while Sievenia brevirostris is 40 steps from 102 TABLE 1. Summary classification of the Decapoda (modified from Bowman and Abele. 1982) with re- spect to the taxa used in this study, Number of Nucleotides Decapoda ‘Suborder Dendrobranchiata Family Penaeidae Penaeus azrecus Wes 2.0.0.2 eee eee 130) Family Sicvoniidae Steyonta brevirosfris Slimpson Suborder Pleocvemata Infraorder Caridea Family Alpheidae Alpheus heterochaelis Say occ yee eee Family Atyidae Typhlatva rogersi Chace and Manning Family Procarididae Procarts ascensionis Chace and Manning ..., Family Palaemonidac Palaemanetes kadiakensis Rathbun Infraorder Stenopodidea Family Stenopodidae Stenopus hispidus (Olivier) ....-----..-.1, Infraorder Astacidea Family Astacidse (several taxa, morphological dam) Family Cambaridae Pracambaris leonensis Hobbs .. 2.22... -. 4,721 Infraorder Thalassinidea Family Axiidae Coralaxius abelei Kensley and Gore (morphological data) Infraorder Brachyura Family Raninidae Ranilia muricata H. Milne Edwards ...... 1. Family Portunidae BR the node). The next branch off the tree (B-C) is 33 steps and leads to a node (C) that joins all caridean shrimp, including Pracaris as- censcionis which comes off this node (C) with a branch length of 19; a relatively long branch (C-D) of 52 steps leads to a node (D) joining the three remaining caridean shrimps [an atyid, Ty- phlatya rogersi, comes off first with a branch length of 27 steps followed by a branch (D-E) of 24 steps leading to a node (E) joining an alpheid, Alpheus heterochaelis, with a branch length of 19 steps and a palaemonid, Palaemonetes kadi- akensis, with 4 branch length of 14 steps}. Re- turning to the main branch, there ts a segment (B-F) of 28 steps with a side branch of 35 steps leading to a stenopidid shrimp, Srenopus hispidus. The next branch (F-G) is 38 steps and leads to a node (G) with one branch of |) steps leading to the crayfish Procambarus leanensis; MEMOIRS OF THE QUEENSLAND MUSEUM the next branch (G-H) is 14 steps and leads to a node (H) that joins two brachyuran crabs, Ranilia muricata with a branch length of 8 steps and the blue crab Callinectes sapidus with a branch length of 18 steps. The data were also evaluated by the bootstrap method (Felsenstein, 1985) which involves ran- dom sampling of the original data set with re- placement until a new data set equal in size to the original is obtained. Each of the new data sets (in this case 100) is analyzed using maximum par- simony and the number of times each node oc- curs is recorded. This method provides an indication of the level of support for each node in the tree with 95% considered to be statistically significant. The bootstrap value joining the two dendrobranchiates is 95% while that of (B) join- ing all pleacyemates is 94%. The values for the caridean shrimps (C, D, E) are 99-100%. The value tor the node (F) joining the so-called rep- tant taxa is 86%. if S. hispidus is considered a member of this group. The value is 96% (node G) for taxa traditionally considered to be reptants and the value for the node joining the two brachyuran crabs is 100%, These results suggest considerable support for the relationships dia- gramed in Fig. la. MORPHOLOGICAL ANALYSIS Maximum parsimony analysis of the morpho- logical data using Euphausia sp. as the outgroup yielded a single minimum length tree (Fig. 1b) of 74 steps with a consistency index of 0.568 based on a total of 40 phylogenetically informa- tive characters. The first branch to come off the tree with a length of 3 steps leads to Penaeus; this 1s followed by a branch that leads to a nade (C) joining Procarts (5 steps) and a caridean (8 steps); the next branch leads to Stenapus (2 steps) while the terminal node joins an axiid (9 steps) and an astacid crayfish (2 steps). A bootstrap analysis reveals limited support (55%) for the pleocyemate lineage (node B) and somewhat larger values for the Caridea (67%, node C), the Stenopididea (65%, node D) and the Reptantia (82%, node E), DISCUSSION COMPARISON OF TREES Comparison of Fig Ja and 1b reveals that the twa trees have similar topologies for the taxa in common. Both trees recognize a dendrobran- chiate lineage separate from all other decapods, COMPARISON OF PHYLOGENY OF DECAPODA Procaris Typhlatya Palaemonetes Stenopus Penaeus : §™ Sicyonia 103 a 4 B 4 3 a 5 2 § a 4g ie] 2 u 3 ke} 2) ue) § g 5 8 a6 3 a Q 2 < 5 B < FIG. 1. Relationships among the taxa shown as inferred by maximum parsimony analysis. a, based on nucleotide sequences of 18S ribosomal RNA, tree length = 432 steps based on 195 characters, CI = 0.692. b, based on morphological data, tree length = 74 steps based on 40 characters, CI = 0.568. % numbers adjacent to nodes are bootstrap values based on 100 replicates. a caridean lineage, a stenopodidean lineage and a reptant lineage. There are several approaches to comparing and evaluating the reliability of phylogenetic hypotheses based on maximum parsimony (Ar- chie, 1989b). A common approach has been to compare consistency indices (CI) among the trees. CI is the minimum number of steps on the tree when no homoplasy is present divided by the observed number of steps. While this seems a reasonable approach to use, Archie (1989a) showed that the CI is highly and negatively correlated with the number of taxa and proposed another statistic for comparative purposes. In the present case the number of taxa does not differ much (7 vs 10) and the CI for the molecular data set of 10 taxa is higher than that for the morpho- logical data (0.692 vs 0.568). Another approach (Archie, 1989b) is to compare the maximum number of steps possible on a tree to both the minimum possible and the observed number of steps. For the morphological data the maximum tree length is 104, the minimum length is 42 while the observed is 74. Archie (1989b) suggested using these values to calculate a ratio, HERM (= homoplasy excess ratio maximum), which is the maximum number of steps minus the observed divided by the maximum number minus the min- imum possible number of steps. Thus the value is 1 when no homoplasy is present and 0 when there is no phylogenetic information in the data. For the morphological data, HERM = 0.484. This somewhat low value is not unexpected given the relatively low bootstrap values ob- tained for each of the tree nodes (Fig. 1b). An examination of the characters mapped out on the tree reveals that 25 of the 40 reverse at least once and only 15 (indicated by an asterisk in Appen- dix I) map without homoplasy. It is interesting to note that of the latter 15 characters, 10 are con- cerned with the presence/absence of exopods and gills on the pereiopods. The molecular data demonstrate considerably less homoplasy. The maximum tree length (without Sicyonia, which was dropped to facili- tate comparisons) is 508, the minimum possible is 275 and the observed is 340 resulting in a homoplasy excess ratio maximum (HERM) of 0.721. This relatively high value is consistent with the high bootstrap values obtained (Fig. 1a). Does this mean that molecular data are more reliable than morphological data with reference to decapod phylogeny? Probably not as it may be possible to select a different suite of morpho- logical features with less homoplasy. It should also be emphasized that a single morphological character may be of such fundamental biological importance that it alone can provide strong evi- dence for evolutionary relationships. No single nucleotide site could ever provide such evi- dence. The morphological and molecular data sets should be viewed as complementary. Cen- turies of comparative morphology have provided the background and in many cases posed the interesting questions that may be further investi- 104 TABLE 2. Comparison of data derived from parsi- mony analyses of morphological and molecular data. Mole- | Morph- cular | ological Number of Taxa Number of Variable Characters Number of Phylogenetically Informative Characters Tree Length Consistency Index HERM Bootstrap values Pleocyemata Caridea Stenopodidea ‘Reptantia’ Brachyura gated with molecular data. For example, the comparative morphological investigation of Wingstrand (1972) on pentastome spermatozoan morphology posed the question of their relation- ship to crustaceans that caused Abele et al. (1989) to further test (and support) this relation- ship using molecular data. What that study and the present one do indicate is that nucleotide sequences of 18S ribosomal RNA are reliable data for reconstructing crustacean phylogenies. STATUS OF DECAPOD PHYLOGENY Analyses of morphological data (Burkenroad, 1963, 1981; Schram, 1984; Abele and Felgen- hauer, 1986) suggested abundant support for the recognition of the Dendrobranchiata. Kim and Abele (1990) provided molecular evidence in support of this group and inclusion here of a second dendrobranchiate (S. brevirostris) sup- ports these previous results. Although Abele and Felgenhauer (1986) discussed reasons for reject- ing the concept of a taxon Natantia (originally defined to include penaeids, stenopodids and carideans), the term is occasionally used in de- fining spermatozoan types because penaeids, procaridids and carideans all have ‘unistellate’ or thumbtack spermatozoa (Jamieson, 1991; Fel- genhauer and Abele, 1991). In contrast, stenopodids, the other so-called natant, have a very different spermatozoan structure (Felgen- hauer and Abele, 1991) and I would only repeat an earlier conclusion (Burkenroad, 1963; Abele and Felgenhauer, 1986) that there is little evi- dence to support the concept of a Natantia and many reasons for rejecting it. Additional questions on classification and re- MEMOIRS OF THE QUEENSLAND MUSEUM lationships centre on taxa in the suborder Pleocyemata. One area of discussion concerns the limits of the Caridea and whether or not it includes procaridid shrimp. Schram (1986) rec- ognized two infraorders, the Procarididea and Caridea, placing them in the Suborder Euky- phida, a term coined by Boas for carideans and resurrected by Burkenroad (1981) and Schram (1984, 1986). The disagreement is really one of terminology because there is ample morphologi- cal evidence that procaridids and carideans share a common origin (Abele and Felgenhauer, 1986; Kensley and Williams, 1986; Schram, 1986), a conclusion that is strongly supported by the molecular data presented here. It is also clear that procaridids are separated from other carideans by arelatively long molecular distance (52 steps, Fig. 1a) as well as by differences in gill formulae (Burkenroad, 1984; Abele and Felgenhauer; 1986, fig. 7). The term Caridea is well known and in common usage and, therefore, | would propose to continue its use recognising within it a taxon Procarididea Chace and Manning, to include the two genera Procaris and Vetericaris, and a second taxon Eucaridea to include the remaining caridean taxa. The taxon Stenopodidea continues to be prob- lematic. De Saint Laurent (1979a) and others (Felgenhauer and Abele, 1983; Schram, 1984; Abele and Felgenhauer, 1986) considered the Stenopodidea to be an independent taxon more closely related to reptants than to any other group. The molecular analysis of Kim and Abele (1990) and that reported here supports these earlier results. In addition, as mentioned above, the spermatozoan morphology of S. hispidus (Felgenhauer and Abele, 1991; Jamieson, 1991) is unlike that of any other decapod known, em- phasising its rather isolated position. There has been considerable discussion over the classification and phylogeny of the Brachy- ura (see Rice, 1980, 1983). Recent data on sper- matozoan ultrastructure (Jamieson, 1989, 1990, 1991) and nucleotide sequences of 18S ribo- somal RNA (Spears et a/., in prep.) support the exclusion of the Dromiacea from the Brachyura as well as the inclusion of the Raninidae in the Brachyura. The notion of the Podotremata, Het- erotremata and Thoracotremata as taxonomic or phylogenetic units based on the location of the male and female genital openings appears to be unwarranted, for these groups appear to be mor- phological grades, as stated by Guinot (1977), tather than phylogenetic groupings. The challenge now facing those interested in COMPARISON OF PHYLOGENY OF DECAPODA 105 wv go w it o 4 o 2 U uw a ao a vu z 3 s 3 & S3ssgesg 8s s 2 2 € € & $82Ree8 = § ce) Oo oS a = a & = & 5 3) oO & a =ee = 6 6 § z 5B A= o 3 ba => % o 8 3 & a & a a E & e226 a Stenopodidea Brachyura Caridea Dendrobranchiata Pleocyemata FIG. 2. Summary of phylogenetic relationships of the Decapoda based on both molecular and morphological data, decapod evolution centres on taxa placed in the Reptantia. There seem to be as many groupings of these taxa as there are authors who have studied them. De Saint Laurent (19794) and Burkenroad (1981) did not evaluate phylo- genetic relationships but simply listed the groups that each recognized as belonging to the Reptan- tia if indeed such a group is even valid. For example, De Saint Laurent (1979a) listed the following reptant taxa: Scyllaridea, Eryonidea, Glypheidea, Astacidea, Thalassinacea, Anomala, Dromiacea, and Brachyura. Burken- road (1981) listed only the Palinura, Astacina, Thalassinidea, Anomala, and Brachyura. Bow- man and Abele (1982) and Schram (1986) listed the Astacidea, Thalassinidea, Palinura, Anomura, and Brachyura as infraorders in the Suborder Reptantia. The major differences among, the authors are that De Saint Laurent (1979a) splits the Palinura into the Scyllaridea (although by priority of the constituent taxa one might select Palinuridea as the appropriate name), Glypheidea and Eryonidea and separates the Dromiacea from the Brachyura. The recog- nition of the Glypheidea as a distinct lineage by De Saint Laurent is based on study of the only extant member of this group, Neoglyphea inopi- nata (Forest and De Saint Laurent, 1981). She further suggested that the form of eryonid re- ferred to as Eryoineicus is an adult secandarily adapted to a bathypelagic existence rather than a larval form as suggested by others. In addition, Burkenroad (1981) pointed out that eryonoids differ ina number of features from scyllarids and questioned the unity of the Palinura. Hence, there appear to be sufficient differences among the members of Palinura (sensu lato) to warrant separating the groups, especially to call attention to the need for further study. Although some preliminary molecular data are available (un- published) they are insufficient to comment further at this time. There are also sufficient differences, noted by De Saint Laurent (1979b), among members of the Thalassinidea to raise 106 questions about the phylogenctic status of this taxon. In conclusion, a proposed phylogeny sum- marising our current knowledge based on mor- phological and molecular data is given in Fig. 2. The major questions that remain concerning de- capod phylogeny and classification at the ‘In- fraorder’ level are with the so-called reptant groups. ACKNOWLEDGEMENTS I thank the organising committce of the Inter- national Symposium on Crustacea held at the University of Queensland, Brisbane, for the op- portunity to participate; Ms T. Spears for con- structive criticism, and Ms T, Boline for technical help, LITERATURE. CITED ABELE, L1G. AND FELGENHAUER, B.E. 1986. Phylogenetic and phenetic relationships among the lower Decapoda. Journal of Crustacean Bi- ology @: 385—400, ABELE, L.G., KIM, W. AND FELGENHAUER, B.E. 1989, Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea, Molecular Biology and Eyolution 6: 685-691. ARCHIE, J.W. 19893. A randomization test for the presence of phylogenetic structure in systematic data. Systematic Zoologist 38: 238-2452. 1989%b, Homoplasy excess ratios: new indices for measuring levels of homoplasy in phylogenetic systematics and a critique of the consistency index. Systematic Zoologist 38: 253-269. BOWMAN, T.E, AND ABELE, L.G, 1982. Classili- cation of the Recent Crustaces, Pp. |27. 10 L.G. Abele, (ed_) ‘The biolagy of Crustacea’. Vol. 1. (Academic Press: New York). BURKENROAD, M.D. 1963, The evolution of the Eucarida (Crustacea, Eumalacostraca) in relo- tion lo the fossil record. Tulane Studies in Ge- ology 2: 2-17, 1981, The higher taxonomy and evolution af De- capoda (Crustacea), Transactions of the San Diego Society for Natural History 19: 251-268. 1984, A note-on branchial formulae of Decapoda. Journal of Crustacean Biology 4; 277. DE SAINT LAURENT, M. 19794. Vers une nouvelle classification des Crustacés Décapodes Reptan- lia. Bulletin de |’Office National des Péches de Tunisie 3: 15-31. 1979b. Sur la classification et la phylogénie des Thalassinidae: definitions de Ja superfamille des MEMOIRS OF THE QUEENSLAND MUSEUM Axioidea, de la sousfamille des Thomassinilnae et de deux genres nouveaux (Crustacea Ne- capodsa). Comples Rendus Hebdomadaires des Seances de 1 Académie des Sciences, Paris, Ser- ies D, Sciences Naturellés 228: 1395-1397, FELGENHAUER, B.E. AND ABELE, L.G, 1983, Phylogenetic relationships among shrimp-like deeupods. In F.R. Schram (ed.) ‘Crustacean phylogeny”, Crustacean Issues 1: 291-311. 1991, Morphological diversity of decapod sperma- tozoa.322-341, In R.T. Bauverand J.W.Marlin (eds.), “Crustacean sexual biology’. (Columbia University Press: New York). PELSENSTEIN, J, 1985. Confidence limits on phylo- geniés: an approach using the bootstrap, Evolu- tion 39: 783-791. FOREST, J. AND DE SAINT LAURENT, M. 1981. La morphologic externe de Neoglyphea inopi- nata, espece actuelle de Crustacé Décapode Gly- pheide. Resuliats des Campagnes MUSOR- STOM, | — Philippines (18-25 mars 1976) Vol. 1 (2) Mémoires ORSTOM 91; 51-84. GLAESSNER, M.F. 1969. Decapoda. 400-651. In R.C, Moore (ed.) “Treatise oninvertebrale palae- ontology’ Part R Arthropoda 4 (University of Kansas, Geological Society of America; La- wrence). GUINOT, D. 1977. Zoologie. Propositions pour une nouvelle classification des Crustacés Décapodes Brachyoures. Comptes Rendus Hebdomadaines des Séances de |"Academie des Sciences Paris (D) 285; 1049-1052 JAMIESON, B.G.M. 1989. Ultrastructure compari- son of the spermatozoa of Ranina ranina (Oxy- slomali) and of other crabs exemplified by Portunus pelagicus (Brachygnatha) (Crustacea, Brachyura), Zoomorphology 108: 103-111. 1990, The ultrastructure of the spermatozoa of Petalomera lateralis (Gray) (Crustacea, Brachy- ura, Dromiacea) and its phylogenetic signifi- tance. Invertebrate Reproduction and Development 17: 39-45. 1991. Ultrastructure and phylogeny of crostacean spermatozoa. Memoirs of the Queensland Museum 31:109-142. KENSLEY, B. AND WILLIAMS, D. 1986. New shrimps (families Procarididae and Atyidae) from a submerged lava tube on Hawaii. Journal of Crustacean Biology 6: 417-437. KIM, W. AND ABELE, L.G, 1990. Molecular phylo- geny of selected decapod crustaceans based on 18S rRNA nucleotide sequences. Journal of Crustacean Biology 10: 1-13. RICE, A.L, 1980, Crab zoeal morphology and its bering on the classification of the Brachyura. COMPARISON OF PHYLOGENY OF DECAPOQDA 107 Transactions of the Zoological Society af Lon- don 33: 271-424. 1983. Zoeal evidence for brachyuran phylogeny. 3)3-339. In F.R Schram, (ed.) Crustacean phy- logeny. Crustacean Issues I: 313-339, SCHRAM, F.R. 1984. Relationships within eumala- costracan Crustacea. Transactions of the San Diego Society for Natural History 20: 301-12. 1986, ‘Crustacea’, (Oxford University Press; New York, London), 606p. SWOFFORD, D.L. 1990. PAUP: Phylogenetic Analysis Using Parsimony. Version 3.0. Com- puler program distributed by the Hlinwis Natural History Survey, Champaign, Illinois. WINGSTRAND, K.G. 1972. Comparative spermatol- ogy of a pentastomid, Raillietiella hemidactyli anda branchiuran crustacean, Argulus foliaceus, with a discussion of pentastomid relationships. Kongelige Danske Videnskabernes Selskab Bi- ologiske Skrifter 19: 1-72, APPENDIX |. LIST OF CHARACTERS AND CODES USED. ASTERISKS INDICATE CHARACTERS THAT MAP WITHOUT HOMOPLASY ANTENNA II *], Scaphocerite present (0), reduced or absent (1) MAXILLA 1 2. Palp: present and segmented (()). fused 11), absent (2) THORACOPOD I (MAXILLIPED 1) 3. Modified as a maxilliped; no (0), ves (1) 4, Endopod; 7 segments (0), <7 segments (fused and/or rudimentary) (1), absent (2) 5. Exopod; pediform with flagellum (0). lamellar with flagellum (1), lamellar without flagellum (2) 6. Exopodal Jobe (= caridean lobe); present (1), absent (0) THORACOPOD [i (MAXILLIPED II) 7. Modified as 8 maxilliped: no (0), yes (1) 8. Endopod: 7 segments. (()), <7 segments (fused and/or rudimentary) (1). pediform (0), lamelliform (l THORACOPOD III (MAXILLIPED IIT) 9. Modified as a maxilliped: no (0), yes (1) 10, Endopod; 7 segments (0), <7 segments (fused and/or rudimentary) (1), completely tused (2) PEREIOPOD I 11, Distal segments of endopod: achelate (0), sub- chelate (1), chelate (2) * 12. Exopod; present (0), reduced (1), absent (2) PEREIOPQD II 15, Distal segments of endopod; achelate (()), sub- chelate (1), chelate (2) *14, Exopod; present (()), absent (1) PEREIOPOD III 15. Distal segments of endopod; achelate (0), sub- chelate (1), chelate (2) *16, Exopod; present ((), absent (1) PEREIOPOD IV *)7. Exopod; present (0), absent (1) PEREIOPOD V *18. Exopod; present ((),. absent (1) THELYCUM 19. Thelycum on female; present (0), absent (1) PLEOPOD | *20. Petasma; present (0), absent (1) 21. Appendix interna; present (0), absent (1) 22. Appendix masculina; present (0), absent (1) *23. Configuration of pleapud; biramous (0), uni- tamous (1) PLEOPOD II 24. Appendix interna: present (0), absent (1) 25. Appendix masculina; present (0), absent (1) PLEOPOD III 26. Appendix interna; present (0), absent (1) PLEOPOD IV 27. Appendix interna; present (()), absent (1) PLEOPOD V 28. Appendix intema: present (0), absent (1) UROPOD 29, Diaeresis; absent (0), present (1), present with accessory spines (2) FOREGUT 30, Cardiae pads; absent (1), present (0) 31, Ossicles; all present (0), loss of Some (1), loss. of all (2), modified (3) DEVELOPMENT ¥32. Larva: nauplius (0),.z0ea (1) *33, Eggs; free (not incubated) (0), attached to pleapods (incubated) (1) GILLS 34, Gill structure; dendrobranchiate (0), tricho- branchiate (1). phyllobranchiate (2) SECOND ABDOMINAL PLEURON 35. Arrangement of second pleuron: nonoverlap- ping (0), overlapping (1) BRANCHIAL FORMULA Maxilliped HT 36. Podobranch; present (0), absent (1) 37. Arthrobranch; two present (0), one present (1), absent (2) 38, Pleurobranch; present (0), absent (1) Pereiopod | 39, Podobranch; present (0), absent (1) “40, Arthrobranch; two present (0), one present (1), absent (2) *41, Pleurobranch; present (0), absent (1) Pereiopod I 42. Epipod; present (0), absent (1) 43. Podobranch; present (0), absent (1) *44, Arthrobranch; two present (0), one present (1), absent (2) 45. Pleurobranch; present (0), absent (1) 108 MEMOIRS OF THE QUEENSLAND MUSEUM Pereiopod III *52. Arthrobranch; two present (0), one present (1), 46. Epipod; present (0), absent (1) absent (2) 47. Podobranch; present (0), absent (1) 53. Pleurobranch; present (0), absent (1) *48. Arthrobranch: two present (0), one present Pereiopod V (1), absent (2) 54. Epipod; present (0), absent (1) 49. Pleurobranch; present (0), absent (1) 55. Podobranch; present (0), absent (1) Pereiopod IV 56. Arthrobranch; two present (0), one present (1), 50. Epipod; present (0), absent (1) absent (2) 51. Podobranch; present (0), absent (1) 57. Pleurobranch; present (0), absent (1) APPENDIX II. INPUT DATA MATRIX 111111111122222222223333333333444444444455555555 123456789012345678901234567890123456789012345678901234567 Euphausia 010000000000000000000000000000100000000000000000000000000 Penaeus 001020101020202000001101111111000001001000100010011001110 Procaris 011110101000000000111001111111011211111100110011001101111 Caridea 011111111120200000110000000010111211001101110111011101110 Stenopus 011000101021212111111011111100011101001000100010001001110 Axiid 121120101021210111110010000010011210010010000000001001111 Astacoid 111000101021212111011011110010011110210010001000100011110 MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ULTRASTRUCTURE AND PHYLOGENY OF CRUSTACEAN SPERMATOZOA B.G.M. JAMIESON Jamieson, B.G.M. 1991 09 OL; Ulirastructire and phylogeny of crustacean spermatozoa. Memoirs of the Queensland Musewm 3t; (09-142, Brisbane. ISSN 0079-8835, The flagellate spermatozoon of the Remepidia (Speleonectes), differs from the invertebrate ‘primitive sperm’ (aquasperm) only in lacking a mitochondrial midpiece and in contain- tment in a spermatophore. A flagellum occurs elsewhere in Crustacea only in the Maxil- lopoda (Ascothoracica, Cirripedia. Branchiura, Mystacocarida) and in the related Pentastomida, only the Ascothoracica, of these, retaining the plesiomorphic basal flagellar insertion. Cephalocarid (Muichinsaniella) sperm resembling those of remipedes but lacking the flagellum may represent the ground plan for Lhe Phyllopoda, hitherto thought to be the simple, amoeba-like sperm Seen in cuphyllopods and conchostracans. The Nebalia sperm, lacking an acrosome and with microtubular arms, supports the phyllopod status of phyllo- carids. Copepod sperm show no clear affinities with other groups, though the stellate acrosome-less sperm of the cyclopoid Chondracanifus resembles that of some branchiopods, Ostracod sperm include a filiform type performing undulatory waves by means of wing-like structures originating from the endoplasmic reticulum. Jn the Malacos- traca, stomatopad (Sguilla, Orarosquilla) sperm are ovoidal, lacking appendages, with acrosome (re-acquired?) and a pertoralorium; absence of a nuclear membrane, and diffuse chromatin are decapod tendencies: unusual, doublet centrioles are a peracarid-decapod feature. The syncarid (Anaspides tasmaniae) sperm has a subacrosomal filament | perfora- torium], exeptional for Crustacea in being coiled. A syncarid apomorphy is he cytoplasmic ‘skirt’, a plesiomorphy the condensed chromatin and persistent nuclear membrane. Pera- carid monophyly is confirmed by presence, with the questionable exception of tanaids, of across striated pseudoflagellum (possibly a centriolar rootlet homologue) joining the main body at junction of acrosome and nucleus. Tanaid sperm, rounded, lacking appendages, with Jarge acrosome and scattered mitochondria, seen also in syncarids and stomatopods, possibly indicate a basal rather than terminal or intercalated position of the tanaids in the Peracarida. Euphausid and stenopodid sperm, ovoidal and lacking appendages, apparenily lack an acrosome. Dendrobranchiale (penaeid), procandean, caridean shrimps and prawns have sperm with a single acrosomal spike but rarely have arms analogous wilh those characteristic of decapods, Several spikes containing microtubules which traverse the nucleus and often contain chromatin are charactenstic of Palinura (Panulirus, Jasus): Astacidea (Astacidae, Nephropidae); Thalassinidea; Anomura (Paguridae, Diogenidae, Coenobitidae); and Brachyura, though microtubules are reduced or absent above the ‘oxythynchs’. The acrosome of Eubrachyura resembles thal of paguroids, and especially in ils subspheroidal shape Pagurus and Clibanarius, suggesting a paguroid-brachyuran (sister-group?) relationship while the thalassinid (Callianassa) acrosome differs greatly from that of the Astacidea~-Anomura-Brachyura assemblage, contraindicating a [halassinid origin of the Brachyura. The discoidal acrosome and reduced arms of dromiid (Dromidia,, Petalomera) sperm may be plesiomorphic condilions of a group with no close relationship to other brachyurans, Phylogenetic heterogeneity of the Podotremata is supported by differences between dromiid and raninoid sperm and similarities (postnuclear tail) between Ranina and majids, The conventional oxystomate-oxythynch-cancrid-brachyrhynch sub- division of the Brachyura ts nol supported by sperm ultrastructure. Dorippids and portunids, with similar sperm, are placeable in the Helerotremala, whereas the former classification separates the two families in the Oxystomala and Brachyrhyncha, respectively. Familial characteristics of sperm are exemplified by the distinctive ‘xanthid ring’ basal around the perforatorium of xanthids. Thoracalremata (Mictyroidea, Grapsoidea and Ocypodoidea) appear to be typified by presence of an apical opercular button, concentric lamination of the ouler acrosome zone and modification of the xanthid ting. [ Crustacea, phylogeny, spermatozoa, ulirastructure B.G.M. Jamieson, Zoology Department, Universiry of Queensland, St. Lucia, Queensland 4072, Australia; 1 October, 1990, 110 Spermioctadistics, the use of spermatozoal ul- trastructure for reconstruction af phylogeny (Jamieson, 1987), has recently been vindicated (Abele ez al., 1989) from a parsimony analysis of RNA sequences which verified aliribution of the Pentastomida to the Crustacea on the basis of sperm ultrastructure (Wingstrand, 1972). The present paper presents a preliminary survey of sperm ultrastructure in crabs (Brachyura) as a contribution, pending further descriptive work and a computer analysis, towards elucidation of the phylogeny of this group, A phylogenetic review of the sperm of the Crustacea, which includes new ultrastructural observations, will first be presented, A phylogenetic parsimony analysis derived solely from sperm ullrastructure of the type attempted by Jamieson er al. (1987) for Oligochaeta will be deferred pending accu- mulation of additional data, CRUSTACEAN SPERMATOZOA A phylogenetic tree of the Crustacea based on the somatic cladistic analyses of Schram (1986) is given in Fig. 1. Other phylogenies signifi- cantly differing from this might have been used in this essentially heuristic survey (¢.g, Bowman and Abele, 1982). The ultrastructure of sperma- iozoa of the included groups is indicated dia- rammatically according to accounts published y authors cited in the text, below, for these taxa, CLASS REMIPEDIA The Remipedia are primitive, cavernicolous crustaceans only recently described (Yager, 1981) and placed at the base of the crustacean phylogenetic tree by Schram (1986). The body lacks tagmosis into thorax and abdomen. The head is small and the trunk is divided inte many segments. each bearing birarnous, paddle-like appendages, The single known Species, Speleanectes benjamini, is hermaphrodite. Spermatophores are produced cach of which is about 38 pm long with three to possibly six sperm (nuclei) individually located at the proxt- mal end. Each sperm cell (Fig. 1) has three distinet regions: a large nucleus, an acrosontal complex and a flagellum. A flagellum is clse- where seen in the Crustacea only in the Maxil- lopoda, The ovoid nucle: are approximately HY um long and 5 um wide, The inverted cup-shaped, electron dense acro- some is apical on the nucleus. An acrosomal rod peneirates much if not all of the length of the nuclcus (asin cephalocarids). Several mitachon- MEMOIRS OF THE QUEENSLAND MUSEUM dria scattered in the cytoplasm are possibly elim- inated by maturity. A flagellum, of the 9+2 pal- tern (origin unknown but presumably postnuclear), extends several times the length of the nucleus. Centrioles were not observed (Yager, 1989), Jamieson (1987) drew parallels between the albeil aflagellale spermalozoon of the Cephalo- carida and the flagellated aquasperm of the Xi- phosura (with no implication of relationship) and suggested that this similarity, together with the flagellate condition of maxillopod sperm, seemed to suggest that ancestral crustaceans had a primitive sperm sensu Franzén (1956, 1970}, the aquasperm, in the author’s terminology, which in its least modified manifestation has been lermed the plesiosperm (Jamicson, 1986). The remipedian sperm constitutes a remarkable validation of this view as it has the characters we mightascribe to a cephalocarid sperm if a flagel- Jum were added; though mitochondria have not been seen in the cephalocarid. Yager (1989) appears correct in deducing that the rounded form of the nucleus in the remipedian sperm indicates that it is more plesiomorphic than that of the Aseothoracica (see below), hitherto though) to be (he most plesiomorphic for the Crustacea, in which the nucleus is cylindrical. Although the occurrence of a ‘primitive’ sperm in early evolution of the Crustacea can now confidently be asserted, presence of this (though somewhat more modified than the plesiosperm) in Remipedia does not obligatorily demand, nor does it contest, the status of most primitive crustacean taxon envisaged for the Re- mipedia by Schram (1986). Abele er ai (pers. comm.) have suggested from analysis of FRNA sequences that remipedes ure phylogenetically allied to the copepod-cirripede section of the Maxillopoda and are nearer to the Copepoda, CLASS MAXILLOPODA Until discovery of rermpedes, the most basic crustacean sperm, and still the least modified maxillopod sperm, (Grygier, 1980, 1981, 1982) was that of the starfish parasite Dendrogaster (Ascothoracica) (Fig. 1), The anterolateral position of the acrosome in Dendragaster is 4 notable modification, how- ever; it consists of an empty vesicle overlain by an clectron dense layer. The head fs bullet- shaped. the midpiece, approxomately as long hut half as wide, has six or more swellings, possibly representing mitochondria; the post- CRUSTACEAN SPERMATOZOA 111 TANAIDACEA CARIDEA BRACHYURA Palaemonetes MYSIDA ISOPODA CUMACEA DENDROBRANCHIATA AMPHIPODA PERACARIDA Penaeus i | EUPHAUSIACEA Euphausia CIRRIPEDIA BRANCHIURA chin Gi COPEPODA PENTOSTOMIDA (CYCLOPOIDEA) MYSTACOCARIDA. ASCOTHORACICA Chondracanthus EUMALACOSTRACA STOMATOPODA Oratosquilla : PHYLLOCARIDA Nebalia BRANCHIOPODA Simocephalus BRACHYPODA (CEPHALOCARIDA) Hutchinsoniella REMIPEDIA i MAXILLOPODA | Speleonectes PHYLLOPODA REMIPEDIA MALACOSTRACA PHYLLOPODA MAXILLOPODA Part of acrosome Pseudoflagellum Myelin-like Perforatorium membranes Glycogen body Nucleus ‘Schram (1986) Mitochondria =O] Centres Flagellum FIG. 1. Phylogeny of the chief groups of the Crustacea, based on Schram (1986; see inset) with diagram of spermatozoal ultrastructure after authors cited in the text. Original. 11? eriol nuclear fossa houses the basal body of the 9+2 axoneme. The flagellate condition of the ascothoracican sperm is clsewhere restricted (apart trom the Remipedia) to the related masillopod groups Mystacocarida (Brown and Metz, 1967) (Fig. 2G, H), Branchiura, and the related pentas- tomids, (Wingstrand, 1972; Abele et al., 1989) and Cirripedia (Turquier and Pochon-Masson, 1960, 1971; Munn and Barnes, 1970a. b; Po- chon-Musson et al., 1970; Kubo ef al., 1979; Healy and Anderson, 1990) (Fig, 1, 2K), These maxillopods, with the exception of the As- cothoracica, are unified by the synapariorphic origin of the flagellum at the anterior end of the nucleus, The Ascothoracica, with their postnu- clear axoneme, appear to be an isolated relict, preserved through the adoptian of parasitism, that arose near the base of the Maxillopoda. COPFPODA Copepods, usually placed in the Maxillopoda, have a wide variety of aflagellate sperm (Coste etal,, 1979; Pochon-«Masson and Gharagozolou- van Ginneken, 1979: Rousset ef al., 1Y78: Brown, 1970, Raymont e al., 1974, Manier es al, 1978). Their form is very variable. In Tishe hiolo- (huriae (Harpacticoida) (Fig. 21) the spermato- zoon is clongate with definite head and neck (Pochon-Masson e al., 1970, Pochon-Masson MEMOIRS OF THE QUEENSLAND MUSEUM and Gharagezolou-van Ginneken, 1977, 1978, 1979): in Chondracanthus angustatus (Cyclo- poida) the form is star-shaped (Rousset ef af,, 1978). In the Calanoida, Calanus htyperboreus has a discoidal spermatozoon (Brown, 2970) while in Calanus finmarchicus it is oblong (Ray- mont ef al,, 1974), Caligoida have a globular spermatozoon in Nedbranchia cygniformis (Manier et a/., 1978) whereas in Lernanthropus kroyert (Fig. 2J) it has the form of an clongate spindle with sinuous contours (Coste ez al., 1979), Mitochondria are represented in all groups except the Calignida, Only in Neo- branchia eygniformis do centrioles persist into the mature spermatozoon. Microtubules are pre- sent only in elongate sperm (Lernantiropus kroyeri) or in those with spine-like protuber- ances (Chondracanthus angustalus), The acro- some varies from a (wisted point on the tip of the nucleus in Tisbe holothuriae to merely a dense plate on the nucleus in“. Kroyeri or, possibly, a group of vesicles in Neobranchia cvgniformis, The sperm of the cyclopoid Chondracanthus angustatus (Fig. 1) deserve special mention as they show remarkable similaritics to those of the Branchiopoda and Phyllocarida, The mature (spermalophoral) spermatozoon of C, angusta- ius consists of a globular region with irregular contours from which arise three or four ribbon- like arms, with axial microtubules, which give the gameic a stellaic appearance. Mitochondria FIG. 2. Ultrastructure of the spermatozait of some major groups of the Crustacea, From Jamieson (1987) after various authors. A~D,Ostracod, Cvpridypsis. A. head and middle part. B, Tail. C, Enlarged cross section {rom middle region. D, Complete sperm (ram Reger. [970a), E, Cephalocarid, Mutchinsoniella macrantha (trom micrographs by Brown and Metz, 1967), F, Branehiopod, Polvartemta forcipata (from Wingstrand, 1978). G, H, Mystacocarid, Derechetlocaris typteus (aller Brown and Metz. 1967). 1, Copepod, Harpacticoid, Tishe Holathuriae (after Pochon-Masson and Gharagazolou van-Ginneken, 1977). J, Copepad, Siphanostomid, Lernanthropus kroyeri, mid-region of sperm (trom Coste ef al., 1979). K, Cirripede, Generalized diagram (from Pochon-Masson er al. 1970), L, Isopod, Armadillium welgare (from Reger er al., 1979), M, Isopod (from Cotelli ev al, 1976), N, Tanaid. Tanats cavolinit (from Cotelli and Lora Lamia Donin, 1980). 0, Crangonid shrimp, Crangon vulgaris from Pochon-Masson [968b), P, Decapod, Palinura, Panulirus argus (from Talbot and Summers 1978), O, Decapod, Brachyura, Generalized oxyrhynch sperm (from Hinsch, 1973). R, Decapod, Astacidea, Homarus americanus (Talbot and Chanmanon ,1980a). Abbrevialions, a= acrosome; aa= amorphous part of acrosome; ac= apical cap; ad= anterior dise; af= acrosomal filament (pertoratorium ); at= acrosomal tubule; av= acrosomal vesicle; ave= contents of acrosomal vesicle} avm= acrosome vesicle membrane: bd= hasal disc; c= centriole; col=collar; ec= electron dense core; f= flagellum; fl= foamy texture: G1, G2= grooves on surface of sperm: ga= granular part of acrosome; pr= groove, H= head; la= laminar acrosome: jam= inner acrosvmal material; Ir= lamellar region; m= mitochon- drion; Mi= middle part of sperm; mme= microtubule membrane complex; mo= membranous organelle; mi= microtubules; my= myelin figute; n= nucleus; na= nuclear arms;.nc= nuclear cuff; ne= nuclear envelope; nl= nuclear lamella; am= nuclear membrane: oam= ovter.acrosomal membrane; p= perforatorium, pe= periacro- somal material; pm= plasma membrune; pp=posterior projection; ps= pseudopodium; pw= periflagelar wall; fa= feniform part of acrosome, sk= skirtlike structure; sm= subacrosomal material, T= tail part of sperm; la= cross Striated lail-like appendage: r= thickened ring; v= vesicle. CRUSTACEAN SPERMATOZOA 113 iit are grouped at the bases of the arms. The swollen portion of the sperm is entircly occupied by nucleoplasm., A nuclear envelope is absent. The chromatin is finely granular and homogeneous, Centrioles and acrosome are.absent. As in phyl- locarids and branchiopods, an acrosome 1s ab- sent: numerous vesicles produced in the late spermatid from the nuclear membrane are nol considered tn be acrosomal (Roussct ef al., 1978), OSTRACODA Ostracnds, regarded from somatic morphology as derived from the base of the Maxillopoda (Fig. 1), have aflagellate filiform sperm performing undulatory waves generated by peculiar mem- branous organelles (Tétart, 1967; Reger, 1970a; Reger and Florendo, 1969a, b) (Fig. 2 A—D), the contractile bands of Gupta (1968) or wing-like structures of Zissler (1966, 1969). Recently Wingstrand (1988) has deseribed non-filiform sperm in ostracods. CLASS PHYLLOPODA The classification of Schram (1986) which places the Branchiopoda, Brachypoda (Cephalo- carida) and Phyllocarida in an enlarged Phyl- lopoda is observed here, CFPHALOCARIDA The cephalocaridan sperm was described by Brown and Metz (1967) for Hutehinsonrella macrantha (Figs. 1, 2E). Before discovery of remipedes, cephalocarids were generally re- garded as the most plesiomorph crustaccans.on general anatomy, including (Paulus, 1879) that of the ommatidia- Although the sperm is acentriolar and aflagel- late, and mitochondria have not been observed, it has an anterior pointed acrosome and a rounded nucleus perforated by a rod which js interpreted as equivalent to the perforatorium of Limulus by Baccetti (1979), This, with fagella- tion of maxillopod sperm, suggested (Jamieson, 1987) that ancestral crustaceans had a primitive sperm sensu Franzén (1956, 1970), a fact since demonstrated by Yager for remipedes, Because of the absence of a flagellum, eephalocarid sperm are more derived than those of remipedes. BRANCHIOPODA The branchiopods, widely regarded (Siewing, 1963) as a basal group for the Crustacea have profoundly modified sperm, supporting the ad- vanced position given to the group by Schram MEMOIRS OF THE QUEENSLAND MUSEUM (1986). Wingstrand (1978) concludes from an exemplary study of the astounding variety and bizarre forms of branchiopod sperm (Berard, 1974; Brown, 1969; Delavault and Berard, 1974; Garreau de Loubresse, 1967) thal the ancestral branchiopods must have had simple, atmoebs- like sperm of the type seen in euphyllopods and conchostracans. There is, however, no sugges- tion that this amoeboid form seen, lor instance, in Polyartemia forcipatus (Fig. 2F), represents.a Primitive sperm type for the Crustacea as a whole and a flagellated form of the cephalocarid sperm may reasonably be envisaged as ancestral in the Phyllopoda. PHYTLLOCARIDA Phyllocarid (Nebalia) sperm have no polarity; no acrosome: and possess pseudopodia-like lobes; and 20-30 spines, each supported by nine small tubules. The large number of spines is considered by Jespersen (1979) to indicate that they are not modificd flagella, Although this may well be correct, it may be noted that larger num- bers of modified axonemes occur in each sperm of catenulid turbellarians. Phyllocarid sperm Were considered nearest to those of branchiopods by Jamieson (1989c) who noted that Lauterbach (1975), on other grounds, had suggested a branchiopod origin for phyllocarids and hence the Malacostraca. | concur here with Schram (1986) in excluding the Phyllocarida from the Malacostraca and allying them with the former Branchiopoda and Cephalocarida in the Phyllopoda. However, spermalological evi- dence appears to support a sister-group relatian- ship between phyllocarids. and branchiopods, with cephalocarids as the sistergroup of the phyllocarid-branchiopod assemblage (Fig. 1) contrary to the sister-group relationship of cephalocarids and branchiopods recognized by Schram for extant forms. CLASS MALACOSTRACA STOMATOPODA The sperm of Squilia mantis has been de- scribed by Cotelli and Lara Lamia Donin (1983), that of Oratesyuille stephensoni by Jamieson (1989c) and that of Gonodactylus bredinii by Felgenhauer and Abele (1990). Each stoma- topod sperm (Fig. 1), aflagellate and obovoid, is surrounded by an electron dense coat, A sperma- lophore is absent. In contrast, spermatophores are present in eucarids, peracarids (isopods, am- phipods and mysidaceans) and copepods. The CRUSTACEAN SPERMATOZOA discus-shaped acrosome vesicle, is penetrated and underlain by a straight, slender acrosome rod (perforatorium) ensheathed, below the vesicle, in subacrosomal material. Feulgen-positive granular material, indicating chromatin, fills most of the length of the cell but there is no certain nuclear membrane. Two centrioles, con- sisting of doublets each with a radial ‘foot’ as in decapods and peracarids, occur near the acro- some and like it are embedded in the chromatin, Myelin-like membranes are associated with degenerating mitochondria in the posterior re- gion of the cell. Thiéry-positive granules are aggregated as a glycogen body posteriorly in the cell. Stomatopods resemble decapods in their diffuse sperm chromatin but are placed below the syncarid-peracarid-decapod assemblage, If, as is penerally agreed, syncarids originated fromthe malacostracan stem above the departure of the Hoplocarida but at the base of the Eumalacostraca (Brooks, 1969; Jespersen,; 1983), the development in stomatopods of a dif- fuse nucleus and disappeance of a discrete nu- clear membrane must be considered parallelisms (not synapomorphies) with these conditions in decapods. The nuclear membrane tends to be disrupted in dendrobranchiate shrimps and prawns (Talbot and Summers, 1978), is usually intact in procarideans and carideans, and is usu- ally disrupted in Anomura and Brachyura. SYNCARIDA Each spermatozoon of the synearid Anaspides fasmaniae (Fig. 1), described by Jespersen (1983), is surrounded by a capsule (coat) as in stomatopods, and, as in the latter, a spermato- phore is absent. A very clongate subacrasomal filament (perforatoriun) bypasses the nucleus as in isopods, amphipods and cumaccans, rather than penetrating it as in stomatopads. In Anas- pides the porforatorium makes a posteriorly widening spiral of 3-4 turns, a remarkable con- vergence to the condition in the xiphosuran Limulus. As in stamatopods, subacrosomal material forms a sheath around the filament. Posteriorly the filament forms, with the peripheral cytoplasm, a membranous skirt, not seen in other crustacean sperm. which gives the sperm the form of a bell. An axoneme is absent al all stages. The nucleus is condensed with a persistent envelope, In the phylogram (Fig. 1) somatic evidence for the position of the synearids at the base of the cumalacostracans has been accepted, Similari- ties of synearids with most peracarids are the presence of a perforalorium (itself a plesiomor- 115 phy) which, as questionable synapomorphies, (1) is filiform and (2) bypasses the nucleus. The caridoid escape reaction (Dahl, 1983) unites syn- carids, cucarids and peracarids. PERACARIDA Monophyly of peracarids has been denied by Wattling (1981) who considers that they consist of three independent lineages from a syncarid- like ancestor, the mysidacecans; the amphipods; and an isopod-tanaid-cumacean assemblage. From sperm ultrastructure this is clearly incor~ rect. Thus, in mysidaceans, amphipods, isopods (Fig. 2L, M) and Cumacea each sperm consists of twa convergent linear components: the main body of the sperm, containing the nucleus and capped by the acrosome, and joining this anteri- orly, a transversely striated tail-like but non- flagellar structure (possibly a centriolar rootlet homologue) (references in Cotelli et al., 1976; Reger et al., 1970; Reger er al., 1979; Fain- Maurel e¢ al., 1975a,b). This highly peculiar morphology is untikely to have originated more than once. Tanaid Sperm, rounded, lacking appendages, with Jarge acrosome and scattered mitochondria (Cotelli and Lora Lamia Donin, 1980) (Fig. 2N), seen also in syncarids and stomatopods, possibly indicate a basal rather than terminal or interca- lated position of the lanaids in the Peracarida bul these may represent apomorphies related to the specialized fertilization biology of tanaeids, wilh fertilization in a tube. Presence of the perfora- torium in non-lanaid peracarids may be a plesia- morphy ora reacquisition. It has been suggested. however, that the gamete deseribed by Cotelli and Lora Lamia Donin (1980) is in fact a sper- matid and that mature tanaid sperm conform, by light microscopy, lo the typical peracarid struc- ture (Siegs, pers. comm.). This observation, if venfied, would unite all peracarnids as a mono- phyletec entity. EUcAgiDa ORDER EUPHAUSTACEA Euphausid sperm, ovoidal and lacking append- ages, and with irregular central material which may be chromatin (Jamieson, unpublished) (Pig. 1), but otherwise virtually unknown, give little indication of the eucarid ground plan, If lack of urms Were plesiomorphic for eucarids, the arms of most decapods would have to be regarded as having developed independently of hose of phyllopods. This is further suggested by their absence from non-cucarid malacostracans. ORDER DECAPODA Since completion of the draft of this review, a review of decapod sperm by Felgenhauer and Abele (in press) has eeett made available to me (hrough the kindness of the authors. Brief refer- ences to species which they investigated is made in the following account of decapod sperm. SUBORDER DENDROBRANCHIIIATA SUPERFAMILY PENAEOIDEA The Penacoidea, which, with the Sergestojdea, form the Dendrobranchiata, were at one time grouped with the crangonid and palaemonid shrimps within the Natantia as opposed to the Reptantia which contained, inter alta, hermit crabs, crayfish, lobsters and crabs, Penaeoids are now regarded as distinct from the Suborder Eukyphida, containing the Procarididea snd the Caridea, and the Euzygida, contuining the Stenopodidea (Schram, 1°86). Paraphyly of penaid and eukyphid shrimps, as opposed te monophyly of the Natantia, appears to be indi- cated from rRNA studies by Abele ef al. (pers. comm.). These authors, with considerable yusti- fication, retain the names Cariea for Euky- phida, and Stenopodidea for Euzygida and are followed here. Although it does not establish (nor does it contraindicate) its monophyly, the old group Natantia is characterized by uniformity of gross spermatozoal ultrastructure. Similarities include division of the spermatozoon into three regions: acrosomal spike, cytoplasmic collar and nucleus. However, some claims made by Talbot and Summers (1978) and Kleve et al, (1980) for characteristics uniting natantian sperm (absence of centrioles, disso- lution of the nuclear envelope with confluence of nucleoplasm and cytoplasm to form sper- mioplasm) and supposedly distinguishing them from ‘reptant sperm’ are unreliable, being typical of the penacids but not of carids, though some disruption of jhe nuclear en- velope occurs in the carid Palaemonetes, The single spike, giving what is paradoxically but conveniently called the ‘unistellate” condition, distinguishes ‘natantian” sperm from the ‘mul- listellate’ sperm (with more (han one spike or arm) of the Astacidean-Palinuran-Decapod as~- semblage. The distinction gocs deeper as the natanlian spike is acrosomal in function, con- tains actin and undergoes a Ca”? dependeni reaction (Penaeus aztecus, P. setiferus, Brown et al., 1976; Sicyonia ingentis, Clark ef al, 1981, Clark and Griffin, 1988: 8. brevirostris, MEMOIRS OF THE QUEENSLAND MUSEUM Kleve and Clark, 1976, Brown ec al, 1977). Fluorescein labelled anti-actin indicates thal it is the spike which contains actin, and therefore functions like an acrosome filament (perfora- torium), Acridine orange and PAS positive response of the amorphous cap from which the spike arises suggest that the cap is at Icast analogous to an acrosome vesicle (Brown et al,, 1976). In Macrobrachium rosenbergii, al- though the sperm first attaches to the egg by its wide base, the spike bends within 15 sec- onds and penetrates the egg investment from which the sperm base is relevsed (Lynn and Clark, 1}983a). The multiple spikes of non- natant decapods are not acrosomal and contain cither cords of microtubules er extensions of the nucleus or both. Sperm ultrastructure has heen described forthe penacids Penaeus aztects, Clark er al, 1973 (Fig. 1); P. japonicus, Ogawa and Kakuda, 1987; P. setiferus, Lu er al., 1973; Felgenhauer, Abele and Kim, 1958; Felgenhauer and Abele, 1990; Sicyvonia brevirastris, Brown et al., 1977; and §. ingentis, Kleve et al, 1980, Shigekawa ef af. 1980), Shigekawa and Clark, 1986, Clark er al., 1981, Clark and Griffin, 1988. ‘The spermatozoon of Sicyonia ingentis well exemplifies penacid sperm though the acrosome (spike) region is more elaborate than in Penaeus. The sperm is composed of a spherical mainbedy which is partially encompassed by a morpho- logically complex cap region (acrosomal com- plex) from which extends the single spike. The mainbody houses an uncondensed Feulgen-posi- tive nuclear region which is surrounded posteri- orly and laterally by a cytoplasmic layer. A single layer of 0.06 jum vesicles lines the periph- ery of this layer; the bounding membranes of the vesicles are apposed to and appear to fuse with the plasma membrane, Large, 0.7 jam vesicles containing whorled membranous and granular material extend from the inner surface of the cyloplasmic Jayer into the central fibrillar re- gion, A nuclear membrane is also absent in the sperm of Penaeus setiferns (Lu ec.al., 1973). In Sicyonia the jucleus is separated from the cup- like acrosomal complex by a dense plate end a highly organized crystalline lattice which is composed of geometric 350 A squares. The cap region consists, in posterior—anterior sequence, of the dense plate; the crystalline lattice; convo- luted membrane pouches surrounding these; a central granular core immediately anterior to the Jattice and medial to the pouches; spherical bo- dies (voids in the core substance); an electron CRUSTACEAN SPERMATOZOA dense saucer-shaped plate embedded in the centre of the cap and with 12-15 petaloid radiat- ing extensions; and a large anterior granule. The anterior granule gives RNA-ase stable red fluorescence with acridine orange staining, It is conical, with its concave posterior surface ap- plied to the saucer-shaped plate. The spike, which is helicoidal and approximately 6 yam long, extends from the anterior end of the grinule, Cap and spike ate bound by a double membrane formed by fusion of the plasma mem- brane and the convoluted pouch membrane, The pouches and anterior granule, which are PAS- positive, and the spike are considered to com- prise the acrosome (Kleve er al., 1980). Although the nucleus is typically sub- spheroidal in penaeids, it is shown to be consid- erably depressed antero-posteriorly in Penaeus japonica by Ogawa and Kakuda (1987), SUBORDER PLEQCYEMATA 1 here follaw the taxonomic synopsis of Bow- man and Abele (1982) in placing all remaining decapods in the Pleocyemata. INFRAORDER CARIDEA S.LAT. The Infraorder Caridea s, lat, as recognized by Bowman and Abele (1982) contains the infraor- ders Procatididea and Caridea sens Schram 1986, These two groups will be termed the pro- carideans and carideans here. Their sperm re- semble those of dendrobranchiates but there are tendencies for the nucleus to become basally concave so that the sperm, with its anterior spike, takes on a tack-shape, and for development of cross striated longitudinal fibres in the spike, Cross siriation is, however, described for the spike of Penaeus setiferus by Felyenhauer et al. (1988) in the absence of fibres. Felgenhauer and Abele (1990) distinguish those carideans in which the spike is solid and contains cross striated fibrils (c.g. Palaemonetes) from those in which the spike is tubelike with distinct electron dense walls containing anastomozing radial fi- brils (e.g. Rhynchocinetes, Dupré and Barros, 1983; Procaris ascensionis, Felgenhauer et al., 1988), The sperm of Procaris ascensionis has a typi- cal tack or ‘inverted umbrella’ shape, [tis said to differ from sperm of carideans sensu sfricta in having fibrous ridges on the free margins of the cell body and in Jacking periodic cross striations of the fibres which form the spike (Felgenhauer efal,, 1988), However, these striations are absent from some caridean sperm. il? The spermatozoa of caridean shrimps have been described or at least illustrated ultrastruc- turally for the oplophoroid Paratya australien- sis, Jamieson and Robertson, in prep. Atra margaritacea and Typhlatva rogerst, Felgen- hauer and Abele, 1990; the bresilioid Rhyn- chocineies typus, Barros et al., 1986; the palaemonoids Palaemon elegans, Pochon-Mas- son, 1969; P. serratus, Sellos and Le Gal, 1981; Palaemanetes paludosus, Kochlet, 1979 (Fig. 1); Palaemonetes kadiakensis, Felgenhaucr et al, 1988, Felgenhaver and Abele, 1990; and Macrebrackium rosenbergii, Lynn and Clark, 1983a, b, Dougherty, 1987, Dougherty ef a/., 1986, Harris and Sandifer, 1986; and the cran- gonvids Crangon septemspinosa, Arsenault ef al., 1979, 1980, Arsenault, 1984; C. vulvaris, Pochon-Masson. 1968b (Fig. 20); and the hip- polytid Aippolyte zostericola, Pelgenhauer and Abele, 1990. Cross striations typical of, but not constant for, the spike of the caridean sperm are seen in thal of Macrobrachium rosenbergii, Lynn and Clark, 1983a, b; Palaemonetes paludosus and Palae- mon elegans, Pochon-Masson, 1969. These ele- ments of the spike continue into the cap-like expansion at its base lying on the nucleus. The caridéan spike has been said nol to be membrane bound and ta be litle more than a naked perfora- torium of asecondarily simplified acrosome (Pao- chon-Masson, 1969). However, the same author also states thal it is delimited by a simple mem- brane covered by the plasma membrane in Palaemon. A bounding membrane 1s said to be absent in Crengan septemspinosa hy Atsenault (1979). Cross striations were not seen in the spike of Crangon vulgaris examined by Pochon- Masson (19686) nor in Paratve australiensis, (Jamieson and Robertson, in prep). In Paratya the nucleus is subspheroidal as in penacids, but it is depressed in other carideans. It is ellipsoidal in Palaemon elegans (Pochon- Masson, 1969); oblong or oblate spheroidal (Ar- senault ef al ., 1979), having the farm roughly of an ellipsoid with somewhat flattened free sur face, in Crangon septemspinosa; while in Palae- moneles paludosus the nucleus has become inverted cup-shaped, giving the sperm, with its terminal spike, the approximate form of a tack (Kochler, 1979), Transition from an ovoid (plesiomorphic) to the concave (apomorphic) form 9ccurs. in spermiogenesis in ?. paludosus, Persistence of the nuclear envelope appears usu- ally to sel carideans apart from penaeids, though some diseuption of the envelope occurs in Palae- 118 monetes paludosus, (Koehler, 1979), li this spe- cies the envelope is said to be multilayered on the free, concave side but to be lost on the convex side nearest the spike, allowing the uncondensed chromatin to merge with the cytoplasm to form so-called spermioplasm as in Sicyomia; there are numerous PAS-positive vesicles, each with at least two membranes, embedded in the nucleus near its free, concave surface and originating by pinocytosis of the cell surface in the spermatid. Vesicles are normally present peripheral and mostly basal to the nucleus in caridean, us in penaeid sperm. They form a wide reticular zone uround the base and sides of the nucleus. in Paratya australensis. The sperm of Rhyachocinetes typus, described by Barros ez al. (1986) from 2 scanning electron microscope examination, is.of particular interest as it forms a link morphologically with the higher, non-natant decapods in having 1] co- planar radial arms in addition to the typical natantian terminal spike, Contact with the egg continues to be made by the terminal spike which exerts a lytic action, It remains to be determined whether the arms are homologous with those of higher decapods. Mitochondria occur in the cytoplasmic collar of carid sperm but mostly lateral to the nucleus (Crangon vulgaris, Pochon-Masson, 1968b; Palaemon elegans, Pochon-Masson, 1969; C. septemspinosa, Arsenault ef al, 1979). Centri- oles have been observed (generally absent from dendrobranchiate sperm) between the spike and the nucleus, in the cytoplasmic ‘collar’ region, in several carids (Crangen vulgaris, Pochon- Masson, 1968b; C. septemspinosa, Arsenault et al., 1979; Palaemon elegans, Pochon-Masson, 1969), Ongin of the acrosome during spermiogenesis tom the Golgi apparatus is argued for Cravigon sepiemspinosa by Arsenault et al, (1979), hut generally in decapods a Golgi apparatus has not been reported and origin of the acrosame appears to be from vesicles derived from the endo- plasmic reticulum. MEMOIRS OF THE QUEENSLAND MUSEUM INFRAORDER STENOPODOIDEA Sperm structure in this taxonomically prob- lematic group has been examined, for Stenopus hispidus, by Felpenhauer and Abele (1990), The sperm of S. Aispidus, were considered by Felgen- hauer and Abele (1990) to resemible those af stomatopods as Burkenroad (1981) had sug- gested from a light microscope study of the sperm of S. cf. scufellus. The spermatozoon of §. hixypidus is a simple elliptical cell, ca. 7-10 um in diameter, with a prominent lamellar body located on one side against the plasma mem- brane, and resembling that flanking the acro- some in brachyurans. No distinet acrosomal region or stellate appendages were present. Fel- genhauer and Abele (1990) doubted, however, that the sperm were mature on the grounds that arms, typical of other reptants, were absent. The absence of an acrosome is a notable difference frarn stomatopod sperm and, Wilh the ellipsoidal armless form, is here scen a5 a notable resem- blance to cuphausid sperm of possible phylo- penetic significance. INFRAORDER ASTACIDEA Ultrastructural studies of the Astacidea in- clude the families Astacidac (Astacus astacus = A, fluviatilis), Pochon-Masson, 1968b, Lépez- Camps et al., 1981; A. leptodactylus — sperma- tocytes only — Eliakova and Goriachkina, 196A; Cambaroides japonicus, Kaye et al,, 1961; Ya- suzumi e7? al., 1961; Yasuzumi and Lee. 195f; Cambarus sp., Anderson and Ellis, 1967; Paci- Jastacus lentusculus, Dudenhausen and Talbot, 19794, 1982; Procambarus clarkii, Moses, 19614, b); P. leonensts, Felgenhauer and Abele, 1990): Nephropidae, subfamily Nephropinae (Nephireps norvegicus, Chevaillicr, 1965, Chevaillier and Maillet, 1965; Chevaillier, 19666, 1967a, 1967b, 1968); subfamily Ho- marinate (Homarus americanus, Talbot and Chanmanon, 1980a (Fig. 2R), 1980b; H. wul- garis, Pochon-Masson, 1965b, 1965c, 1968a; Enoplometopidae (Enoplometopus occidentalis, Haley, 1985) and Parastacidae (Cherax fenui- manus, Beach and Talbot, 1987, Jamieson, un- FIG, 3, Micrographs of the ultrastructure of the sperm of some decapods. A, a parastacid, Cherax tenuimanus- B and C, w palinurid, Jasus novaehollandiae. C, microtubulur arm af J. nevachollandiae. D, a gelaiheid, Allogalathea sp, E, a porcellanid, Perrolisthes lamarckit, F, diogenid, Clibanarius corallinus. G, a majid, Menaethius monoceros, H, a dromiid, Petalomera lateralls, 1, a taninid, Ranina ranina. J, a portunid, Caphyra rotundifrons. K, a mivtyrid, Mietyris langicarpus. All original, Abbrevations: a= acrosome; ab= apical button; c= capsule; ce= centriole; cl= concentric lamellae: cy= cytoplasm; ec= extensions of capsule; em= extra-cellular matrix; ia= inner acrosome zone; Ja= lateral arms; m= mitochondria; ma= mierotubular arm; mt= microtubules; n= nucleus; n= nuclear arm: o= operculum; oa= outer acrosome zone; p= perfora- torium; pmp= posterior median process: sac=sulbacrosomal chamber; sp= spermatophore; tr= thickened ring, CRUSTACEAN SPERMATOZOA 119 12U published) and ©. alhidus, Beach and Talbat, 1987). The acrosomal-nuclear complex is elongate in the Nephropidae (Figs 2R, 4) but compact and dome-shaped in the Astacidae and Parastacidac (Figs 3A, 4). Enoplometopus is exceptional for the investigated Nephropidae in its dome-shaped acrosome, Wider than long (Fig, 4), resembling that of the Astacidac. This supports exclusion of Enoplemetopus from the Nephropidae by De Saint Laurent (1988), who placed it in a Separate family, the Bnoplometopidac, and superfamily, the Enoplomctopoidea. ASTACIDAE AND PARASTACIDAE Sperm ultrastructure of astacids and para- stacids indicates combined monophyly of the two families. The nucleus of the spermatozoon of Astucus astacus isa biconcave disc with major axis perpendicular to that of the gamete and with a sinuous outline. As in other decapods, the chromatin forms a fine, weakly osmiophile net- work of fibrils varying from 20 A to 200 A (Pochon-Masson, 196%b; Yasuzumi and Lee, 1946; Moses, 1%5la). Occasional clear spaces contain microtubules. In the equatorial plane the nucleus is elongated to form the characteristic spikes (spines, arms or pseudopodia). These number four in Cambarvides and Procambarus clarkii butexceed 20in P. Jeanensis and five, six. or seven in Cambarus viridis (references in Moses, 1961a, b; Felgenhauer and Abele, 1990). Elsewhere folds of the nuclear envelope sur- round mucoid digitations arising from the con- yvoluted membranes in outer parts of the cell (Pochon-Masson, 1968b). There is evidence for formation of jamellar material peripheral to the nucleus ftom the nu- clear membrane, from smooth ER, and from mitochondria and for formation of the wall of the spines from the nuclear membrane and also from the convoluted membranes (Kaye ef a, 1961; Eliakova and Goriachkina, 1966; Yasuzumi and Lee, 1966; Andersen and Ellis, 1967; Pochon- Masson, 1968b: Moses, 196Ya, b; Dudenhausen and Talbot, 1979), Yasuzumi and Lee (1966) have demonstrated that the convoluted mem- branes, especially surrounding the nuclear mem- branes, are the site of TTPase. Tlis considered by Moses (1961b) and Ander- son and Ellis (1967), for Astacidea, and by Talbot and Chanmanon (19804), for Nemarus, MEMOIRS OF THE QUBENSLAND MUSEUM that the nuclear membrane becomes fused with the plasma membrane as a tegument’ containing ‘spermioplasm'’, admixed nucleoplasm and cy- toplasm. Microtubules, ¢, 200 A (Pochon-Masson, 1948h), 220-310 A (Yasuzumi and Lee, 1966) ore. 300 A wide (Anderson and Ellis, 1967), with associated DNA, form several parallel bundles some of Which extend into the spines (Moses, 1961a, b; Anderson and Ellis, [967; Pochon-Masson, 1968b), each of which con- tains, for instance, 30 evenly spaced micro- tubules in Cambaroides (Yasuzumi and Lee, 1966), The microtubules probably are re- sponsible far tnovement of the spines which has been observed in crustacean sperm (Pochon- Masson, 1968b). Centrioles are said to be absent from the ma- ture sperm of A. astacus by Pochon-Masson (1968b) and were observed to disintegrate by maturity in Procambarus (Moses, 1961a,b) and Cambaroides (Yasuzumi et al., 1961) but persist in the mature sperm in Cambarus (Anderson and Ellis, 1967). No Golgi apparatus is known in spermatids or spermatozoa of crayfish but lamel- lar ER in the spermatid resembles this structure (Kaye ev al., 1961), The acrosome in all investigated astacids and parastacids is a dense inverted cup-shaped struc- jure, crescentic in longitudinal section, with the opening towards the nucleus. Tt is wider than long, in contrast with nephropids (Homarus, Ne- phrops) in which, with the exception of Eno- plametapus, it is greatly elongated (Fig. 4). In Astacus astacus, the acrosome is differentiated into an apical operculum (Pochon-Masson, 19686) or apical formation (Lépez-Camps er ai., 1981) and a more basal, thick doughnut-like ring. No such apical differentiation is recognized in Procambarus clarkii, P. leonensis, Cambarus sp. and Cambarwvides japonicus (Moses, 19614; Felgenhauer and Abele, 1990; Anderson and Ellis, 1967; Yasuzumi and Lee, 1966, respec- tively). In Cherax albidus (Parastacidae) some apical whorled material is present within the vesicle but is absent in C. tenuimanus (present study; Beach and Talbot, 1987) (Fig. 3A). The mature acrosome of Pacifastacus is again differ- enliated as an apical cap consisting of whorled stacks of lamellae in addiiton to crystalline inner acrosomal material; and outer acrosomal mate- rial which is homogeneous except for a periph- FIG, 4, Plot af acrosome length against widih for various reptants, Standard deviations for each species are nut Shuwn bul ate small. Acrosome length nm CRUSTACEAN SPERMATOZOA Acrosome length/width A Astacidea A Paguroidea mw Dromiidae O Ranina OHeterotremata @ Thoracotremata @Palinura, JasusoAllogalathea w Petrolisthes 16 AHomarus & Birgus ELONGATE 4Coenobita Astacus A leptodacty lus 6 DEPRESSED AAstacus astacus Eupagurus = Ranina ° oO Allogalathea 4 Enoplometopus Clibanarius—4 o¥ fe) : o (A Paci fastacus v 24 Petrolisthes & AProcambarus A Cherax w Petalomera @ Jasus 0 2 4 6 8 10 12 acrosome width pm 121 122 eral electron dense band (Dudenhausen and Tal- bot, 1982). At maturity in Cambarus the crescent is embedded in dense material within the fila- mentous spermioplasm (Anderson and Ellis, 1967). It seems possible that the reported ab- sence of an operculum in some species may be due to slight immaturity of the spermatozoon and that the internalized whorls of Cherax albidus represent an intermediate ontogenetic stage of the acrosome. In all examined Astacidae and Parastacidae there is a large subacrosomal chamber. In Cam- baroides, Cambarus and Procambarus, a plug- like mass of granular material with filamentous extensions fills the posterior opening of the acro- some. Thin beaded filaments, also shown for both Cherax species by Beach and Talbot (1987), extend into the central concavity from this basal material. At full development an apical process (horn- like process of Yasuzumi and Lee, 1966 or ante- rior acrosomal process of Anderson and Ellis, 1967), which is possibly a derivative of the sus- tentacular cells (Moses, 1961a), emerges from the anterior region of the acrosome. This is clearly the structure questionably considered an acrosomal tubule in Procambarus leonensis by Felgenhauer and Abele (1990). As in most other Malacostraca, the acrosome does not appear to be a Golgi derivative, the hall-mark of the acro- some in other animal groups. Dudenhausen and Talbot (1979) state that the proacrosomal ves- icles, which fuse to form the acrosome, originate from the ER in Pacifastacus. Yasuzumi et al. (1961) state that the acrosome forms from granules in the spermatid similar to those found in the interzonal spindle region in the meiotic divisions. In A. astacus the sperm is not freed from a mucoid sphere until it reaches the external me- dium when, as in Pacifastacus, the spines unfold. The PAS-positive mucoid sheath is provided by the intercalary cells (Moses, 1961a). NEPHROPIDAE The spermatozoa of Homarus americanus (Talbot and Chanmanon, 1980a) (Fig. 2R) and H. vulgaris (Pochon-Masson, 1965c, 1968b) conform with the gross ultrastructural pattern described for the Astacidae but differ, chiefly, in the pronounced elongation of the acrosome (Fig. 4) which projects as a cylinder. Each sperm is 17 or 19 um long and consists of acrosome, sub- acrosomal region, collar containing various or- ganelles, nucleus, and spikes (here three) each 20 um long in H. vulgaris and 38 um long in H. MEMOIRS OF THE QUEENSLAND MUSEUM americanus) which are extensions of the nu- cleus. The acrosome is traversed throughout its length by a weakly PAS-positive electron dense column, the inner acrosomal material, which widens at the ends to form a deep fossa enclosing the finely granular plug-like subacrosomal mate- rial, posteriorly, and a flange supporting an api- cal cap anteriorly. This column is surrounded by a wider zone, strongly PAS-positive and of mod- erate to low electron density, the outer acrosomal material (Talbot and Chanmanon, 1980a). The apical cap, which is weakly PAS-positive, has four concentric zones which, centripetally, are (1) an external wide crystalline zone, (2) a nar- row electron dense crystalline zone, (3) a crys- talline moderately electron dense zone which is a cup-shaped extension of the central, inner acro- somal material (all three identical with the opercular sphincter in H. vulgaris, sensu Po- chon-Masson, 1968b), and (4) the moderately dense contents of this cup (apical portion of central canal, Pochon-Masson, 1968b) which are continuous with the central column. The tip of the cap is deeply indented (Talbot and Chan- manon, 1980a). The acrosome is bounded by a single, tripartite membrane. The acrosome of H. vulgaris is almost identical but the central column is penetrated throughout its length by a narrow central canal (Pochon-Masson, 1968b). The collar and region subjacent to the subacro- somal material, contains small mitochondria with poorly developed cristae and, centrally, a pair of centrioles. The subacrosomal material, which is more dense basally than elsewhere, and the collar are in direct continuity with the chro- matin of the nucleus. The nucleus extends for a short distance as a ‘cuff’ around the base of the acrosome and is not delimited from the acrosome by amembrane. Elsewhere, though, itis bounded by a membrane which appears to be a product of the fusion of the nuclear envelope and the plasma membrane. This composite membrane projects outwards as the spikes or nuclear processes but the nuclear chromatin, which is granular or fi- brillar and uncondensed, is said not to extend into them. The processes are traversed by micro- tubules ensheathed in and interwoven by sheet membranes. The microtubule-membrane com- plexes of the spikes converge in the region of the collar and interconnect to form (as in the axiid, below) a three-sided vault the apex of which immediately underlies the base of the acrosome (Talbot and Chanmanon, 1980a). The acrosome reaction of the H. americanus sperm has been elegantly described by Talbot CRUSTACEAN SPERMATOZOA and Chanmanon (1980b) and corresponds closely to the report of Pochon-Masson (1965c. 1968h) for H. vulgaris (see also Brachyura, Po- chon-Masson, 1968a) but cannot be described here. The ultrastructure of the sperm of the Sub- family Nephropinae, exemplified by Nephrops norvegicus (Chevaillier and Maillet, 1963) is essentially similar to that in the Homarinae de- scribed above. There are again three nuclear processes containing a complex system of lamellae but remarkably, unlike homarince sperm, the processes lack microtubules. Only the basal part of the spine contains lamellae and is Feulgen (DNA) positive. The acrosome (‘cap- sule’) is elongate and consists of a peripheral region and an axial baton. The baton is here interpreted as the homologue of the subacro- somal! material or perforarorium jn homarines, differing In being (like the entire acrasome) much more elongate. This is bounded by a space (here considered the equivalent af the central canal of A. vulgaris) surrounded by an inner fibrillar and, external to this. a homogeneous layer together probably equivalent to the inner acrosomal material (central column) in Ho- marus, It is proteinaccous and PAS negative, The peripheral region is clearly the homologue of the outer acrosormal region and. like it. is PAS-positive, A protemaceous ‘apical granule’ is possibly the equivalent of the homarine apical cup (operculum) ENOPLOMETOPIDAE As indicated abave,, the sperm of Exoplame- lopus occidentalis, described by Haley (1986), who termed it an axiid, appears to (he writer to be remarkably similar to that of the Astacidae and Paraslacidae and to differ from that of the Nephropidae, in which it has also been placed. and from the paguroid-brachyuran assemhlage in the struclure of the acrosome vésicle. This has the form of a thick walled inverted cup, wider than long, enclosing « very spacious subscro- somal space in which there is finely granular material but no pertoratorium, Centrioles al the base of the acrosome produce microtubules which extend between membranes of the lamel- Jar region distally through the uncondensed nu- cleus as the cores of three radial arms. Decondensed nuclear material surrounds these microtubular cores at least in the bases of the arms. The nuclear and plasma membranes are fused except where the acrosome lies between them. Two types of milochondrion-like struc- 123 tures are present. The first do not survive inta early spermatids while the second form (ap- parently from membranes of the lamellar region according to Haley but possibly in fact generat- ing these) during spermiogenesis. INFRAORDER THALASSINIDEA The Thalassinidea contains seven families of which only two families have representatives which have been investigated for sperm ultra- Structure: Callianassa australiensis (Callianas- sidae) and Thalussina anomala (Thalassinidae) (Tudge, pers, comm.). C. anstraliensis has a spherical sperm with four radiating microtubular arms; a Small, flatacrosome; the remainder of the sperm body being composed of nuclear and cy- toplasmic material. 7, anomala has a morpho- logically different sperm being more oblong in shape and possessing a latger acrosome vesicle capped by an operculum with three horizontal layers, The acrosome vesicle is anterior to the cytoplasmic region, from which several micro- tubular arms orginate, and a small nuclear re- gion is present posteriorly. INFRAORDER PALINURA The ultrastructure of the spermatozoon af the spiny lobsters, Panulirus argus and P. guttarus, has been investigated by Talbot and Summers (1978), that of Jasus novaehallandiae by Jamie- son (in prep.) (Fig. 3B,C) (Palinuridae) and that of Seyllarus chacei (Seyllaridac) by McKnight und Hinsch (1986). Each Panulirus sperm (Fig. 2P) is spherical and consists of a nucleus, lamellar region and, at one pole. the acrosome, The nucleus contains uncondensed, Feulgen-positive chromatin and is limited by an intact nuclear envelope which is very closely applied to the plasma membrane except where the nucleus abuts the acrosome and lamellar regions. A variable number (3-12) of spikes radiates from the nucleus. They are exten- sions of the nucleus and are bounded by its envelope. Microtubules span the nucleus and extend into the spikes. The chromatin is continu- ous with the lumen af the spike but does not extend into it. The spikes are stationary and the sperm is non-motile. The lamellar body, which lies at one side of the base of the acrosome und external to the nuclear envelope. contains numerous stacks of membranes and small mito- chondria-like bodies, The acrosome vesicle (PAS-positive region) is lens shaped and is limited entirely by a mem- brane, It is structurally complex and is divisible 124 inlo four discrete zones which are respectively, in posterior-anterior sequence, homogeneous; scrolled; crystalline; and flocculent.. The homo- geneous region forms an electron dense cap sit- uated in a depression in the nucleus and surrounding the scroll and part of the crystalline regions. The scroll region is electron dense with numerous lucid channels which produce the dis- tinctive scroll pattern. The crystalline region is dome-shaped and in section has a very regular prid arrangement of dense squares which in longitudinal seclion are seen to be vertical rods, The fourth, anteriarmost, region contains a dis- persed flocculent moderately dense material with coalesced heads or granules. The vesicle is surrounded by periacrosomal matertul which is flocculent near the base of the acrosome and filamentous at the apex. It includes eleetron dense bundles of filaments which in longitudinal sections appear as dense cores in pockets formed between the acrosomal and plasma membranes, Microtubules and centrioles were sometimes scen in the basal part of the periacrosomal region (Talbot and Summers, 1978). The acrosome of Scyllarus chacei is unique in investigated Crustacea in having electron dense rays (40 in number) radiating from a dense disc which lies at the apex of the bell shaped vesicle, under the plasma membrane, like the struts of an umbrella, Beneath these the acrosome contains homogeneous, scrolled and crystalline areas, The nuclear membrane is folded and irregular and the chromatin diffuse. The cytoplasmic area contains the lamellar complex, a few mitechon- dria and a large number of microtubules. The number of microtubular arms arising from the body of the sperm as extensions of the cytoplasm is not specified (McKnight and Hinsch, 1986). Panulirid sperm conform to the general *rep- tant’ plan and are nearest to those of the astacids such as Homarus and Nephrops. The latter differ, however, in having a constant number (three) of spikes and in having « very clongale acrosomal vesicle with the periacrosomal mate- rial (percutor organ or perforatorium) extending up into the base of the vesicle. Possession of crystalline material (Talbot and Summers, 1978; McKnight and Hinsch, 1986) is an unusual con- dition for decapods, shared with nephropids, though with doubtful homology. Tn the absence of a basal invagination of the acrosome, the palinurid sperm differs conspicuously from sperm of astacids and the anomuran-brachyuroid assemblage and it would not appear that palin- MEMOIRS OF THE QUEENSLAND MUSEUM urids are near the ancestry of the fatter assem- blage. INFRAORDER ANOMVRA (8. strict, Anomala s. Schram, 1986) The Anomura contain 13 families. Sperm mor- phology at the light and electron microscope eve] has been carried owt on representatives fram six of these: within the Paguroidea, the Diogenidae (Clibanarius longitarsis, Dhillon, 1964, 1968; Clibanarius taeniatus, Clibanarius virescens, Tudge, unpubl, Clibanarius coral- linus, Jamieson, in prep. (Fig. 3F), Dardanus sp., and Diogenes sp,, Tudge, unpubl.); the Coeno- bitidac (Cornobite elypearus, Hinsch, 1980 a, b: Coenohila spinasas, Tudge, unpubl., and Birgus lairo, Tudge and Jamieson, 1991); and the Paguridae (Pagurus (=Eupapurus) bernhardus, Pochon-Masson, 1963; Chevaillicr, 1966, 1967, 1968, 1970): in the Galatheidac, Al/ogalathea sp. (Jamieson, in prep.) (Fig. 3D): in the Porcel- lanidae, Petrolisthes lamarckit (Jamieson, in prep.) (Fig. 3E) and in the Hippidae, Emerira talpoida, Pearse ef a/., 1942; Barker and Austin, 1963; E. analega, Vaughn,1968a, b; Vaughn ef al., 1969; Vaughn and Locy, 1969; Vaughn and Thomson, 1972; and E, asiatiea, Subramoniam. 1977). Most of the anomurans have sperm morphol- ogy characterised by an ¢longate to oblate, com- plex acrosome projecting anteriorly to the nuclear material and capped by un clectron- dense, domed or conical operculum; and three long microtubular arms (possibly more in the Hippidae), radiating from the cytoplasmic re- gion anterior to the nucleus; and diffuse chroma- tin. Clibanarius spp. and Pagurus bernhardus, are exceptional only in having a shorter, more ovoid acrosome, A scatler diagram showing the proportions of the acrosomes (Jength: width) in various rep- tants, including anomurans, is given in Fig. 4. BRACHYURA In the present study of brachyuran spermato- zoal ultrastructure it is proposed to inyestigate the validity of two conflicting classifications of the Brachyura. The first, which has been summa- rized by Warner (1977) and is the more familiar to most workers, divides the Brachyura inte five sections, the Dromiacea, Oxystomata, Oxyrhyn- cha, Cancridea and Brachyrhyncha. This classi- fication, with included families for which sperm ultrastructure is Known, is shown in Table 1. Footnotes in the Table allude to the alternative CRUSTACEAN SPERMATOZOA 125 TABLE 1. Ultrastructural investigations of spermatozoa of the Brachyura. Higher taxon & Family Dromiacea! Dromiidae Oxystomata Raninidae* Oxyrhyncha Majidae’ Parthenopidae’ Cancridea Cancridae* Brachyrhyncha Portunidae® Dorippidae? Calappidae’ Xanthidae™ Leucosiidae’ Pinnotheridae* Grapsidae® » 4 Geryonidae Mictyridae” Ocypodidae* Macrophthalminae* Species Dromidia antillensis Stimpson Petalomera lateralis (Gray) Runina ranina (Linneaus) Chionoeceles opilio (Fabricius) Libinia dubia Milne Edwards Libinia emarginata Linnaeus Macrocoeloma trispinosum (Latreille) Menaethius monucervs (Latreille) Mithrax sp, Latreille Pitho lherminiert Rathbun Podochelu gracilipes Stimpson Podochela riset Stimpson Stenarhyneltus seticornis Lamarack Heteracrypta granulata (Gibbes) Parthenope serratus (H. Milne Edwards) Cancer borealis Stimpson Cancer irroralus Say Cancer magister Dana Cancer pagurus Linnaeus Cancer producius Randall Callinectes sapidus Rathbun Portunas pelagicus (Linnaeus) Carcinus muenas (Linnaeus) Ovalipes ocellaius Caphyra laevis (A. Milne Edwards) Caphyra rotundifrons (A. Milne Edwards) Neodorippe astuta (Fabricius) Calappa hepatica Alcock Menippe mercenaria (Say) Alergatis floridus (Linnaeus) Liagore rubromaculata De Haan Etisus laevimanus Randall Piladius areolatus (Milne-Edwards) Eurypanopeus depressus (Smith, 1869) Eurytium limosum (Say. 1818) lliacantha subglobosa (Stimpson, 1871) Pinntxia sp. White Eriocheir japonicus De Haan Grupsus albolineaius Lamarck Sesarma erythrodactyla Hess Sesarma reticulatum (Say) Geryon fenneri Manning & Holthuis Geryon quinquedens Smith Mictyris longicarpus Latreille OQcypada ceratophthalma Ortmann Uca dussumiert H. Milne Edwards Sperm ultrastructure Brown (1966a, 1970); Felgenhauer and Abele (1990) Jamieson (1990) Jamieson (1989b) Beninger et al. (1988) Hinsch (1973) Hinsch (1969, 1971, 1973. 1986); Vaughn and Hinsch (1972); Hernandez e al. (1989) Hinsch (1973) Present study Hinsch (1973) Hinsch (1973) Hinsch (1973) Hinsch (1973) Hinsch (1973) Hinsch (1973) Hinsch (1973) Langreth (1945, 1969) Langreth (1965, 1969) Langreth (1965, 1969) Pochon-Masson (1968a) Langreth (1465, 1969) Brown (1966a,b); Felgenhauer and Abele (1990) Jamieson (1989b, 1990); Jamieson and Tudge (1990) Chevaillier (1966b, 1967, 1969); Goudea (1982); Pearson and Walker (1975); Pochon-Masson (1962 [spermiogenesis only], 1965, 1968b); Reger et al. (1984) Hinsch (1986) Present study Present study Jamieson and Tudge (1990) Present study Brown (1966a) Jamieson (1989a, 1989) Jamieson (1989a) Jamieson (1989a) Jamieson (1989a) Felgenhauer and Abele (1990) Felgenhauer and Abele (1990) Felgenhauer and Abele (1990) Reger (1970c) Du ef al. (1987); Yasuzumi (1960) Present study Present study Felgenhauer and Abele (1990) Hinsch (1988) Hinsch (1988) Present study Present study Present study Macrophthalmus crassipes H. Milne Edwards Present study 1, 2, 3, 4 Attributions in the alternative system of Guinot (1978) are: 'Podotremata, Dromiacea *Podotremata, Archacobrachyura 3Heterotremata “Thoracotremata, 126 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 2. Brachyuran classification of Guinot (1978). Section Sub-section Podotremata Dromiacea Superfamily Sperm ultrastructure known Homoalodromoidea Archaeobrachyura Heterotremata Eubrachyura" Thoracotremata Gecarcinoidea Dromivoidea Homoloidea Raninoidea Tymoloidea Dorippoidea Calappoidea Portunoidea Xanthoidea Majoidea Parthenopoidea Bellioidea Leucosioidea Grapsovidea Mictyroidea Pinnotheroidea Hexapodoidea Ocypodoidea Dromiidae* Raninidae* Dorippidae* Cancridae, Calappidae* Portunidae* Xanthidae*, Geryonidae Majidae* Parthenopidae Leucosiidae Grapsidae" Mictyridae* Pinnotheridae Ocy podidae* Hymenostomatoidea *Jamieson, Jamieson and Tudge. “De Saint-Laurent (1980b), classification, developed by Guinot (1977, 1978) in which the Brachyura are divided into three groups; the Podotremata (in turn divided into the Dromiacea and Archaeobrachyura). the Heter- otremata and the Thoracotremata (Table 2). It will be shown that Guinot’s classification, though requiring modification, is more con- gruent with sperm ultrastructure than is that pre- sented by Warner. Guinot’s system is based on two, and only two, apomorphies: location of female pores an the sternum of segment 6; and location of the male pores on the sternum of segment 8; these contrast with a plesiomorphic location on the coxa of the corresponding ambu- latory limb. The Thoracotremata possess both apomorphies; the Heterotremata have only the first, the male pores remaining plesiomorphi- cally coxal, though in some families they have migrated to a coxosternal position (Palicidae, some xanthoids) or even a lateral sternal position (some portunids, e.g. Callinectes); the Podotre- mata, as the name suggests, have female and male pores on the coxac. Although this classifi- cation is better supported by sperm ultrastruc- turc, recognition of the Heterotremata on a single apomorphy, the sternal female pores, might not be expected to give a robust group though more confidence might be attached to the Thoracotre- mata based on the apomorphic,, sternal location of female and male pores. Even if acquisition of sternal female pores were a unique, monophy- letic event, the Heterotremata must be paraphy- letic if its descendants (Thoracotremata ) are not included in it as a subset. In Fiy.5 paraphyly of the Heterotremala and monophyly of the in- cluded Thoracotremata is indicated. This caveat does not, however, undermine the lerminal group, the Thoracotremata and this group is supported by spermatozoal apomor- phies. The six species of the Thoracotremata examined here (Fig. 8) show three synapomor- phies (Fig. 5): (1) concentric lamellation of the outer acrosome zone is present in five species, though varying in development in these and ap- parently absent in Uca dussumieri; (2) the oper- culum has an apical button (not seen in Macrophthalmus); and (3) a differentiation of the acrosome contents which appears to be an extension of the basal ring (‘xanthid ring’ of Jamieson, 1989a) is present in at least the grap- sids, the mictyrid and Ocypoda, its homology being uncertain in Uca and Macrophthalmus, In contrast to spermatozoal support for at Icast the thoracotreme assemblage, the Dromiacea— Oxystomala—Oxyrhyncha—Cancridea—Brachythyncha classification (henceforth D—B classification) is CRUSTACEAN SPERMATOZOA Dromiidae Raninidae Majidae Poriunidae Dorippidae Xanthidae ~Scalappidae ~ short pertoratorium 127 o oc & : : oa r=} Da 8 RS Co < 2 @ @ @ Cs s & < 2 & ¥ & > 2 fy < < zg iJ > > 2 LL fe Ss @ & x x So oe S ¥ FS ow Sg Ss o£ &§ & L$ F F Ss ne = ¢ FF £ FF FS é v ¢ ~ > ~ + s ££ S eS £ ¢ sg s & oe Phreatoicidea Kussakin (1979) Schmaituss (1989) % e @ a s 2 o § s «© =e © $ wr x & Ss & AJ > a PF Fae SF F FEF Feo SF # ° Sg & Ss & By Ss s z 3 < £ £& & £ é x wv Ss = RS fs ss & & F S&F EF F é TTF VP g yr Ff F ¥ FF y Antnuridew Phoratopodiaae Bruce (1981) Tirolanid-like ancestor Wagele (19898) FIG. 4. Some evolutionary trees from previous studies, by Kussakin (1979), Bruce (1981), Schmalfuss (1989), and Wagele (1989a). For the final analyses, however, we decided to analyse the data with all characters left un- ordered (nonadditive). If a character state judged to be plesiomorphic is present for only some members of the taxon in question, e.g. ‘accessory flagellum on antennule in most gammaridean amphipods’, it is scored present in the data matrix for the entire taxon unless otherwise stated, i.e. the derived condition is presumed to define a subset within the taxon. Conversely, of course, if an apomorphic state is present in only some members of the taxon in question, the entire taxon is not scored apomor- phic for that character, but is scored plesiomor- phic. Initially polarized characters were scored as indicated in the ordering of the character state numbers: 0 = plesiomorphic, 1 = apomorphic, 2 = more apomorphic than 1, etc. Homology deci- sions were made on the basis of ontogenetic data and comparative morphology (positional data and anatomical similarity). PHYLOGENETIC ANALYSIS The character state data were analysed with four numerical cladistic analysis packages: HENNIG86 (version 1.5), PHYLIP (version FIG. 3. Examples of various isopod families and genera of the suborder Flabellifera. A, Cirolanidae (Metacirolana joanneae, SDNHM). B, Tridentellidae (Tridentella glutacantha, from Delaney and Brusca, 1985). C, Aegidae (Aega plebeia, from Brusca, 1983). D, Cymothoidae (Ceratothoa gilberti, from Brusca, 1981), E, Limnoriidae (Limnoria quadripunctata). F, Serolidae (Serolis carinata, SDNHM A.0114). G, Anuropidae (Anuropus bathypelagicus). H, Sphaeromatidae (Gnorimosphaeroma insulare). 1, Sphaero- matidae (Exosphaeroma amplicauda). J, Sphaeromatidae (Bathycopea daltonae). K, Sphaeromatidae (Par- aleptosphaeroma glynni). 3,2), PAUP (version 3.0), and MacClade (ver- sion 2.1). HENNIGS86 is advantageous because of tts speed, successive weighting algorithm, ability to depict polytomous tree branches, and ability to store many equal-length trees in memory, The successive weighting program (Farris, 1949, 1989) is useful in reducing the impact of homoplasous characters on tree to- pology, Despite Platnick's (1989) recommends- tion of HENNIG&S as the program of choice, PAUP, MacClade, and the PHYLIP program packae remain useful for comparative and ana- lytical purposes (Sanderson, 1990). PAUP is by far the most user-friendly, is useful to check different character optimisations (a feature cur- rently absent from HENNIG86) on the final trees, and to obtain detailed computations of C.T. (consistency index), character changes, and OTU apomorphy lists. The program MacClade 3.0 was used (on a Macintosh Computer) to branch swap on the final set of trees, in order to evaluate changes in tree length, homoplasy levels, and character placement on selected al- ternalive trees, including those of Schmalfuss (1989), Wagele (1989a), and others, MacClade and PAUP are extremely uscful in their user- friendly ubility to generate graphic repre- sentations of character traces on trees, although MacClade ts senously hindered by its inability to depict multifurcations- The principal statistics used in tree evaluation were overall tree length (step length) and con- sistency index (C_1.). Consistency and retention indices for cach individual character were also computed and used to evaluate their overall ho- moplasy levels. Carpenter (1988) recently argued that consen- sus trees should not be used to construct clado- grams. However, we agree with Anderberg and Tehler (1990) that strict consensus trees are both useful and informative because they reduce the conclusions to only those components which all equal-length shortest |rees have in common. In fact, they are probably a necessity when high levels of homoplasy invest a data sel. Even if successive weighting (i.e, the successive ap- proximations character weighting method of Farvis, 1969) is used, multiple equally parsi- monious trees may derive from a data set high in homoplasy. Thus, we belleve that when numer- ous equally parsimonious trees exist. a strict comsensus tree should be presented. In order to distinguish between some closely related jaxa, We included some characters thal are currently known io be unique to a given MEMOIRS OF THE QUEENSLAND MUSEUM suborder or family (Appendix HT), However, because we were concerned in this study with identifying sister group relationships within the lsopoda, we did not make an effort to identify all of the unique synapomorphies that define only individual taxa (suborders or families). Some characters that proved to define only terminal taxa In our final trees were early-on suspected to be useful in distinguishing larger sister groups. These may be viewed as ‘uninformative’ charac- ters in the final trees by some workers. However, they were important in comparative analyses and tree testing, and as additional taxa and data are described some of these characters may no Jonger remain unique {to a single terminal taxon, For these reasons, we felt it was important to leave them in the data matrix, thus allowing others to use our dala sel as a starting point for further tree (esting. The data set is available. on diskette on request. DISCUSSION OF CHARACTERS S1ALkED Eves Mysidaceans and mictaceans have compound eyes set on short, movable eyestalks (although evestalks are absent in the mictacean Hirsutia), In amphipods, a ‘rudimentary cyestalk’ has been reported from ingolfiellids, Dahl (1977) and Lowry and Poore (1989) have argued that this small process in ingolfiellids is not a true ecye- stalk, but rather is a cuticular process or scale, Lowry and Poore’s argument hinged on the ob- servation thal unequivocal eye stalks in other peracarids have ‘an attitude and position very different’ than seen in the ingolfiellids. Dahl's argument was based on the absence of ‘dioptric and nervous elements’ in this structure. The first argument is not particularly strong because the position and attitude of peracarid eye stalks vary greatly. A positional change in the ingolfiellids could have been caused by a lateral rotation of the entire cye-antennular-antennal complex, Dahl's argument is stronger, although it relies on reductions rather than homologies. Among tan- aidaceans, articulated eye-lobes occur in some Apscudomorpha and Tanaidomorpha, including those with eyes in a variety of positions ranging from that seen in the Mictacea to that seen in the ingolfiellids. In amphipods and isopods the eyes are entirely sessile, although they may be ele- vated on lobes of varying sizes in some species of Phreatoicidea, Gnathiidea, Valvifera, and Asellota. Al the level of the Peracarida most workers might regard motile stalked eyes as {he PHYLOGENETIC ANALYSIS OF THE ISOPODA ancestral condition, and sessile eyes (and loss of eyes) us derived conditions, However, as Bow- man (1984) has noted, the primitive condition in Crustacea 1s still unknown, Thus we lett this char- acter unordered in all analyses. Character No, 1 ts: eves stalked and basally articulated (0), vs eye stalks reduced, lobe-like, but sometimes wilh basal unticulation (1), vs cyes sessile (2). CARAPACE Character 2 describes the development of the carapace. In mysidaceans the carapace generally covers all & thoracomeres and laterally covers the bases of the maxillae and maxillipeds (state fl). In all other peracarids, the carapace is either reduced or absent. In tanaidaccans and mic- taceans, lateral carapace folds still cover the bases of the maxillae and maxillipeds (state 1). In amphipods and isopods a carapace is absent (or exists only as a head shield) and there are no lateral carapace folds (state 2), Because of con- \roversy tegarding the origin (and convergent reductions) of the crustacean carapace, character 2 was left unordered in initial analyses. MOovuttinG lsapods are apparently unique among crustaceans In that the moulling is biphasic, the posterior exoskeleton being shed carlicr than the anterior exoskeleton (George and Sheard, 1954; Price and Holdich, 1980a, b). The break between the two halves occurs at the junction of per- eonites 4 and 5, and the two halves are out of synchrony throughout the moult cycle. Charac- ter 3 iss monophasic moulting (1) vs biphasic moulting (1). Haart and BRANCHIAL STRUCTURES Mysidaceans, tanaidaceans, and mictaccans utilise thin-walled vascularised regions on the carapace for respiratory exchange (percopodal gills are absent). However, loss of [ree curapace folds inthe Amphipoda and Isopoda necessitated the transfer of respiratory functions to other areas of the body (Grindley and Hessler, 1971). Amphipods have unique medial pereopodal cpipodites (‘coxal gills’) presumed to function in respiratory exchange, Whether the medial epipods of amphipods are homologous to the lateral epipods of other crustaceans is not known, In non-isopod peracarids, the heart is positioned in the thorax. The isopod heart is located in thoracomeres 7/8 and the pleon, and they utilize the pleopods for respiration. Character is: heart entirely thoracic (07 vs heart thoraco-abdominal (1). Character 5 is: branchial structures cephalo- thoracic (0) vs branchial structures abdominal (1). Only isopods are scored apomorphic for these two characters. Bopy SuAre Living mysidaceans are laterally compressed. Mast isopods have dorsoventrally flattened bo- dies, Although the badies of amphipods (gam- marideans) and phreatoicideans superficially appear laterally compressed, their bodies are ac- tually more cylindrical or tubular (semicircular in cross-section), The apparent lateral compres- sion in these two groups is an illusion created by the large. ventrally expanded, pereona!l coxel plates and pleonadl epimeres in amphipods, and the large pleonal epimeres of most phreatoi- cideans. Some phreatoicideans also have lateral expansions of the perconal tergites (i.e. true cpimeres, or “pleura') that hang down to give the body an amphipod-like appearance. The cylin- drical nature of the phreatoicidean body was recognised long ago (Nicholls, 1943, 1944) al- though not all authors have acknowledged it (Wiigele, 1989a). In mictaceans, and in an- (huridean and nmcrocerberid rsopods (as well as many arcturid Valvifera and some Asellota) the body is also cylindrical. or semicircular in cross- section. Subeylindrical bodies also may oceur in the Lynseiidae, Given the variety of body shapes that occur in the isopods and other peracatid orders, we can make no judgment on which shape is primitive and which is derived. Body farm is probably strongly sclective and based largely on a group’s behaviour and preferred habitat, and therefore any real phylogenetic sig- nal we may seck has a high probability of being obscured. For example, we could identify ‘nar- row and elongate’ as a potentially homologous feature, but in fact this would introduce obvious homoplasy because the groups that would be sa classified, the Anthuridea and the Microcer- beridea, are probably narrow for entirely differ- ent reasons; the former arc tubiculous and the latter are interstitial, Consequently, we have been cautious regarding use of body form jnour analysis, Some isopods carry the flattened (depressed) bady form to an extreme. Several flabelliferan families (Bathynataltidae. Keuphyliidac, Plakar- thriidae, and Serolidac) have extremely broad and flattened bodies, with broad coxal plates and the cephalon encompassed by the first percanite or at Jeast surrounded by the first pereonile coxal region (character 7) (Serolis, Fig. 3F). The Sphiteru- 134 matidae also includes a number of genera with extremely flattened bodies (Amphorowella, Chitonopsis, Naesicopea, Paracasidina,Playt- nympha, Platysphaera, Paraleptosphaeroma, Platycerceis), as does the [doteidag (Moplisa) and Cirolanidae (Hansenolana), However, these cases are uncommon and are assumed to repre- sent derived conditions in these three families. They also differ from the above taxa in that the cephalon is not entirely encompussed by per- eonite | and the lateral coxal plates are not free. Hlustrations of the dorsal aspect of phora- topodids tend to depict these animals as markedly flat and broad. However, the body of phoratopodids is actually dorsally arched and straight-sided, reminiscent of the ciralanid genus Politolana and many sphaeromatids (Bruce, 1981, pers. obs.). In the Anuropidue the body 1s greatly inflated and globular (character 89), reminiscent of cer- tain hyperiid amphipods. Anuropids are ap- parently all parasiles on gelatinous zooplankton, a feature also shared with most, if not ull, hy- periid amphipods (character 90), In two flabelliferan families, Limmnoriidae and Lynseiidae, the orientation of the head on the pereon differs from that seen in all other isopods. In these two groups, the head is set off from the first pereonite (second thoracomere) and is capable of left-right rotation (character 40); in all other isopods the head fits snugly against the first pereonite and is usually somewhat immersed in it, restricting head movement lo a flexion in the dorso-ventral plane, In the family Serolidae, the tergite of the seventh percomere (and sometimes also the sixth) is reduced and fused with (he adjacent anterior tergile, tendering it indistinguishable dorsally (character 69), Gut TuBr The gut tube of mysidaceans and amphipods has an endodermally derived midgut region (a "truc midgut’). [thas long been known, hawever, that isopods lack an endodermally derived midgut (see recent reviews by Bettica ef al., 1984, Forgarty and Witkus, 1989, and Ilames and Hopkin, 1989). The entire gut tube of an isopod is ectodermally derived; the only en- dodermally-derived structure is the *hepatopan- creas’ (the digestive caeca), According to Scholl (1963) the gut of tamaidaceans may also be en- lirely ectodermal, The condition in mictaceans is not known, Character 8 is: gut tube with en- dodermally derived midgut (0) vs gut tube en- MEMDIRS OF THE QUEENSLAND MUSEUM tirely ectodermally derived, withoul a true midgut region (1). Striatep Muscues Nylund (1986), Nylund ef ai. (1987), and Tjonneland e¢ al. (1987) have described a pattern of membrane systems in the heart myofibers of isopods that they claim is unique within the Malacostraca. We do not find the reasoning given by Nylund ef al. (1987) for placement of the isopods as a sister group to all other cumalacostracans to be logical, because it relies on differences between groups rather than on similarities among them, to define relationships. Nevertheless, ultrastructure of the heart myo- fibres appears to be a unique synapomorphy for isopods, Character 9 is: striated muscles of typi- cal malacostracan lype (0) vs striated muscles with unique myofibril ultrastructure (1), Stconp THORACOMERE Mysidaceans, mictaceans, amphipods, and most isopods have a free second thoracomere (thus one pair of maxillipeds), although the fossil pygocephalomorphans have two sets of maxil- lipeds, In gnathiid tsopods, (he second thoracom- ere is partly or wholly fused to the cephalon, and ihe second thoracopods form » second pair of maxillipeds (called pylopods). In the praniza Slage these appendages are prehensile and used for attachment to the host; in adults they are more typically maxilliped-like. Gnathiids are the only isopods in which the second thoracomere and its appendages are entirely integrated into the head, Dorsal. medial-only fusion of the second thoracomere with the cephalon occurs in several genera in various other isopod suborders and families (Bathynataliidac, Serolidac, several sphacromatid genera |Ancinus, Rathycopea}, some Valvilera [Lyidvtea, Arcturidae], some Asellota [Stenasellus], some Microcerberides | Microcerberus mexicanus]|, and some Phreatoi- cidea), but these cases are nat full fusion and do not incorporate the first pereopods into the mouth field, as in gnathiids. Complete fusion of the second thoracomere to the cephalon may occur in several deep-sea Asellota genera (Ha- plomesus) but, again, the first pereopods are not modified as maxillipeds or appendages of the buccal field. These represent derived conditions found within the Ascllota and occur only in certain deep-sea forms. Character 10 is: second thoracomere free, not fused lo cephalon (0) vs second thoracomere entirely fused to cephalon, with its appendages (the pylopods) functioning PHYLOGENETIC ANAL YSIS OF THE [ISOPODA with the cephalic appendages and serving as a second pair of maxillipeds. Gnathiidea is the only taxon scored apomorphic tor character 1). Troracic Exorons In mysidaceans and mictaccans, all the thora- enpods (primitively) bear cxopods. In \an- aidaceans, Only the anterior thoracopods have >xopods. In amphipods and isapods, no thora- copods have exopods, Character 11 is; al least some thoracopods with exopods (0): cxopods absent from all thoracopods (1), EMBRYOGENY AND HATCHING STAGES All Peracarida have direct development, and in all orders except Mysidacea and Amphipoda the young leave the marsupium ws mancas. resern- bling small adults but with the last (seventh) pair of pereopods not yet developed. However, in some hyperiid amphipods the young do emerge us Virtual mancas, with the seventh legs un- developed or as little more than a limb bud (Bate, 1861; Laval, 1980). Brusca (1954) suggested that the mancoid stage in peracarids may be the product of variations in timing in embryogeny and hatching. Its absence in mysidaceans and amphipods may be lied to a more rapid embryo- togical development (or to delayed postembry- onic hatching) in these taxa (Stecle and Steele, 1975), Manca-like hatching stages also occur in hathynellaceans (which may hatch with several posterior thoracopods undeveloped). Moreover, some thermosbaenaceans and bathynellaccans never develop posterior legs even as adults. In gnathnids, the young leave the marsupium as a morphologically very distinct mancoid stage called the praniza ‘larva* (Wagele, 1985), Mysidaceans and amphipods also differ from other peracarids by possession of ventral flexure of the embryo within (he embryonic membrane, all other peracarids having a dorsal embryonic flexure.. The embryos of mysidaceans and am- phipods develop a ventral (=caudal) furrow that separates the caudal papilla from the ventral part of the rest of the embryo. This is presumably linked to the presence of ventrally curved em- bryos, completion of cleavage in the early stages, und early appearance of the egg-nauplius stage in these groups rapid early holoblastic cleavage. In all thet peracarids that have been studied (except perhaps thermosbaenaceans), develop- ment is slower, the naupliar and metanaupliar somiles appear nearly simultancously, body somites beg proliferating before the the dorsal (=caudal) furrow forms, and the embryos curve dorsally, (Weygolu!, 1958; Sirémberg, 1972), Evcarids in general tend to have ventral flexure of the embryos. Character 51 is: embryos curve ventrally (mysidaceans and amphipods) (0), vs embryos curve dorsally (all other peracarids) (1), Character 12 is: hatching stage not a manca (0) vs hatching slage a manca (1), Character 13 ts: withouta praniza stage (1) vs with a praniza stage (1), Characters 12 and 51 were left unordered in the initial analyses. Bopy SYMMFTRY Only in the isopod Suborder Epicaridea does loss of body symmetry typically occur in adult females. Some species of Cymothoidae may be- come twisted to one side or the other, but this is not regarded as true asymmetry in the sense of loss of, or gross modification of, appendages an one side of the body, asin the epicarideans. Some epicaridcans (most Cryptoniscidac and En- toniscidae) may be so modified as to resemble little more than large egg sacs. Character (4 is: adult females bilaterally symmetrical (0) vs adult females with loss of symmetry (1). PARASITISM Adult female epicarideans are obligate para sites on other crustaceans; the miniature males live in close association with the female, usually buried among the female’s pleopods, Character 13 is: adults not parasitic on other crustaceans (U) vs adulls obligate parasites on other crustaceans (1); only Epicaridea is scored apomorphic for this character. Adult Cymothoidae are obligate and permanent hematophagic parasites on fresh- water and marine fishes, Charactet 66 is; adults obligate and permanent parasites of fishes. Only the Cymothoidae are scored apomorphic for this character, Members of the Acgidac, Coral- lanidae, and Tridentellidac — which are often referred lo as ‘parusiles’ — do nol altach per- manently to their prey, nor do corallanids restrict their diet to fishes. Species in (hese families can be considered as micropredators or temporary parasites, CUTICULAR SENSILLA ' Holdich (1984) has described two types of cuticular sensilla that he regards as unique to the Oniscidea. The first (character 16) is the cuticu- lar tricorn sénsillum, which he adequately decu- ments for the Oniscidae (Qniscus) and Porcellionidae (Porcellio, Porcelliarides), somewhat less convincingly for the Armadillici- idae (Armadctllidium) and Armadillidae (Venez- 156 ile), and even less convincingly for the Ligtidae (Ligia, Ligidium), Philosciidae (Philoscia), Tyl-. idae (Tylos), Platyarthridae (Platvarthras), Tri- chonisctdae (Androniscus, Trichoniscus), and Scyphacidae (Alloniscus, Deto), Powel and Hal craw (1982) document tricorns on Oriseus asel- lus. bul not an Ligia beudiniana or any non-oniseidean species they studied. Modified tricorns similar to those of the aquatic genus Haloniscus can been seen on SEM photographs of the uropeds of Calabozoa (Van Lieshout, 1983, lig. Sd-e), We have scored both onis- cidean infraotders (Tylomorpha and Ligiamor- pha) and the Culahozoidea apomorphie (1) for (his character. The second kind of sensillum is the ‘antennal and uropodal spikes” (character 17), which are complex compound sensillar structures at the tips of the antennae and uropo- dal rami. We have scored both oniscidean in- fraorders apomorphic (1) for this character, PEREON AND PEREOPODS In Isapoda and other peraearid taxa, the per- copods tend to form two functional groups: an anterior set of legs that are directed forwards (antero-ventrally), and a posterior sel of legs that are directed backwards (postero-ventrally). Often this grouping allows the anterior legs to have a somewhat (or extremely) different role in locomotion or feeding than the posterior legs. In Phreatoicidea, Ascllota, and Microcer- beridea, the legs are grouped 4:3 (four pairs af anterior percopods directed forwards and three pairs of posterior pereopods directed back- wards). This seems to be the case with the ter- restrial isopods and the Calabozoidca as well, although the strong isopody in these taxa tends to decrease the difference between the anterior and posterior groups. The 4:3 grouping may be a natural tagmosis for the isopods owing to the MEMOIRS OF THE QUEENSLAND MUSEUM biphasic molt boundary between pereomles 4 and 5, Nevertheless, most other isopods show 4 clear 3:4 tagmosis. The 3:4 condition prevails in all families of flabelliferans, as well as the An- thuridea, Gnathiidea, Epicaridea, and the genus Hadromastax (currently placed in the family Limnoriidae, but being elevated to separate family status. by Bruce and Miller), The preda- tory and parasitic isopods (Anthuridea. Anuropidae, Cirolanidae, Corallanidae, Cy- mothoidae, Protognathiidae, Tridentellidac, Epi- caridea) have 3 pairs of raptorial or grasping anterior limbs, while the 4 pairs of posterior limbs are dedicated more for locomotion. In the strictly parasitic Cymothoidae and Epicaridea, all 7 pairs of legs are strongly prehensile, How- ever, the limbs of eymothoids and epicarideans appear fundamentally different. In cpicarideans, the dactyl is a short acute hook that folds against a greatly enlarged or swollen propadus, which in turn usually articulates on a small triangular carpus, In cymothoids, the dactyl is greatly elon- gated and articulates on an clongate propodus; the curpus is not reduced or triangular shaped, and it usually has an indentation to receive the lip of jhe dactyl, We believe that Wigele's (1989) homologisation of these two kinds of legs is probably in error. The Plakarthriidae seems unique in its posses sion of a 1:6 arrangement of the legs; the basis of pereapod | ts directed posteriorly, whereas in the rest of the legs the bases are directed anteri- orly, However, this may be a secondary effect of the overall body form and orientation of the Perconites, so we have scored this character with a‘?* for this family. Although the Gnathiidea have a more highly derived body lagmosis, their anterior 3 percopods are still directed anterior- wards, and the remaining limbs are directed post- FIG. 5. Examples of isopod antennules, A, Flabellifera, Aegidae (Aege longicornis, type). B, Flabetlifera, Cymothoidae (Verecila actwninata, from Brusca, 1978). C, Flabellifera, Cirolanidae (Parabathynomuys ratefensis, USNM 170251); note sensilla (insert figure to right), D, Flabellifera, Cirolanidae (Bathyncmus giganteus, SDNTIM), E-F, Flabellifera, Cirolanidae (Bathynomus doderleini, USNM 39321); E, ventral view, F, dorsal view; note ‘seale” (insert figure to rightol EB), G, Oniscidea (Ligéa exotica, USNM 43352). H, Oniscidea (Ligidium ungicaudatum, USNM 83070), 1, Anthuridea (Cyathura guareensis, from Brusca and Iverson, 1985). J, Anthuricea (Calathura sp, USNM 99253), K, Anthuridea (Malacanhure caribisen, USNM 173521). L, Phrealoicidea (Phreafomrerus latipes, USNM 60659), M, Gnathiidea (Bathygaathia curvirostris, USNM 10580). N, Flabellifera, Bathynataliidae (Aathynatalia gilchristi, USNM 170549), 0, Serolidae (Serolis albida, USNM 123900). P, Serolidae (Serelis bramleyana, USNM 123911), Q, Flabel- lifera, Anuropidae (Anuropus antarcticus, USNM 112260), R, Valvitera, Idoteidae (Synidotea francesne, from Brusca, 1983). S, Flabellifera, Plakarthriiday (Plakarthrium punctatissium, USNM 32500), T, Epi- cartdea (Scalpelloniscus penicillatus, alter Grygier,1981), U, Epicaridea (Pseudasmmetrione markhami, after Adkinson and Heard, 1980) V, Flabellifera, Limnoriidae (Limnoria kautensis, after Cookson and Cragg, 1988). PHYLOGENETIC ANALYSIS OF THE ISOPODA 157 \ { - 3 2 { \ ! 7 4 Xe | je P MEMOIRS OF THE QUEENSLAND MUSEUM LOOM 20eM FIG. 6. Scanning electron micrographs of the antennular seale of Rathynomus giganteus (Flabellifera, Cirolanidae), Images show 4 different magnifications. eriorwards; this is most casily seen in the active praniza stage. In the Valvifera, both the 3:4 and 4:3 condition occurs; Arcturidae and Amesopodidae have the 4:3 condition, whereas Chaetiliidae, Holog- nathidae, Idoteidae and Xenarcturidae have the 3:4 condition. In the Pseudidotheidae the fourth leg is directed straight out to the side, and species in this family may appear to be 3:4 of 4:3, or even one condition on the left side and the other condition on the right. Because the 3:4 condition is considered primitive in this suborder (Brusca, 1984: 104) Valvifera are scored for that state. The out-group taxa show a variety of func- tional groupings, which may or may not be ho- mologous with the situation seen in the Isopoda, The tanaidaceans and gammaridean amphipods have 24:3 grouping, similar to the Phreatoicidea. In mictaceans, the grouping appears to be 2:5. At least this is the case in Mictocaris: the condition in Hirsutia is less clear, but it appears to be the same. Mysidaceans have no distinct functional grouping of the pereopods, i.e. all legs arise more or less Straight out, ventrolaterally from the body. Hence, four pereopodal conditions, or ‘states’ exist for character 18: 2:5, 3:4, 4:3, and no functional grouping, The relative polarity or direction of evolutionary change(s) associated with this character is unknown, and this charac- ter was initially left unordered in the data set. The states of character 18 are assigned the following codes in the data matrix; 0=no functional group- ing (mysidaceans); 1] = 3:4; 2 = 4:3; 3= 2:5. In adult Gnathiidea, the seventh pereonite is reduced and without pereopods (character 19). Although the seventh pereonite may be lacking in some anthuridean genera (Colanthura, Cruregens, etc.; Poore, 1984) and in a few deep- sea Asellota (Wilson, 1976; 1989), thiscondition PHYLOGENETIC ANALYSIS OF THE [SOPODA is not regarded as primitive in these subnrders, It is probable that genera of isopods in which sexu- ally mature adults lack the seventh perconites evalved by way of neotenic events. In the Phoratopodidae, the posterior pereopods form sculling ‘oars’, and the dactyls are reduced or lost (character 88), Flattened posterior swim- ming percopods also occur in some Munnop- sidae (Asellota) and, to a limited extent, some Cirolanidac (Natatolana), but it is not the primi- tive condition for these two families. True chelipeds do not occur in isopods, except for a few rare cases such as the unusual genera Carpias (Asellota) and Chelanthura (An- Wuridea) although various subchelate and pre- hensile conditions do occur. In three groups, Argidae, Cymothoidae, and Epicaridea, the per- eopods are prehensile, [n aegids, pereopods 1-3 only are prehensile; in cymothoids and epicarids all 7 pairs of pereopods are prehensile. We define a prehensile pereopod as.one in which the dacty! is as long or longer than the propodus, acute, and recurved. Although the pereopods of most epi- carideans are prehensile and used for clinging to their host (crustaceans), they differ fundamen- tally from the Icgs of acgids and cymothoids, as noted above, with which they may not be ho- mologous. At lewst some of the anterior per- eopods of scrolids. phoratopodids, certain Sphacromatidae (Bathkycopea, Tecticeps), and astacillid valviferuns ure subchelate, but we do not regard these condilions as homologous to the prehensile pereopods of cymothoids, aegids or epicarideans. Character 65 is: pereopods nol pre- hensile (except at most pereopod 1) (0), pes- copods 1-3 prehensile (Acgidae, Cymathovidae, Epicaridea) (1), ANTENNULES The antennules of mysidaceans, mictaceans, and amphipods are biramous. {n these groups the flagella arise from the third peduncular article, as in other Peracarida and Fumalacostraca, The antennules of (anaidaceans may be either biramous, with the flagella arising from the fourth article (Apseudomorpha) or uniramous (Neotanaidomorpha, Tanaidomorpha). The antennules of nearly all isopods are uniramous (ste Figs. 5 and f for examples of isopod anten- nules), Mewever, the literature contains many allusions (0 taxa that allegedly possess antennu- Jar scales, or other structures said to represent vestigial flagella or remnants of the nrssing antennular ramus (presumably the exopod}. These various taxa belong to three suborders: Flabellifera, Anthuridea, and Epicaridea. These matters are briefly reviewed below, In the fal- lowing discussion, the ‘peduncle’ of the anien- nule is defined as the enlarged, basal region of the antennule that bears intrinsic musculature. The flagella of isopod antennules lack intrinsic musculature (i.c_no muscles have their origin in the flagellum); flagella arise from the distal-most peduncular article. As in so many other instances, Calman (1909) appears to have been the first to comment on the possible generality and significance of scales on the antennules of isopods, noting their presence in two groups, the genus Bathynonus (Cirolanidae) and ‘cryptoniscan larvae of certain epicarideans.’ Calman did not indicate which epicarideans be was referring to, nor did he pro- vide figures of these structures. [lowever, he referred to therm as ‘minute vestiges of the inner flagellum’, and was presumably referring to spe- cies of Bopyridae sensu lato. Hansen (1925) repeated Calman’s remarks, as have many sul sequent workers. Wagele (19834) used Cal- man's comment as a basis for “homologisation of this (scale-bearing) article with the last peduncular segment of other Malacostraca,’ on the apparent assumption that the antennular peduncle of isopads is homologous to the pro- topod of the other segmental bady appendages. Menzies (1957) added an overtone of generality with a passing comment in his widely cited lim- noriid tnonograph, which reads; “The eonspicu- ous scale attached to the first antenna of Paralimnoria is also characteristic of the genus Limiorie and, as Calman remarks, of the genus Bathynomus (Cirolanidae) and cryptoniscids (suborder Bopyroidea}. It has since been found on Mesanthura (Subarder Anthuridea, Miller and Menzies, 1932, p. &) and the young of Cirolana (unpubl. data) and it is possibly char- acteristic of isopods in general’ (sic). Menzies (1957) provided an illustration of this structure for Paralimaoria andrewsi, In Barhynemus(B. giganteus, B. doederleni, B. kapala) the “antennular scale’ takes (he form of a large, cuticularized, voleano-like process with a deep pit al the terminus from which arise numerous long setae (Fig. 6), Under light micro- scopy this scale resembles a large complex sen- silum. However, SEM examination reveals the scale to be covered with a cuticle bearing the same type of culicular surface Structure seen on the rest of the budy, and to be encircled basally by what may be an articular membrane. Thus, we lenlatively mlerpret this structure as a true scale, Tau i.e. vestigial second ramus. However, in Lhe sim- ilar appearing Parabathynamus a scale does not exist, although a sensory pil is present in the same position on the peduncle, and arising from it is the same kind of setal cluster seen in Barhy- nomus. The lwo kinds of sensory structures are precisely in the same place, and look very similar in all respects, except that in Parabathynomus the sensory pil sits on the cuticular surface, rather than at the end of a scale. In another very similar genus, Booralana, a cluster of sensory sctac arises from a very shallow depression at this same location on the third peduncular article. but there is neither a ‘scale’ or a distinct pit. As for the antennular ‘seale’ of the cryptonis- cus stage, Calman appears to have been relying on Bonnier (1900) and Giard and Bonnier (1887), who stated that the antennules of epi- earideans ‘are often biramous. with numerous sensory filaments,” The cryptoniseus stage of the family Bopyridae sensu lata possesses complex antennules of uncertain homologisatian, The first article, and often the second, typically bear toothed "gnathobasic margins’ thal are of impor- ance in species-level taxonomy. One to three lobes may arise from the third article, gach highly invested with bundles of Jong setac- It is these sensory lobes that Bonnier and Calman presumably interpreted as scales, or vestigial rami or flagella, When several of these sensory Jobes are present, only one (usually the largest) bears acsthetascs, the others are much smaller and bear only ‘simple’ sensory setae, Thus, the large lobe could reasonably be homologised ta a reduced antennular flagellum, but the other one or two lobes appear Lo be large, complex sensilla, or possibly one of these represents a true anten- nular scale. Nielson and Strémbery (1973) de- scribed these lobes in an unidentified bopyrid as being ‘heavily equipped with sensory hairs, densely crowded together...” and noted that the anlennule 18 ‘apparently an effective sensory organ as well as an accessory adhesive one.’ The lobes have been clearly figured by Niclson and Striimberg (1965). Bourdon (1968), Grygier (1981), and others. Grygicr (1981) described the antennular peduncles of Scalpelloniscus penicil- Jatus and S§. binoculis as 3-articulate, noting that the third article bears a ‘pair of |-merous rami and a large, ventrolateral bulb completely covered with brush-like bundle of capillary acs- thetases...", Kensley (1979) has described the antennules of the cryploniscus stage of Zonaphryxus trilobus (Dajidae) also as bearing a trilobed second article. MEMOIKS OF THE QUEENSLAND MUSEUM In limnoriids, most species Uc possess an antennular scale on the distal margin of the third peduncular article, In some species, this ‘scale’ resembles litre more than a large, simple seta (Paralimnoria andrewst Calman). in most, how- ever, it is a Smull, orw-piece, articulating, selue- bearing structure not unlike that of young bopyrids. The antennular scales of limnoriids are very small and difficult to observe without the use of a scanning electron microscope (for good illustrations and SEM photographs see: Kus- sukin and Malytina, 1989, fig. 3: Cookson and Cragg, 1988, figs, 3d, 4d; Cookson, 1989, PhD Diss.). L.J, Cookson (pers. comm.) feels that the Keuphyliidae (Keuphylia nodosa) possesses a scale similar to that of limnoriuds but we have not observed this scale ourselves mor was it il- lustrated by Bruce (1980), In the case of the Anthuridea, ‘scales’ or ves- ligial flagellar processes almost certainly do not exist. We have examined dozens of anthuridean species and failed to find anything resembling a scale or vestigial ramus. We are aware of two teports of such structures in anthurideans. The first was by K.H. Barnard (1925) who claimed an antennular scale wus present on Yenanthura brevitelson, Kensley (1980), using SEM tech- niques, showed this structure to merely bea large sensillum. The other claim was thatof Miller and Menzies (1952), who noted an antennular Seale in a single female specimen of Mesanthura hieroglyphica (from Hawaii), Miller and Men- zies stated, “An antennal scale here observed on the first antenna of a female specimen has not, 10 our knowledge, been reported previously in the Anthuridac. Because of its minute size and ils posilion, itis not readily seen, hence may have been overlooked in other species in the family. IL was not found, however, in the other Hawaiian anthurids described in this paper’ (sic), Their ‘scale’ appears identical to the sensory seta shown by Kensley for X. brevitelson. The final group said to possess antenpular scales, ‘the young of Cirolara’, was cited by Menzies (1957) as, *...ampubl, data)... To our knowledpe, Menzies never published these ‘data’, nor has anyone clse shown antennular scales in this genus. One of us (RCB) has ex- amined hundreds of young Cirolanidae, in Cirolana and many other genera, and has never seenantennularscalcs in any genus of this family other than Badiynomus, In summary, we conclude that only Batiy- nomus, limnoriids, the eryptoniscus stages of bopyrids, and perhaps keuphyliids may possess PHYLOGENETIC ANALYSIS OF THE ISOPODA Siructures on the antennules that might be rea- sonably interpreted as scales, Although we are not entirely convinced that these minute, uniar- ticulate structures are anything, more than com- plex sensilla, we have entered this character into the data matrix anyway. For character 20. all four oul-groups are scored as possessing a biramous antennule (ora scale), and among the isopods the epicarideans and limnoriids are scored the same (0); Cirolanidae is secured *?* because apparently only the genus Buthynomus (of a total of approx. 45 genera) has a scale; Keuphylitdac is also scored *?' because we are uncertain whether a scale is actually present in this group. All other isopods are scored | — lacking antennulat scales, Mysidaceans, mictaceans, amphipods, and other Bumalacostraca (except lanaidaceans) ap- pear to primitively possess a 3-articulate anten- nular peduncle. It scems reasonable to homologise these articles to the 3-articulate pro- topod of other crustacean appendages. Neverthe- less, this 18 Nola certain homologisation because in all crustacean nauplii this appendage is uni- ramous. Morcover, the Apseudomurpha tan- iidaceans have (he aecessory [laygellum on the fourth article of the antennule, arguing for o four-arliculate protopod in this group. Mast isopod workers have regarded the anten- nular peduncle of the sopoda to be 3-articulate. However, Bruce (1981, 1986) felt that isopods *primilively” have 4-articulate antennular peduncles hecause he interpreted the small fourth article that occurs in many groups (that most other workers view as the first flagellar article) as the last, or fourth, peduncular article. Duc to this different interpretation of the fourth article of Cirolanidae (and other non-asel- lote/non-phreatoicidean groups), Bruce (1981, 1986) and Wigele (1983a) were al odds over whether the “primitive’ isopod antennular peduncle was 3-articulate (Wiigele) or 4-urlicu- fate (Bruce), Wigele’s opinion is based on the third article of Bathynomus bearing the scale, which he homologises with a vestigial second flagellum, and at this time we are inclined to accept this homology argument, especially given that the primitive eumalacostracan condition ts almost certainly a 3-articulule antennular peduncle, We see no reason not ta accept that the small fourth article of Barhynoamus is ho- mologous with the short fourth article of most uther Cirolanidae, Anthurides, Bathynatalindae, Gnathiidea, and other laxa (Pig, 5), but da nat consider this article te he part of the peduncle. lal Our examination of the antennule of Bailiy- nomus giganieus (culicle cleared with xylene) indicates that (he 4th article lacks intrinsic musculature, thus conforming to our definition of the flagellar article. Several other authors that have alluded to a 4-jointed antennular peduncle in Bathynomus may have been misinterpreting the first (proximal) article for two articles, due to the presence of a strong ridge on the medial surface of that joint, such that it could be casily mistaken for lwo pieces (Fig. 5 C-F). The fourth peduncular article of Bathvnataliidac noted by Kenslcy (1978) and Bruce (1986) corresponds to the small first flagellar article of other flabel- liferan families. A 4-articulate antennular peduncle un- questionably does occur in two flabelliferan groups, Phoratopodidae and Serolidae. But, in both of these cases the ‘extra’ fourth article rs neither basal nor docs it appear to be ho- mologous to the short fourth article noted above in other isopods, but rather appeats to be the tesu|to?t a subdivision of the third article into twa large cqui-Width joints with continuous marginal contours. In the Serolidae we have examined, the fourth and fifth articles contain no intrinsic musculature, Yan Lieshout's (1983) description of Calabozoidea states Calabozoa pellucida has a S-articulate pedunele, but her figure 2C gives the appearance of a 4-articulate peduncle, possibly with a sensillum on the fourth article, Our observations of Calabozoa indicate that the antennule comprises only 4 articles, presumably a 3-articulate peduncle and uniarticulate flapel- lum (the terminal article bears one aesthetasc and one large seta). The antennules of oniscids are so reduced that we score them as undecided (*7") for this character. Character 21 is: antennular peduncle 3-articulate with an undivided third article (0) vs 4-articulate, presumably by way of subdivision of the third article (1), Only phora- topodids and scrolids are scored apomorphic for this character, Reduction of the antennules probably oecurs in at leastsome species in every isopod suborder, and may oceur in various condifions within a single suborder or family, When the antennules are reduced, a corresponding reduction of the deutocerebrum and its olfactory lobes also usu- ally occurs. (Where it has been studied). The mode of reduction in the various suborders clearly differs. Reduction typically accompanics exploitation of parasitic or interstitial habitats. Valviferans have a S-artivulate pedunele, with the flagellum often reduced to one ar a few vestigial articles. Although antennular reduction is rare in gnathiids, some species also have a 2-articulate peduncle and the Magellum reduced to a few articles. In the interstitial Microcer- beridea, reduction is such that the peduncle can- not be distinguished from the flagellum, A similar reduction takes place in the parasitic Cymothoidae and Epicaridea. Epicarideans have highly reduced antennules, usually of 2-3 urti- cles; a 3-articulate peduncle is generally ap- parent during larval stages, but reduced in adults. In oniscideans reduction results in very small, J-, 2. or 3-articulate antennules, which in some cases. are not even mobjle (although Holdich, 1984; figs 24, 53, shows 4-articulate antennules in Porcellio and Deto). Setation on the second and/or third article suggests that loss of both peduncular and flagellar articles has probably occurred in the Oniscidea, Oniscidean anten- nules also differ in arising directly between the antennad, instead of anteto-medially to Them, as in most other isopods (character 22). Some an- thuridean species also have small, 3-articulate antennules, with setation again suggesting loss of one of the peduncular articles as well as most of the flagellar articles, Among the Flabellifera, all manner of anten- nule reduction occurs, In many cases, il appears that the two basal-most articles have fused, as in many Cirolanidae (C. tuberculata, Delaney, 1986; C, triloba, C. furcata, C, similis, and C. wetoriee, Bruge, 1981; Neocirolana bicrista, Holdich et al., 1981); many Corallana and Ex- corallana (Delaney, 1982, 1984), and perhaps Plakarthrium. In Anuropus, only two antennular articles remain, and their homology is uncertain, However, the second (distal) article in Anuropus is unique in being enormously expanded and scalloped (character 23). In most limmoriids, the peduncle appears to have lost one article, andthe flagellum is also reduced to only a few articles, although mancas tend to have all 3 peduncular MEMOIRS OF THE QUEENSLAND MUSEUM articles. In Lynseiidae and Keuphyliidac, all 3 peduncular articles are present and the flagellum isteduced to 3-very short articles. The antennules are very short in the Cymothoidae and the dis- tinction between the peduncle and flagellum is indiscernible, the entire structure usually being reduced to 7 or § short articles (Fig. 5). Reduced antennular flagella are common in various spe- cies in many genera of Cirolanidae, wherein a 3-articulate peduncle bears a flagellum reduced either by loss or fusion (or both) of the flagellar articles (some Eurydice, Melaciralana, Cirolana, etc.). In examining these various antennular reduc- tions, it is obvious that they are not all ho- mologous. In fact, reduction in most, or even each, group could have been by entirely separate evolutionary cvents. Some may be homologous reductions, but until detailed ultrastructural and anatomical studies have been accomplished a judgmentin this regard cannot be made. For this reason, we have not used antennular reduction as a character in the data set. ANTENNAE A review of the literature suggests that confu- sion exists regarding the number of articles in the antennal peduncle of peracarids (Fig. 7), Much of this confusion’ seems to have derived from viewing the number of peduncular articles as a single feature, when in fact it should probably be examined as at least two separate features (the number of articles in the protopod; and, the num- ber of proximal articles of the ramus that com- bines with the protopod to form a functional unit recognized as the pedunele). We define peduncle as the enlarged basal articles of the antenna that bear intrinsic musculature. The flagella of isopod antennae Jack intrinsic musculature, ic. no muscles have their origin in the flagellum. The antenna of mysidaceans has a 3-arliculate protopod (at least primitively, e.g, Mvsis), which FIG, 7. Examples of isopod antennae, A, Flabellifera, Cirolanidae (Bathynamus gigenteus, SONHM), dorsal aspect showing articulation with head, base of antennule, and floating cuticular piece on articulating membrane, B, Flabellifera, Cirolanicae (Rathynomuy doderleini, USNM 39321, dorsal aspect). C, Phreatoi- cidea (Phreatomerus latipes, USNM 60659). D, Flabellifera, Ciralanidae (Eurydice caudara). B, Flabel- litera, Aegidae (Aega longicornis, holotype), F, Gnathiides (Bathyenathiecurvirestris, USNM 10580), note fusion of distal articles (3 and 4, or 4.and 5), G, Valvifera, Idoteidae (Synisoma sp.). H, Valvifera, Idoteidae (Synidotea francesae, holotype). 1, Anthuridea (Malacathura caribbica, USNM 173521). J, Anthuridea (Calathura sp,, USNM 99253). K, Flobellifera, Cirolanidae (Politolana wickstenae, holotype), F, Flabel- litera, Cymothoidae (Nervcila acuminate). M, Flabellitera, Anuropidae (Anuropus antarcticus, USNM 112260). N-P, Valvifera, Pseudidotheidae (Pseudidathea miersit, USNM 139139). N, entite antenna, with 4-articulgte peduncle and 2-ariiculate Migellum; O-P, first wo peduncular articles, seen from both sides, Q, Oniscidea, Ligiamorpha (Ligia baudiniana, SONHM). R, Oniscidea, Ligiamorpha (Ligia exotica, USNM 43252), S, Oniscidea, Ligiamorpha (J igia occidentalis, SONHM), PHYLOGENETIC ANALYSIS OF THE ISOPODA 163 164 combines with the first two or three flagellar articles to form a 5- or 6-articulate peduncle, although the protopod articles are fused into | or 2 pieces in most living species. A large lamellar scale (the scaphocerite) arises from the third protopodal article in mysidaceans. Mictaceans and amphipods have 2-articulate protopods, that combine with the first 3 flagellar articles to form 5-articulate peduncles (although this is reduced in some amphipods). Mictaceans, and perhaps some apseudomorph tanaidaceans, have a scale on the second article, suggesting that it could be homologous with the third protopodal article of mysidaceans. Amphipods lack an antennal scale. The antennal peduncle of most isopods also comprises 5 articles, although in some taxa it is reduced to 4 or fewer articles, and in the Asellota and Microcerberidea (and possibly some Ciro- lanidae) a 6-articulate peduncle occurs. A review of these conditions in isopods is given below. Milne Edwards and Bouvier (1902) described the antennal peduncle of Bathynomus (Cirolanidae) as 6-articulate. However, they ap- parently mistook the large articulating mem- brane between articles 1 and 2 for an extra article (as noted by Bruce, 1986), Hansen (1903) also described the antennal peduncle of Bathynomus as 6-articulate, but Hansen was focusing on a minute strip of sclerotised cuticle at the base of the antennal peduncle, at the edge of the articu- lating membrane, that he considered to be the vestige of a proximal antennal article, or pre- coxa. Hansen’s conclusion that this cuticular fragment is homologous to a precoxal article was based on the observation that it moved (‘articu- lated’) within the antennal socket when the antenna was moved. Hansen (1903) also claimed to have found 6-articulate antennal peduncles in several species of Cirolana, and in the asellote genera Eurycope and Asellus. Hansen (1905a, 1916) later added Conilera (Cirolanidae) and Ligia (Oniscidea) to the list of taxa with 6-articu- late antennal peduncles, and in his 1925 review added Janira maculosa (another asellote), con- cluding that the 6-articulate condition was primi- live in isopods, and loss of the precoxa was a derived condition. In Hansen’s view, then, the primitive isopod antenna was similar to that of mysidaceans, with a 6-articulate peduncle composed of a 3-articu- late protopod (comprising the precoxa, coxa, and basis) plus the first three articles of the en- dopodite; the rest of the endopodite forming the flagellum. Hansen also noted that in most Asel- lota and in Ligia with a 6-articulate peduncle, the MEMOIRS OF THE QUEENSLAND MUSEUM third article bears a movable scale, or ‘squama’, representing the vestigial exopod. Calman (1909) agreed with Hansen’s conclu- sions, noting that the antennal peduncle of ‘isopods normally comprises 5 articles, but that in the Asellota, Bathynomus, and Cirolana it is 6-articulate, and in some Asellota with 6-articu- late peduncles a scale occurs on the third article. Wigele (1983a; referring to the protopod as the ‘basipodite’) agreed with Hansen’s conclusions that a 6-articulate peduncle is the primitive isopod condition. Wagele used figures taken from Hurley (1957) and Vandel (1960) to il- lustrate 6-articulate peduncles in an asellote (lathrippa longicauda) and a ligiid (Ligia ital- ica), following Hansen in his claim that in the Asellota and Ligiidae a small exopodite (scale) occurs on the third peduncular article. Wigele (1983b) also argued that a 6-articulate antennal peduncle is characteristic of the Microcer- beridea. Other authors have agreed or disagreed with Hansen’s opinion regarding the occurrence of a 6-articulate peduncle in isopods. The literature thus contains references to 6-ar- ticulate antennal peduncles occurring in at least some genera in four groups: Asellota, Microcer- beridea, Oniscidea (Ligiidae), and Cirolanidae. The contention of a 6-articulate peduncle in the Isopoda is tied to Hansen’s and Calman’s homol- ogisation of isopod antennae with a ‘primitive’ crustacean somite appendage with a 3-articulate protopod comprising a precoxa, coxa and basis, with the paired rami arising from the latter. How- ever, it is of considerable interest to note that, among the Malacostraca, an antennal precoxa (and hence a 3-articulate protopod) unquestion- ably occurs only in the groups described above — the mysidaceans and certain isopods. In all other malacostracans the protopod comprises only 2 articles, and the rami (or scale) arises from the second article. This suggests the possibility that the primitive state in Crustacea is a 2-articu- late antennal protopod. We have examined the cuticular piece noted by Hansen on the articulation membrane of the antenna of B. giganteus and also found it to move when the antenna is moved. However, this piece does not articulate with any other article, or with the head, but simply floats free upon the mem- brane. A similar free-floating cuticular piece oc- curs in many genera of Cirolanidae (as noted above), although it has rarely been noticed due to its small size and failure to be removed with the antenna upon dissection. Bruce (1986) com- mented on these structures, noting their presence PHYLOGENETIC ANALYSIS OF THE ISOPODA in at least 12 Australian genera of Cirolanidac and illustrating them for three species (Bathy- nomus immanis, Cirelana cranchii, and Nate- folana rossi). Homologisation of this piece with a true basal, or “precoxal’ article seems a rea- sonable hypothesis, although in our opinion still very much open to testing. Moreover, we know of no flabelliferan isopod that has an antennal scale. In Ligiidae, the antennal peduncle is usually 5-articulate, or occasionally 4-articulate, In this family, both the first and second article may be split by ‘fracture lines” (often subcuticular) on one side, so that an observation trom only one side of the appendage might give the illusion of there being more than one article present — a situation somewhat analogous to that noted abave forthe antennule of Badhynomus. We have examined Ligidiun ungicaudatum, Ligia oc- cidentalis, L. baudiniana, and L. exotica and can find no trace of a precoxal article. Richardson (1905), Van Name (1934), Sutton (1972), Kens- ley and Schotte (1989), and others have also noted that the antennal peduncle of Ligiidae is ho more than 5-articulate, Fragmentation, split- ting, ridges, etc. occur on the proximal articles of the antennal peduncles in many groups, in- eluding Ligiidae, Anthuridea, Phreatoicides, and others. This splitting may have led some authors to mistakenly interpret one of the pieces as a small precoxal article (and thus describe a “6-ar- ticulate’ peduncle). The first mention of an ‘extra! article at the base of the antenna in ligitds was apparently Hansen (1916) who stated, *...in Ligia eceanica we found not only six joints in the peduncle, but even an exopod or squama on the third joint... Hansen's illustration shows what appears to us (0 be a S-articulate peduncle, with the first and second articles fragmented; his ‘precoxal remnant” appears tu be a fragmented plate of the first article, and his ‘scale’ appears to be the protruding edge of a fragment on the second article. The Inner margin of the second article is often slightly elevated, to form a low lobe-like ridge, (hat has perhaps been mistaken for a ‘scale’ in Ligia. Wiigele’s (1983) illusira- tion of Ligia telica (after Vandel, 1960), show- ing @ G-articulate peduncle and a scale, is probably such a misinterpretation, [In the Asellota, 6-articulate antennal peduncles do occur in numerous genera of many families (Fresi, 1972; Gruner, 1965; Hessler, 1970; Siehenaller and Hessler, 1977; Wilson, 1976; 1980, }986a; Wilson and Hessler, 1981); e.g. Haplomunnidae (Haplomunna, Munella, 145 Thylakogaster, Abyssaranea). Desmosomatidac (Balbidocolon, Eugerda, Chelatar, Mirabil- (coxa, Mamedossa, Prochelatar, Tarwolia, Whgia, Thaumastosema); Nannoniscidac (Hebefustis, Exiliniscus, Panetela, Rapaniscus, Regabellator); Munnopsidae (Eurycape), Janir- idae (Jaera, faniropsis); Pleurocopidae { Pleuro- cope); and Munnidae (Munna). Antennal scales occur on the third peduncular article in many of these same asellote taxa, and also on the third article af some species wilh fewer than 6 articles in the peduncle, such that one would interpret the antenna a5 retaining the 3-articulate sympod, but withonly | or 2 articles of the endopod contribut- ing to the peduncles. Wiigele (1982b, 1983b) illustrated a 5-articu- late antennal peduncle for Micracerberus mira- bilis, although he stated that a 6-articulate antennal peduncle is diagnostic for the Micrucer- beridea, Wigele (1983b) clearly shows a ‘pre- coxal article’ on the antenna of Microcerberus tabai. Baldari and Argano (1984) figured a 5-ar- liculate peduncle in Microcerberus redangensis, but stated that it was 4-articulate. Pennak (19538) claimed M. mexicanas had a 5-articulate peduncle, Messana er al, (1978) clearly showed and stated that Micrecerberus anfindicus has a 6-arlicled peduncle. Perhups both the 5-articu- late and 6-articulale conditions occur within the Microcerberidea bul, since the 6-articulate con- dition definitely does occur we regard it as the primitive state. Nicholls (1943, 1944) noted that the antennal pedunele of phreatoicids was 5-articulate, but that a ridge (ar groove) lines the lower boundary of the antennal socket that might suggest the existence of a former proximal (precoxal) article that had been incorporated into the head. How- ever, Such a ridge occurs in many isopods, in- cluding Bathynomus, and Milne Edwards and Bouvier (1902) and Hansen (1903) regarded it as simply part of the head skeleton. An antennal scale probably does not exist in the Anthuridea, In some species, such as Malacanthura caribbica, 2 minute, simple. un- jointed, non-articulating structure exists on the Sth peduncular article; it appears to be a superti- cial cuticular structure, perhaps a sensillum of some kind. We have seen no such structure, or anything resembling a scale, inspecies of Cala- thura or Mesanthura that we have examined. Kensley (pers. comm.) has taken SEM phato- graphs of many anthuridean species, including species that Menzies and K-H_ Barnard claimed had antennal scales, and failed to find anything ats) other than yarious, small, superficial, cuticular structures (spines and setae). In valviferans, the first two articles of the antennal peduncle are more-or-less fused and operate as a single unit, allhough the cuticle of (hese two articles often appears to be ‘frag- mented’ into several pieces, Bruce (1980) de- scribed Keuphylia nodosa (Keuphyliidae) as having w 5-articulate antennal peduncle with a scale on the second article. We have examined this species and consider this structure 1s not a truc ‘scale’) |t appears to be a cuticular fold or a one-piece sensory lobe, and it is on the second (not the third) peduncular article. Character 24 is; antennal peduncle 6-articulate (UV) vs antennal peduncle 5-articulate (1), My- sidaceans, tanaidaceans, microcerberids and ascllotes are scored (0); all other taxa in the data matrix are scored (1). In Cirolanidae both condi- tions might exist (given the hypothesis that the small cuticular pieces on the articulating mem- brane in some species represents a vestigial basal article), and the condition in limnoriids and pro- tognathiids is uncertain; hence these three qaxa are scored (?), Character 24 was left unordered in initial analyses, Character 25 is: antenna biramous, or with a vestigial second flagellum orscale (0) vsantenna uniramous, and without a vestigial second flagellum or scale (1). Mysidaceans., tun- aidaceans, mictaceans, and asellotes are scored primitive for this character (0); all other taxa are scored (1). The ‘scale’ drawn by Bruce (1980) un Xeuphylia appears to us to be a non-articulat- ing stnsory lohe on the second peduncular ar ticle, Character 26 is: Antennae present (1) ve antennae vestigial in adults (1). Only Epicaridea is scored derived (1) for this character. MANDIBLES Of the many different ‘characters’ recognis- able on isopod mandibles, many show suo much homoplasy that they are of little use at The sub- ordinal level of analysis. Insome groups, such as many phreatoicids and asellotes, allofthe typical peracaridan mandibular structures persist, at least on the left mandible. However, reduction, loss, or extreme specialisation of the mandibular pulp, molar process, spine row, anu lacinia mo- bilis appears to have occurred at least several limes in most isopod suborders. Although clear trends can often be seen, especially within cer- lain family clusters, the high level of overall homeplasy in modifications of mast af these MEMOIRS OF THE QUEENSLAND MUSEUM structures reduces their usefulness. in phylo- genetic analysis at the subordinal level, The isopod mandibular palp, like that of other peracarids, is primitively 3-arliculate. Kussakin (1979-26) illustrated a 4-articulate mandibular palp for Caecocassidias pataganica (Sphacro- matigae} and for Cyathura polita (Anthuridea), even though he described the Isopoda as having mandibular palps of 3 or fewer articles. Kus- sakin's figures of 4-articulate mandibular palps are almost certainly in error. Like Hansen (1890) and Bruce (1983. 1988) for several species of Acgidse, Kussakin probably mistook a fold at the base of the proximal palp article for an artic- ulation: Reduction of the mandibular palp (to one or two articles) has occurred im several laxa, and complete loss of the palp has occurred in many groups (Oniscidea, Calabozoidea, Keulphyli- idae, Lynselidae, Gnathtidea, Epicaridea, some Anthuridea, some Cirolanidae, many genera of Asellota, and all non-Holognathidac Valvifera). In gnuthiids (praniza) and epicarideans, the mandibles are modified as small scythe-like pointed stylets with serrate cutting edges, There are two fundamentally different kinds of mandibular molar processes in isopods, A broad, flat or truncated, grinding molar process is char- acteristic of Phreatoicidea, Ascllota, Microcer- beridea, Oniscidea, Valvilera, and most genera in the flabelliferan family Sphaeromatidae. A thin, elongate, blade-like, slicing molar process, with a row of teeth or denticles along the anjero- distal margin, is Characteristic of the primitive Anthuridea (Hyssuridac), and the flabelliferan families Anuropidac, Cirolanidae, Phora topodidac, and Protognathiidac; a reduced blade-like molar process, or its apparent vestige, occurs in most species in the flabelliferan fami- lics Aegidac, Corallanidac, Cymothnidae, and Tridentellidae. Bruce (1981) suggested that the molar process of Phoratopodidae is ‘vestigial’. However, our observations of Phoratopus remex Hale indicate that, while the molar is slightly reduced in size, it is nonetheless. a well- developed, serrate, blade-like structure similar to that of Cirolanidae. The serrate condition alse exists in the Anuropidae and Protognathiidae, in which it is (as in Cirolanidae) ‘articulated’ on the hody of the mandible. In Corallanidae and Tri- dentellidae (and the cirolanid genus Calyptolana Bruce) the molar process is also ‘articulated’ and blade-like, but shows a loss.of the serrate toothed margin and a reduction in size (and even coms plete disappearance in some genera and species). PHYLOGENETIC ANALYSIS OF THE ISOPODA In the primitive anthurideans (Ryssuridae) the hlade-Lke molar process also occasionally ‘ar- ticulates* on the body of the mandible and may bear a serrate or toothed margin (Poore and Lew Ton, 1988a; Wagele, 1981b). In the sphacromatid subfamilies Ancininac ind Tecticeptinae (Ancinus, Bathycepea, and Tecticeps), (he molar process is cither absent or vestigial (Tecticeptinac) or modified as a thin blade-like structure (Ancininae). However, we Jo not regard the molar of Ancininae to be ho- mologous to the blade-like molar described above for the Anthuridea and other flabelliferan families, In ancinines, the molar is apically acute (nol rounded), lacks teeth or denticles at the antero-distal margin, and bears large knife-like serrations along the postero-distal margin, An- cininae and Tecticeplinae possess al) the other features typical of Sphaeromatidae- A molar process is absent in the Epicaridea and Gnathiidea, and in the fMabelliferan families Limnoriidac, Lynseiidae. Bathynataliidac, Keuphyliidac, Plakarthriidac, and Serolidae. The molar process fs also seconilarily vestigial or absent in some genera of Sphacromatidac and Idoteidac, and in few anjhuridean and onis- cidean families. In most isopods, the incisor is a multitobed grasping structure, but in groups specialised for predation or parasitism the incisor is typically blade-like and/or acute, for piercing tissues (Pro- tognathiidae, Corallanidae, Tridentellidae, Aegidae, Cymothoidae, praniza stage of Gnathiidea), In most Limnoriidae the incisor process bears a unique ‘rasp and file’ structure, and a similar condition appears lo be approxi~ mated i) the Lynsciidae (Menzies, 1957; Poore, 1987; Cookson and Cragg, 1488). The presence and size of the lacinia mobilis and spine row components vary greatly among the Peracarida. In the Isopoda, the nature of these structures appears to be closely tied to lifestyle {especially feeding behaviour) and hence strongly selected for and perhaps of limited phy- logenetic value above the gencric level, The presence of both a lacinia and spine row (on both the right and left mandible) is. presumably the primitive peracaridan condition (Dahl and Hessler, 1982), and in many mysidaceans, mic- taceans, and amphipods a gnathal lacinia and associated spine row persist. However, in many isopod groups these structures have been modi- fied, reduced, or lost. especially on the right mandible. No doubt a wealth of phylopenetic information will become available once a more 7 thorough understanding of pattern and homoal- ogy among these sirticlures has been achieved. In most Phreatoicidea, Ascllota, Oniscides, Calabozoidea, and Valvilera, a tacmia and spine tow, often closcly associated with one another, are usually present (at least on the left mandible). The lacinia and spine row are oflen modified, reduced, or lost in the various Mabelliferan fami- lies and genera. A distinct lacinia and spine row are usually absent in the Anthuridea, although remnants may persist in the primitive family Hyssuridae (Poore and Lew Ton, 1988a); the unique ‘lamina dentata’ of anthurideans is pre- sumably the homologue of one or both of these mandibular structures, In the Microcerberidea, the lacinia is absent and only a row of small spines is present, In the Phreatoicidea, a spinose lohe may be present in lieu of a distinct laciniat and spine row, at Jeast on the left mandible; the homology of this spinose lobe is uncertain, but it may represent either a fusion of the lacinia and spine row, ora loss of the lacinia and specializa- lion of the spine raw, A samewhat similar ap- pearing modification occurs in certain Asellota (Aselus), Cirolanidae, and Keuphyliidac. The Limnonidae have 2 somewhat similar structure (called the “Iaciniod spine’), and in the unusual genus Hadromastax only a single simple spine remains. [In the Serolidae. two spine-like struc tures of uncertain homology are usually present. both articulating: one may represent the lacinia and the othera single, enlarged spine of the spine row, or both may be enlarged spines. In the Phoratopodidac and Sphaeromatidac a large gnathal lacinia, with an assuctated spine Tow, a generally present. In the Bathynatalindae a large gnathal lacinia is also present, but with po trace of the spine raw. In the Anuropidae, Protog- nathiidae, Corallanidae, Tridentellidae, Aegidae and Cymothoidac the lacinia and spine row is absent or reduced to a few. vestiziul, spinclike structures, Mandibular characters used in the analysis follow. Character 27 is: mandible with a lamina den: jata — a synapomorphy unique to the Anthu- tidea. Character 28 1s: mandibles of adult males prossly enlarged, projecting anteriorly, forceps- like — asynapomorphy unique to the Gnathtidea (although convergently approximated in the unique cirolanid speci¢s Gnathalana mandibu- lariy Barnard), Character 29 is; mandibles lost in adult females — also asynapomorphy unique to the Gnathlidea, Character 30 is: molar process a broad {lal grinding structure (0) vs molar process a thin blade-like slicing structure (1). Taxa ty MEMOIRS OF THE QUEENSLAND MUSEUM 168 ~~ oT oy \ 2 4 Of % 7 i % | “Ye. i — \ \ | \ / «. N < } a 34 ‘ . Sermo ZN, « ) | SPP A. } \ Sy ie, eas op Bi | ry he Ns t — Z / ; 4 PHYLOGENETIC ANALYSIS OF THE ISOPODA which the molar proccss is absent are scored ‘2° for this character. Character 50 describes four states of the mandibular incisor: broad and multi- toothed (0); teeth reduced fo form a serrate or crenulate margin (1); teeth lost (or fused?) to from a conical projection with basal ‘rasp and file’ (2); and, incisor modified as a recurved, hooklike, acute or subacute piercing-slicing structure (3). Character 91 is; mandibles mod- ified as clongate scythe-like structures with a serrate culling edge (Epicaridea and Gnathiidea). The following taxa are scored as lacking a mandibular palp (character 35): Ligiamorpha, Tylomorpha, Calabozoidea, Epicaridea, Gnathiidea, Keuphyliidae, and Lynsciidac. Loss of the mandibular palp in certain genera of An- thuridea and Asellota is assumed to have taken place independently after the evolution of these suborders, i.e. itis a secondarily derived feature in these taxa. The situation in Valviferans is debatable; Brusca (1984) suggested that pre- sence of a mandibular palp was the primitive valviferan condition and loss of the palp oc- curred after the origin of the unique species Holognathus stewarti, whereas Poore (1990) sagpested that the ancestral valviferan had al- ready Jost the mandibular palp and itreappeared Jater in H. stewarti, We choose the more pursi- monious alternative and assume that the man- dibular palp did not reappear within the Valvifera (sensu Brusca, 1984). Valviterans are thus scored ‘0° for character 35, MAXILLULES The typical isopod maxillule comprises | or 2 prone articles, and two distal lobes — an inner (medial) and outer (lateral) lobe. Mast workers regard these lobes as endites although the precise homologies of the maxillulary arti- cles is uncertain, and the bwo distal lobes. are referred to in the literature by a variety of terms, ¢.g. inner and outer lobes, plates, endites, or rami; or, exopod anid endopod, Furthermore, the proximal articles and region of articulation be. tween the articles and lobes are rarely figured in the literature. Calman (1909) and Hansen (1925) viewed this appendage as comprising only the articles of the protopod, the two proximal articles being the precoxa and coxa, the outer lobe the basis, and the inner lobe an endite of the precoxa. In mysidacens, amphipods and tanaidaceans, at least primitively, there are also two lobes that are clearly endites arising from the second and third articles, as well as a short palp. In mic- laceans two lobes also exist, bul the nature of their articulation and the proximal lobes of this appendage are uncertain. Bowman and Iliffe (1984) refer to these lobes as both endites and as endopod (the distal ‘endite’) and exopod (the proximal ‘endite’), Bowman et af, (1985) re- ferred to these structures. simply as the ‘inner’ and ‘outer’ lobes. Mictaceans, like isopods, lack a maxillulary palp. In a number of isopod taxa the maxillules are highly modified. In the anthurideans, the outer Jobe is a slender stylet and the ioner lobe ts minute (presumably vestigial) or absent. The maxillules of anthurideans have rarely been il- lustrated (Poore, 1978, fig. 17b; Poore and Lew Ton, 1988, fig. 7; and, Poore and Lew Ton, 1Y90, fig. 3). In the primitive anthuridean family Mys- suridac the maxillule bears apical denticles or spines; in the more advanced families (An- thuridae, Antheluridae, Paranthuridae) the api- cal spines are largely reduced, or fused, often resulting ina simple serrate distal margin. Some- what similar conditions (outer lobe a long slender stylet with apical tecth, inner lobe re- duced or absent) exist in the Gnathiidea (praniza stage), Aegidag, Bathynataliidae, Cymothoidae, Lynsciidac, Plakarthriidac, and Tridentellidac. In the Corallanidae the maxillule is highly mod- ified as a sitgle clongate stylet with the apex forming an acute recurved piercing hook. It seems unlikely that these are all homologously FIG, 8, Examples of isopod maxillipeds. A, Oniscidea, Ligiamorpha tLigia exerece, male, USNM 43352). B, Oniscidea, Tylomorpha (Tyles niveus, male, USNM 67703). C, Phreainicidea (PAreatoicus australis, male, USNM 59116), 1D, Asellota (Paramunna quadratifrons, coxa and epipod fet shown, SDNHM specimen), E, Asellota {/anirapsis sp., male; SDNHM specimen). F, Asellota (Lireeus hoppinae, male. USNM 230328). G, Flabellifera, Cirolanidae (Anopsilana sp., male; SONHM specimen), H, Flabellifera, Serolidac (Seralis alhida, gravid female, USNM 123900), [, Flabellifera, Anuropidae (Anuropus antarcticus, non-gravid female, USNM 173141). J, Gnathiidea (Barhygnathia curvirostris, male, USNM 10580), K, Flabellifera, Cirolanidue (Exciralana chamensis, paratype, LACM type No, 3014). L, Plabellifera, Acgidac (Aegu lergirarnis, type). M, Plabellifera, Cymathoidae (Lireneca convexa, female, attached aostegite nol shown, from Brusca 1981). 8, Gnathiidea (Gretiia shed, USNM 1( 2376). 0, pylapod of Barkygnative curv/ratiris, Male, USNM 10580), P, pylopod of Grathia tygia, SNM 112376). Q, Anthuridea (Cyathura gwarcensis, fram Brusca and Iverson 1985), 170 derived morphologies. The maxillules are ves- tigial or lost in adult gnathiids and epicarids. Uncertainty regarding the homologies of the maxillulary articles limits the number of poten- tial characters available on this appendage for phylogenetic analysis. Character 31 is: maxillule present (0), vs re- duced or vestigial in adults (1), vs lost in adults (2). Character 31 was left unordered in initial analyses. Character 32 is: maxillule with palp (0) vs without palp (1). Character 92, the single acute hook-like lobe, is unique to the Coral- lanidae. MAXILLAE The homologies of the maxillary articles of isopods are also unsettled. As with the maxil- lules, there are 1 or 2 proximal articles and 2 distal lobes — an inner (medial) lobe, and an outer (lateral) lobe; the outer lobe is generally divided into two. The proximal articles and ar- ticulation of the two distal lobes are rarely il- lustrated in the literature. Calman (1909) and Hansen (1925) viewed the maxilla as lacking rami and comprising only the protopodal articles with their endites; that is, precoxa, coxa, and basis, with the coxa being expanded as an endite forming the inner lobe, and the basis bearing an endite that forms the split (bilobed) outer lobe. As with the maxillules, the inner and outer lobes of the maxillae have usually been regarded as endites, but they have been referred to in the isopod literature as rami, lobes, plates, endites, and exopod/endopod. The maxillae of mysidaceans retain both the endopod and exopod, as simple one- or two-ar- ticulate platelike structures, and both rami bear endites. Amphipod maxillae primitively re- semble those of isopods but without the divided outer lobe, although in most modern groups they are reduced to one or two simple lobes (as in many oniscideans). The maxillae of mictaceans are very similar to those of most isopods, with a divided outer lobe. The maxillae of tanaidaceans also resemble those of isopods, at least in their primitive form (Halmyrapseudes, Sieg et al., 1982), although in most tanaidaceans the maxil- lae are highly reduced. No isopods retain the primitive crustacean condition of a maxillary palp (the ‘palp’ of Cirolanidae referred to by Bruce, 1986 is actually the inner lobe). Character 34 is: maxillary outer lobe un- divided (0) vs divided into two lobes (1). Micta- ceans, tanaidaceans, and isopods are apomorphic for this character, although in many groups (most MEMOIRS OF THE QUEENSLAND MUSEUM scored ‘?’ in the data matrix) the maxillae are highly modified or reduced to a single lobe or a stylet (see below). In some groups, the maxillae are extremely reduced, vestigial, or absent alto- gether (Gnathiidea, Epicaridea, Anthuridea). In the Anthuridea the maxillae are minute and more-or-less fused with the paragnath (hy- popharynx), or absent altogether. In Protog- nathiidae the outer lobe is apparently absent (Wagele and Brandt, 1988). In the oniscids the maxillae are short and plate-like with 2 non-ar- ticulating lobes, but the homology of these 2 lobes is not clear. Because the variety of maxil- lary reductions in isopods are likely to be the result of different evolutionary processes (non- homologous features), most of these charac- teristics have not been included in the data set. Character 36 is: maxilla modified into a stylet- like lobe with recurved apical (hooklike) setae, a condition seen in certain flabelliferan families (Corallanidae, Tridentellidae, Aegidae, Cy- mothoidae). Character 33 is: maxillae highly reduced and ‘fused’ to the paragnath, or absent altogether (Anthuridea only). Among the Isopoda, only the Phreatoicidea retain the primi- tive peracaridan filter setae row on the medial margin of the maxilla (character 74). MAXILLIPEDS As in most other peracarids, the maxilliped of isopods consists of four distinct regions: a proxi- mal article (the coxa); the basis, with an en- larged, distal, anteriorly directed, blade-like lobe (the endite); an epipod of varying size and shape, lateral to the coxa; and, a palp (primitively com- prising the remaining S articles of the appendage — the ischium through dactylus) (Fig. 8). Am- phipods differ from isopods in possessing (primitively) a 4-articulate maxillipedal palp, and two endites (an inner and an outer) arising from the basis and ischium respectively. The maxillipedal palp is reduced in some taxa in almost all suborders (most Oniscidea [Tri- choniscidae, Tylidae, Oniscidae, Armadillidi- idae], Calabozoidea, many Anthuridea, Gnathiidea, Anuropidae, Aegidae, and Cy- mothoidae). Wagele’s (1989a) claim that a 2-ar- ticulate maxillipedal palp with spines on only the terminal article is a synapomorphy uniting the genus Rocinela (Aegidae) as the sister group of the Cymothoidae is incorrect. Most (if not all) Rocinela have 3-articulate maxillipedal palps with spines on the two distalmost articles (the apical article is minute and easily overlooked). In most isopod taxa, the maxillipedal endites can PHYLOGENETIC ANALYSIS OF THE ISOPOBDA be hooked together by coupling setae (coupling hooks), ¢.g. Phreatoicidea, Asellota, some Valvifera, Epicaridea, Gnathiidea, most Flabel- lifera, Coupling setae also occur on the maxilli- peds of some Mictacea and most Tanaidacea. Maxillipedal coupling setae are absent in Micro- cerberidea, Ligiamorpha, Tylomoarpha, Calabo- zoidea, Anthuridea, and Amphipoda. They have presumably been lost in amphipods as a result of the maxillipeds being fused together; this is also the case in certain tanaid families in which the maxillipeds are fused, such as Leptognathiidae, Pseudotanaidae, and Nototanaidae. Coupling setae may be missing in the anthurideans owing lo the immovable fusion of the maxillipedal coxae and epipods to the head, Coupling sctae are also usually absent in isopod taxa that have reduced endites e.g, Corallanidae, Aegidae, Cy- mothoidae, Lynsetidae, some Cirelanidac; or highly modified maxillipeds {Anuropidae, Plakarthriidac, Protognathiidac, Scrolidac}. In isopods. (as in most peracarids) a lamellar epipod usually arises from the coxa af the max- illiped, In several groups, the epiped may have its proximal part marked off from its distal part by a transverse suture (many Valvifera, Phrea- toicidea, and Flabellifera). In males and non- ovigerous females, the epipods often stem [o function as ‘cheeks’, forming an operculum for the oral field. In gravid females of some taxa (Anthuridea, many Flabellifera), the epipods tend to be onented in such a way lo function as accessory marsupial plates to prevent loss of the embryos from the anterior region of the mar- supium. The isopod epipod is never branchial, as it is in tanaidaceans, In mysidaceans, the epipod is posteriorly directed and carried under the carapace. Epipods are known trom ull isopod suborders except Epicaridea, Gnathiidea, Micro- cerberidea and Calabozoidea. Maxillipedal epipods are also apparently absent inthe families Anuropidae, Corallanidae, and Plakarthriidae, and the unique genus Hadranasiax. In Cirolanidac, Acgidae, and Cymothowae the epipod is apparently reduced or absent in all life stages except brooding females. Wiigele and Brandt's (1988) claim thal Protognathia hacks maxillipedal epipods was based on their study of the single manca-stage individual, Because this genus (and family) was erected on the basis of imanca Specimens, the status of the adult maxil- liped cannot be determined. Incomplete data on the precise ¢listribulion of occurrence of maxil- |ipedal epipods prevent us from using this paten- tially important feature in the data analysis. 171 In at least some isopod groups (e.g. some Phreatoicidea. Ascllota, Valvifera, Flabellifera, Epicaridea, and Gnajhiidea), the maxillipeds of gravid females also bear posteriorly-directed, oostegite-like, often setose luppets. The function of these lappets is not known, but they may function a§ an ogstegite (to close the anterior region of the marsupium), or they may drive a water current through the marsupium, Several wuthors have suggested that the poste- rior cervical groove (fossa occiptalis) on the head of some isopods represents the incomplete line of fusion between the cephalon and first thoracomere. However, these lateral or complete grooves occur sporadically t many distantly related genera (Mesamphisopus, Idotea, Ligia, some Sphacromatidae, ete.) in many suborders, thus rendering this character unsuitable for phy- logenetic analysis a] higher taxonomic levels. Character 37 is; left and right maxillipeds fused together; this condition occurs only in amphipods and some tanaidaceans (not primi- tively, however). Character 38 is: coxae of max- ilipeds fused to heads this derived condition oceurs only in the Anthuridea. Character 39 is: maxillipedal endite without coupling setae (0) vs. with coupling setae (1). Mysidaceans lack coupling setae, but they occur in at least some miclaceans. tanaidaceans, and isopods, Because the character states of the mysidaceans and the amphipods may not be homologous, this charac- ter Was left unordered in initial analyses, Char- acter 41 is; maxilliped with 2-3 endites (0) vs 1 endite only (1). Amphipods have 2 maxillipedal endiles (one on the basis and one on the ischium), mysidaceans have 0-3 endites, and all other taxa in the analysis have one endife (on the basis), Character 42 is: maxilliped biramous; in this analysis, only the mysidaceans have a biramous maxilliped (0), all other taxa have a uniramious maxilliped (1). Character 44 Is: maxillipedal basis elongated and waisted (medially nar- rowed): this feature occurs only in the Lyn- sciidae and Limnoritdae, PerrorupAL Coxae Tn many isopods and amphipods, the coxae of the pereopods are expanded laterally into flat- tened lamellar structures called coxal plates. We define lateral coxal plates as ventrolateral expan- sions of the pereopodal coxae that extend freely (as ‘plates') to overhang the coxa-basis hinge of the leg. Within the Crustacea, such lateral coxal plates occur only. among the isopods and amphi- puss, 172 In gammaridean amphipods. the presence of well-developed lateral coxal plates is generally viewed as the primitive condition, although this has not been demonstrated by any rigorous phy- logenctic analysis of the Amphipoda as a whale. Coxal plates are lacking only in relatively specialized amphipod groups, such as the tube- building Corophioidea, the vermiform and inter- stitial Ingolfiellidae, the pelagie Hyperiidae, and the aberrant Caprellidae, In these groups, (he coxae form simple rings around the bases of the pereapods. The lateral coxal plates of gam- maridean amphipods are generally large and not fused lo their respective pereonal tergites, they can usually be dissected free from the body with the leg, The lateral coxal plates of isopods are gener- ally fused dorsally and ventrally to their respec- tive tergites, although on pereanites 2-7 (and occasionally pereonjte 1) the line of dorsal fu- sion is usually demarcated. They are often quite large (flabelliferans, most valviteruns, Tylomor- pha), although in some they may be smal) (sume Valvifera). In some isopod groups — Valvifera, Anthuridea, Calabozuidea, Serolidae, and soime Epicaridea and Oniscidea (in Porcellio, but probably not in Ligia) — the coxac also expand inward over the sternum. These sternal coxal plates have rarely been figured or discussed (Sheppard, 1957), and they may be absent in females bearing oosiegiles. Sternal coxal plates are clearly absent in many taxa, in both males and females (Phreatoicidea, Ascllota, Plakar- thriidac, Phoratopodida¢). Duc to uncertainty regarding the accurate taxonomic distribution and nature of the sternal coxal expansions, we were unable to incorporate this feature into the data set, However, Utis anatomical feature clearly holds great potential as a source of im- portant data on isopud relationships, and bears further investigation. I, may eventually be shown that sternal coxal plates co-cvolved with lateral coxal plates, bul were subsequently lost in some families. The various conditions of isopod coxac are summarized below, In the Anthuridea, the coxae are extremely clongated and fused almost tndistinguishably with their respective somites; this is perhaps an adaptation to the elongate body form and tube- dwelling lifestyle of anthurideans, They may be well-defined ventrally, but at most are demar- cated dorsally only by a faint line. Strictly speak- ing, because anthundeans do not have lures coxul plates that hang free to cover (heit coxa- basis articulations. by the above definition they MEMOIRS OF THE QUEENSLAND MUSEUM do not have true lateral coxal plates. However. the reduction and fusion of the coxae with the body wall is taken to be a derived state of *coxal plates present’ and thus this group is scared as possessing lateral coxal plates. In many an- thuridean species, {he coxae are expanded as sternal coxal plates and appear to be fused along the ventral midline such that there is no clear distinction between the sternite and the coxa. In the Asellota, Microcerberides, and Phrea- toicidea the coxae may be small or expanded (see. Figs. 1,2, and 9), but they usually have well-de- fined, though largely immovable, articulations with their respective pereoniles (at least on some somites), Although they may be expanded ante- riorly or posteriorly along the edges of their respective somites, they never extend ven- trolaterally as free lamellar plates overhanging the coxa-basis articulation (noteven the enlarged first pair of coxae in the asellote Stenerrium hang ventrally to cover the coxa-basis articulation) (Schultz, 1978; Wilson, 1980a). Thus we do not regard these three groups as having lateral coxal plates. In species of Asellota and Phreatoicidea with small coxae, distinet lergal epimeres, lap- pets, or spines may be present, Inthe Calabozvidea, the lateral coxal plates are large, (hough indistinguishubly fused dorsally to their respective pereanites (Van Licshout, 1983; pers, obs.). The lateral coxal plates of unis- cideans are alse large, and sometimes dorsal sutures are Visible, as in the Tylidae. In the Epicaridea, lateral coxal plates are pre- sent in females, but are highly Variable in size, ranging from very small and often unrecognis- able posteriorly (in Bopyrinae) to large and prominent (in Orbianinae and loninge), Sterna! coxal plates appear to be present at least in the Bopyridac, In the flabelliferan families, large lateral coxal plates are typically presenton all pereonites (Fig. 3). Usually they are indistinguishably fused ta the first perconite (or largely so), but more clearly defined by so-called ‘sulure lines” on pereoniles 2-7. In 4 families (Serolidae, Plakar- thriidac, Keuphyliidac, and Bathynataliidac) al) of the lateral coxal plates are enurmously ex- panded, and coxae 2-6 or 2-7 [reely articulale with their respective perconites, including those of the first perconite (Wilson ef al, 1976, Kens ley. 1978; Bruce, 1980, pers, abs.j. In Sorolidae the degree of free articulation ts minimal, tut a clear articulatory sulure is presenl and move- ment of the coxal plate results in movement of the ventral coxal region on the sternum. In the PHYLOGENETIC ANALYSIS OF THE ISQPODA 7 a FIG, 9. Lateral views of a flabelliferan and two phreatoicideans, illustrating development of the pereopodal coxae, A. Rocinela propedialis (type, USNM 29248). B, Phrealoicopsis terricola (USNM 78431), C, Phreatoicus australis (USNM 59116; anterior is fo the right). Phoratopodidae (which is monospecific and known from only two female specimens) the coxal plates are enormously expanded ventrolal- erally, clearly marked off from their respective pereonite, but yet they are nat freely articulating (Hale, 1925; Bruce, 1981, pers. obs.). Character 43 is: without Jateral coxal plates (0), vs with lateral coxal plates (1). Character 85 is: lateral coxal plates, if present. not fused with their respective pereonites (Plakarthriidae. Keuphylitdae, and Bathynataliidae are score 1; Serolidae is scored *?’), PEREOPODAL Eripops Character 45 is: with lateral epipods on per- eopods (mysidaceans) (0) vs without lateral epipods on percopods (mictaceans, tan- aidaceans, amphipods, isopods) (1). Character 46 is; pereapods without medial epipods on per- eopods (0) vs, with medial epipods on pereopods (1). Only the Amphipoda have medial epipodal gills arising from the coxae. In the gam- marideans, these are usually paired, thin-walled, leaf-shaped, tespiratary structures that are pre- sent on pereopods 2-7 (although they may be absent from 2 or 7). They may be stalked, foliate, 173 or dendritic, and they are particularly large and convoluted in terrestrial species, presumably ta compensate for loss of respiratory body surface area where the general body cuticle is hardened and waxy to prevent water loss. Insome brackish and fresh-water amphipods, finger-like acces- sory gills and sternal gills may also occur (fresh- water Gammaridae, Crangonycidae, Hyalellidae and Pontoporeiinae). Whether the medial epipo- dal gills of amphipods are homologous to the lateral epipodal gills of mysidaceans and other Malacostraca, or are uniquely derived in am- phipods, is not known. OoSTEGITES Although many tsopods have oostegites on the first five pairs of percopods, the number and placement actually varies considerably within any given suborder, and even within a family (and occasionally within a single genus, e.g. Sphaeroma). In some groups (Tylomorpha, Aegidae. Cymothoidae, many Epicaridea) oostegiles may form on all 7 pairs of pereopods, whereas in same genera of Arcturidae (Val- vifera) only a single pair of oostegites ever develops (on pereopods 4). The Asellota and the Phreatoicidea almost always have oostegites on pereapods !—4, and sometimes on the maxil- lipeds as well, The anthurideans usually have 3 or 4 pairs of onstegites. Other isopods are much more variable. In gammaridean amphipods, marginally setose oostegites usually occur on the coxae of percopods 2-5. In Mictacea, the mar- supium is formed by oostegites that may be marginally sctose and occur on the coxae of peteopods 2-6 (Hirsutia), or not sctose and occur on pereopods 1-5 (Mictocaris). Among, isopods, some groups have marginal setae on the oostegites and others lack setae. Oostegites are reduced or lost in many unre- lated isopod groups that have evolved alternative or aceessary means of incubating the embryos. For example, the evolution of sternal pockets or folds for incubating embryos is often correlated with the habit of conglobation, or folding the body ventrally so that the cephalon and pleotel- son are appressed. Harrison (1984a, b, c) pro- vides an excellent overview of brood pouch morphology in the family Sphaeromatidae, illus- trating the usefulness of these features at the generic level. Some sphaeromatids have the brood pouch composed only of oostegites. Other genera have a brood pouch composed of large, opposing. sternal pockets formed of cuticular folds; these may extend from the posterior mar- einal the slernum and open anteriorly (posterior pockets}, or they may extend from the anterior sternal region to open posteriorly (anterior pock- ets). In still other sphacromatid genera, paired invaginations of the sternal cuticle occur that extend into the body cavity but open via narrow slits (referred to us ‘internal pouches’). Internal pockets and pouches occur in sphacromatid genera thal conglobate (or fold) and have re- duced or lost the oastegites. In some cases, the oostegites are entirely lost (Dynamenella), and in other cases they are rudimentary (many spe- cies of Sphaeroma). All plant-and wood-boring species of Spiaeroma seem to show reduction of the oostegites; ron-boring species have all the oostegites fully formed, presumably working in concent with the internal pockets to form the marsupium. In the cirolanid genus Excirolana, there are 3 pairs of greatly reduced oostegites, but these do not form a marsupium. Instead, the eggs drop from the oviducis into a pair of sacs (‘uteri’) formed by a single layer of cells and located in the thorax Lateral to the gut. These sacs have been viewed as enlarged oviducts (Klapow, 1970, 1972; Jones. 1983). The embryos are brooded here, and since the sacs do not open to the outside during deyelopment this may be vicwed as a form of ovoviviparily, In the cirolanid penus Evryadice there are 5 pairs of oostegites, but in addition the sternum ts displaced dorsally cither side of the nerve cord, with the marsupium and developing embryos filling the entire pereon, surrounding the gut. Klapow (1970) suggested that the brooding modifications in Excirolana and Evrpdice are related to the habitats in which most species occur — wave washed sand beaches. Harrison (1984a, b,c) suggested similar correlations in certain sand beach sphacromalids that have large sternal brood pockets (Tholo- zodium, Sphaeromopsis, Dynamenella, Ancinus, Leptosphaeroma, Paradella). Ligiamorphans belonging to the conglobating genera Armadillo and Armadillidiwm have a brood pouch composed of onstegites, but in ad- dition the sternum bears 5 puirs of invaginations which surround the gut within the body cavity for brooding the embryos. The brood pouch in the conglobating genus Helleria is also cum- posed of oostegites, but the posterior wall of the marsupium extends into the pleon as a large pouch (Mead, 1963; Mead and Gabouriaut. 1988). In the conglobating genus 7ylas, portions of the sternites of ovigerous females are dis- placed dorsally and pressed against the dorsal MEMOIKS OF THE QUEENSLAND MUSEUM culicle, and the developing embryos fill the body. Ooslegiles appear to be absent altogether in the Microcerberidea, and sternal invaginations or folds are also apparently absent, although the female has been described for only a single spe- cies (Wagele, 1982a, b). Wagele speculated that the embryos of microcerberids might be laid free among sand grains — a behaviour currently un- known in any isopod species, However, since all peracarids undergo direct development, and many isopods rely on internal brooding, it would seem more likely that the embryos of microcer- berids Would also be brooded internally, in uteri or the general body cavity. In the parasitic cpicaridean family Cryptonis- cidae, the embryos are brooded in sternal invagi- nations formed by ventrolateral folds of the body wall, whereas in the family Dajidae the brood pouch is formed from ventral extensions of the sternites. Gnathiids lack oastegites altogether and brood the ernbryos within the body cavity. Klapow (1970) claimed that the fertilised ova develop within the ovaries themselves in Parag- nathia, At least some amphipods are also known to utilise internal brood chambers ( Cystosoma). As seen ftom the above review, aspects of oostegite morphology may be useful within families and genera, but no clear patiern of oostegite morphology is discernible al the level of isopod suborders (except perhaps for the Phreatoicidea, the Asellota, and the Microcer- beridea), and therefore oostegite characters were not included in the data analysis. SPFRMATHECAL Duct Wilson (1986b) summarised and claborated upon our knowledge of a unique vagina-like anterodorsal copulatory structure, the ‘sper- mathecal duct’ (or less descriptively, the “cutic- ular organ’) that occurs in female Asellota. Although all other isopod suborders have not yet been systematically surveyed for this structure, preliminary studies have so-far failed to reveal ils presence in any other groups, Character 47 is presence of the asellote ‘cuticular organ’ or sper- mathecul duct (Wilson, 1986b; Wilson, 1991). Only the Asellota is scored derived for this char- acter. Gesirac Pores information on isopod genitalia has been te- cently summarised (Wilsan, 1991). Important pattems are apparent inthe position of the genital pores. In the Malacostraca, genital pores. typi- PHYLOGENETIC ANALYSIS OF THE ISOPODA cally occur on the coxae of thoracopod 6 in females, and thoracopod & in males. These are relatively conservative features, although the peracarids show some variation. The Phreatoicidea are the only isopods with both female and male pores located on the coxae, In male phreatoicids, the gemiti! papillae (penes) oecur on the medial side of coxae 7 and can be quite large; they are likely to be the primary intromittent organs in this group. In all other isopod suborders, the penes are located on the sternum, usually near the posterior margin of the sternite of thoracomere &, rather than on the coxac. A single, notable, and important excep- tion to this occurs in the asellote genus Ver- mectias Sivertsen and Holthuis, 1980 in which the coxae of the seventh pereopods appear to be divided into 2 pieces, one of which ts slightly expanded medially onto the sternum and bears the penes upon it (Just and Poore, pers. comm.). Within the Ascllota, and the Isopoda in general, the penes show a trend toward migration medi- ally, often with fusion at the midline. Fusion of the penes oceurs throughout the Isopoda and this feature has probably evolved independently in several suborders (Wilson, in press) making itof little use for the present study, The coxae/penes condition noted above in Vermectias may repre- sent an carly evolutionary stage in the migration of the penes fram the coxae to the sternum, and perhaps also an carly stage in the evolution of sternal coxal plates upon which the penes may be borne. In two suborders (Valvifera and Onis- cidea) the penes arise from the sternumof pleom- ere 1, ot from the articulating membrane between pleomere | and perconite 7, Among the non-isopod Peracarida, a variable pattern also exists. The Mysidacea and the Mictacea have coxal openings for the vas deferens, Whereas [he Amphipoda and Tanaidacea have penes on the eighth thoracosternite. In most female isopods and tanaidaceans, the oopore is situated ventrally on the sternite of pereonite 5. In the phreatoicids. however, the pore is clearly present on the medial side of the coxa. Coxal oopores also are found in the My- sidacea, Amphipoda, and perhaps the Mictacea {although our inspection of non-ovigerous female Mictocaris failed to reveal any oopores, either sternal or coxal). The situation of the oo- pore is more complicated in those isopod groups where the coxae ure expanded as sternal coxal plates covering the ventral surface. Available data do not allow us to assess whether the oa- pores simply moved medially with the coxae, or whether they first migrated onto the sternite and then subsequently penetrated the coxac when the pores were covered by the expanding coxal plates. Further, (he precise position of the oopore is unknown for many groups. Character 48 is: male penes on coxae (0) vs penes on sternite (1), Character 49 is: penes on thoracomere & (0) vs penes on pleomere 1, oron the articulaling mem- brane between pleomere | and thoracomere & (1). Only Valvifera, Ligiammorpha, Tylomorpha, and Calabozoidea are scored apomorphic for character 49. ExcreTory ORGans The primary excretory organs among the Malacostraca are antennal glands and maxillary glands. All crustaceans have antennul glands during their ontogeny, but many lose them in adulthood and instead rely on maxillary glands as the primary exeretory organs. Adult isopods, lanaiduceans, and cumaceans lack antennal glands, of possess only a rudimentary antennal gland, and the maxillary gland is well developed (Stromberg, 1972), Conversely, adult: my- sidaccans and amphipods (and the Eucarida} have well-developed antennal glands, Siewing (1952, 1953, 1956) noted that in at least some lophogastrid mysids (Eucopia) small tunctional maxillary glands may also be present, thus possibly reflecting an ancestral condition in Which both pairs of segmental nephridia were funcijonal in adults. The condition in Mictacea is not known. Schram and Lewis (1989) have suppesied thal a series of Segmental glands ey have primitively been present, one pair in eac crustacean head somite, Character 52 is: primary adult excretory organ antennal gland (0) vs max- illary gland (1); no polarity is assumed. Prhborons The pleopods of isopods have multiple func- tions, including respiration, swimming, and copulation. Two key synapomorphics uniquely defining the Tsopoda are; Character 4, thoraco- abdominal heart, and Character 5, respiratory pleopods, These fealures are obviously function- ally/anatomically linked. The only other mala- costracans known to utilise the pleopods as the principal respiratory organs are the stomatopods (Burnet and Hessler, 1973; Kunze, 1981), in which the heart also extends into the pleon. The primitive malacostracan pleopod is a mar- row biramous limb with multiarticulate rami- This type of pleopod is found in the Mysidacea and the Amphipoda. Broad, flat pleapods with 176 MEMOIRS OF THE QUEENSLAND MUSEUM PHYLOGENETIC ANALYSIS OF THE ISOPODA 177 TABLE 2. Comparison of basally derived Isupoda (*short-lailed’ taxa). Legend: M = mate: F = female. Phreatoicidea not reduced free tree, short & narrow Asellota fused {to vanously free, not short ting-like icrocerberidea a no more than two segments in the rami are found in the Mictacea, Tanaidacea, and the Isopoda. Character 53 is: narrow, multisegmented pleopodal rami (0) vs broad, flat, 1- or 2-articu- late pleopodal rami (1). In phreatoicideans and many asellotes, especially primitive Asellota ( Aselloidea, Stenetrioidea), the posterior pleopods bear 2-segmented exopods. In all other isopods the pleopodal exopods are always uniar- liculate, although they may occasionally bear Iransverse ‘suture lines’. Character 77 is: ex- opods of at least posterior pleapods biarticulate (0), vs no pleopods with biarticulate exopods (1). In all non-isopod peracarids (except Mic- tacea), pleopods are primitively used for swim- ming. The pleopods of isopods are also well-developed for this function in most groups. with broad rami and swimming setae on at least some pairs. Several groups (Asellota, Microcer- beridea, adult Epicaridea, Ligiamorpha. Tylo- morpha, adult Cymothoidac) no longer swim with their pleopods, and use them only for respi- ration. Calabozoidea are said ta swim (Van Lie- shout, 1983:175), although behavioural observations may have not been made, In the groups that do swim, a trend occurs in most suborders wherein the posterior pleopods may be naked (with reduced or no marginal setae) and | Reductionof | Fusimof | Condition of Pereapodal pleomeres I—2 | pleameres 3-5 pleapod | pleopod 2 leapod 3 coxge | es seam | F, biramous biramous free M_ uniramous F, absent M,uniramous | M, biramous fused F. absent E, sbsenit uniramous free M, unitramous | M, biramaus | oritamous | Atlantasellidae free, broad fused FE. abserit Fv absent uniramious free M. biramous fused dorsally; strongly M. hiramous i Calabozoidea reduced free (ni iv eniles) Fhitamnite biramous with sternal biramous plates Ditistidéa somewhal M. biramous M, biramous reduced VP biramous F, biramaus. M . biramous (endapod penton | uniramous biramous free fused dorsally; hiramous wilh sternal plates serve primarily for respiration. Loss of marginal setae typically occurs on pleopods 3-5, or 4-5, or just 5, and it may occur on both rami or unly on the endopods. In the family Cymothoidae, the mancas and juveniles have swimming setat on the pleopods, but the obligate parasitic adults do not. The Asellota and Microcerberidea share a number of pleopodal features. In both of these suborders females lack the first pair of pleopods (character 78), and in males the first pleapods (if present) are uniramous (character 81), The first pleopods of males are fused together to assist the second pleopods in sperm transfer in the higher Ascllota. In addition, the male second pleopodal exopod is a small, non-lamellar structure, whereas the endapod is modified as a copulatory gonopod (character 79). Female microcerberids also lack pleopods on the second pleonite (char- acter 82), and the third pleopods are uniramous and fused into a single piece to form an oper- culum over pleopods 4 and 5 (character 83). In male microcerberids, the second pleopodal ex- opod is reduced to a simple [- or 2-articulate ramus. probably not involved in sperm transfer; the endopod is complex and highly variable in shape, but never geniculate (character 84). In the Asellota, females have uniramous second pleo- FIG. 10. Comparison of male pleopods | and 2 in calubozoans, asellotans, and oniscideans. A, Calabozoa (Calabozoidea), penes and pleopods 1-2 in situ (ventral view). B, Culabozoa (Calabozoideu), lelt pleopod 1 (dorsal view). C, Armadillidiam (Oniscidew), penes and right pleopod | in situ (dorsal view). D, Asellus (Asellota), right pleopod 1 (ventral view). E, Calabozaa. left Pleapod 2 (ventral view). F, Asellus, night pleopod 2 (ventral view). G, Armadillidium, tight pleopod 2 (ventral View). 78 pods (character 75), and males Have the exopod of the second pleopod highly modified to func- tion in concert with a large geniculate endopod in Sperm transfer (character 76), Terrestrial pleopodal respiration by use of pseudotracheae is found only in the Tylomorpha and Ligiamorpha, though not in all families (nat Ligiidae or Trichoniscidae). In addition, the Oniscidea and the Calabozoidea share several unique pleopadal similarities (Table 2, Fig. 10), The endopods of male pleopods | and 2 are styliform and greatly elongated {only pleopod 2 in Ligiidac), presumably participating in capula- tion and/or sperm transfer (character 54), And, on pleopods 3-3 (in both sexes) the exopods are broad, heavily chitinised. and opercular, while the endopods are thick and tumescent (character 36). In most tsopods, the endopods are [hin walled and neatly the same size as the exopods, In the recently described family Lynseiidae (Poore, 1987) (he fifth pleopads are reduced loa single plate (character 70), Poore suggested thal this alirtbate was the only unique apomorphy of this family, and we agree. OTHER PLEONAL FEATURES Most malacostracans have 3 free more-or-less equal pleonites, and primitively the 6th pleonite is free from the telson and pleomere 5S, In the Microcerberidea and the Asellota, pleonites | and 2 are completely free and (he remaining pleanites and telson are fused into a single unit with no lateral incisions indicating the fused somites. (The single exception to this appears to be the odd asellote Vermeciias, which has 3 free pleomeres; Just and Poore, pers, comm.), A somewhat similar condition appears to be the primitive state for the Sphacromatidae, but this is presumably a convergence, In sphaeromatids, the primitive condition exhibits lateral incisions demarcating the vestiges of the fused pleomeres, hence we do not regard this ta be a condition homologous to that of asellotans. Some authars huve suggested a close affinity between the Serolidae and certain Sphacromatidae (Ancinus, Tecticeps, Bathycapea) on the lasis of a similar pleonite reduction (Hansen, 190Su; Sheppard. 1933), However, in serolids pleonites 4-5 ure fused to the telson and pleonite | is reduecd, whereas in sphaeromatids pleonites 36 (al least) are Fused with the telson, lateral incision tines primitively demarcate the positions of the fused pleomeres, and the first pleonite is never markedly reduced, Other isopods have vanously modified pleonites, but no other suborders or MEMOIRS OF [HE QUEENSLAND MUSEUM families show a pleonile reduction fike that seen inthe Asellota and Microcerberidea as the primi- tive condition. Character 80 is pleonites 1-5 either free or variously fused, but never (in (he primitive con- dition) with pleonites 1-2 free and 3-5 fused to the pleotelson (0), vs pleonites 1-2 free and the remaining pleonites and telson fused into single integrated unit (1). The varicty of pleonite reduc- tions seen throughout the isopods make it diffi- cult to find further useful homologies. In two taxa, Phreutoicidea and Limnoriidac, pleonite 5 is alWays manifestly longer than all other pleonites (character 73). In the Calabozvidea, pleomeres | and 2 are reduced to only the sternal plates (character 86), Within the Malacostraca, broad fan-like uropous arising [rom the sixth pleomere and functionally associated with the telson is the plesiomorphic state. This ‘tailfan’ arrangement is an integral aspect of Calman’s caridoid facies (Hessler, 1983), Unlike other Eumalacostraca, the Isopoda (and some other Peracarida) show a good deal of variation in uropod morphology and position (Figs 1-3) and the uropods function in avaricty of ways. The caridoid-like tailfan of the Cirolanidac and related families has been taken by many workers.as evidence thal these taxa are primitive isopods, or at least that they represent an archtypical “caridoid’ isopod body plan. However, isopods (like amphipods, tanaids, and perhaps mictaceans) lack the ‘caridoid escape behavior’, and those groups with fan-ijike uropods do not use their flattened uropods for propulsion, as in true earidoids (e.g. my- sidaceans, cuphausiids, or natantians). Instead, they appear to use their uropods as lift planes and steering devices (unpubl, obs, of living Bathy- nomus, Cirolana, and other flabelliferans), A review of the peracarid orders reveals a clear trend toward reduction of the caridoid tailfan morphology, Although it is well-developed among the Mysidacea, the telson and uropods of speleogriphaceans, mictaceans and ther- mosbacnaceans is less well developed as a true tailfan. This is presumably tied to loss of the ‘caridoid escape behaviour’ in these groups. However, in these three groups the flattened, paddle-like shape of the uropods is retained and these appendages probably assist | swimming in some way. In Cumaceans, tandids, amphipods, and many isopod taxa there is noting resem- bling a caridoid tailfan In amphipods pleopods 4, 5 and 6 are modified as 3 pairs of uropods (Character fi), The amphi- PHYLOGENETIC ANALYSIS OF THE ISOPODA FIG. 11. Keuphylia(Keuphyliidae). Ventral view of pleorelson showing arrangement of urapuds in ventral pocket. pod urosome and uropods appear to be used primarily for strengthening the caudal portion of the body, and to permit jumping by rapid poste- nor flexion of the pleon (Barnard, 1969; Bous- field, 1973). In many Gammaridea, however, the third uropods still bear ‘swimming’ setae and may be used (along with the first two pairs) for paddling; males especially tend to have natatory (third uropods (Barnard, 1969: Bousfield, 1973). However, the amphipod third uropod is usually substyliform and not fan-like. The majority of Gammaridea probably do not use the third uropads for active swimming and thesc struc- tures are often reduced or occasionally absent in sedentary groups. The uropodal exopad in am- phipods is biarticulate, and the endopod is typi- cally uniarticulate. In tanaidaceans, amphipods, cumaceans, and many isopods, the uropodal rami are styliform. The uropodal rami of tanaidaceans also are long. multiarticulate appendages, whereas in isopods, the rami are always short and uniarticulate. The mictacean uropodal rami can be either biarticu- late (Mictocaris) or multiarticulate (Hirsulsa), In mictaceans, amphipods, and mysidaceuns, the uropods arise from pleomere 6 and the telson isa distinct somite. In isopods and living tanaids, the sixth pleomerc is fused with the telson, form- ing a ‘pleotelson’, although primitive fossil tan- aids (see below) possessed [ree sixth pleomeres, Many isopods have a well developed, elongate telsonic region of the pleotelson upon which the anus and uropods are basally positioned. Other isopods have a reduced, shortened telsonic re- gion of the pleotelson, and the anus and uropods 179 are positioned in the posterior region of the pleotelson (terminal or subterminal). The uropods always arisc on cither side of the anus. Dahl (1954) suggested that the primitive Phreatoicidean condition was flabelliferan-like (‘cirolanoid’-like), unlike the adult morphology of living Phreatoicidea. This argument was based on observalions made on developmental Stages taken from the brood pouch of the South African phreatoicid Mesamphisopus capensis. We do not find Dahl's argument (or his illustra- ions) Convincing, The kinds cf morphological changes he described can be easily cvolained by natural developmental allometry coic:monly s¢en in most crustaceans. Brenton Knott (pecs, comm.) has seen no evidence of lamellar uropods or other “cirolanoid' morphology inthe developmental stages of any Australian phrea- toicids. Character 57 is: uropods broad and flattened (0); urapods flattened but only somewhat broadened (1); uropads styliform (2). This char- acter was analysed unordered in initial analyses, Character 58 describes the shape of the pleotel- son, State “0” is: telsonic region of the pleotelsan well-developed and elongate, with the anus and uropods at the base of the pleotelson (at the position of pleomere 6) — this is the condition seen in mysidaceans, amphipods, mictaceans, and many isopods. State ‘1° is: lelsonic region very short, with the anus and uropods positioned terminally on the pleotelson; this condition oc- curs in the Tanaidaces, Phreatoicidea, Asellota, Calabozoidea, Microcerberidea, Tylomorpha, and Ligiamorpha. Because the polarity and pecise homology of these conditions is uncer- tain, character 58 was left unordered in initial analyses. A unique up-turned pleotelson apex occurs in the Phreatoicidea (character 72). In mysidaceans, mictaccans, tanaidaceans, and amphipods, the uropodal rami are composed of 2 or more articles; in all isopods they are uniarticulate. Character 59 is: uropodal rami may be multiarticulate (0), vs uropodal rami always uniarticulate (1). In three families (Keuphyliidae, Bathynataliidae, Plakarthnidac) the uropods arise not on the anteorlateral margin of the pleotelson, bul rather posterolaterally, where they lie in shallow ventral channels or furrows (character 55) (Fig. 11). In serolids there is also a tendency toward this feature, but itis not present in all species, hence they are scored ‘?" tor this character, Character 60 is: uropodal exopad folded dar- sally over pleotelson (a unique synapomorphy of Tall FIG. 12. Haliophasma geminata (Anthuridea), SEM of pleon (lateral view). Note deep Outing between pleomeres 5 and 6, and between and between pleomere 6 and telson. Despite fluting, a con- linuious cuticular covering connects these somites and no articular membranes are present, Also note large opercular first pleapods (compliments af B. Kensley). Anthuridea), Character 61 is: uropods modified as a pair of ventral opercula covering the entire pleopodal chamber (a unique synapomorphy for the Valvifera). Character 62 is: uropods form a ventral, operculate, anal chamber beneath pleotelson, covering the anus and distal-most pleotelson region but not covering the pleapods (a unique synapomorphy of the Tylomorpha). Character 63 is: uropods directed ventrally and identical to other pleopods (a unique synapomor- phy of the Anuropidae, and presumably an adap- tation to a swimming pelagic lifestyle), Character 67 is: urapodal endopad claw-like. We regard this as a unique synapomorphy of the Keuphyliidae. Although the uropodal endopod in Paralimnoria is acute, it is nol recurved und claw-like as in Keuphyliidae (and, the endopod of Limmoria is neither acute nor claw-like). Char- acter 68 is: uropodal exopod claw-like (a unique synapomorphy of the Limmnoriidae). Character 71 is: uropods highly modified and represented by a single, elongate, clavate piece, or by an MEMOIRS OF THE QUEENSLAND MUSEUM elongate, clavate peduncle with reduced rami — a unique apomorphy of the Bathynatalidae. Character 87 is: uropods of a single piece, rami fused to peduncle — a unique apomorphy of the Calabozoidea. Inall living tanaidaceans and isopods, the sixth pleomere is fused to the telson, forming a pleotelson. However, fossil Lanaids of the in- fraorder Anthracocaridomorpha have 6 free pleameres (and thus lack a pleotelson), and this is presumably the primitive condition for this group (Schram, 1974; Sieg, 1984: Schram eral., 1986). Some cumaceans and thermosbaenaceans also have a pleotelson. A pleotelson is present in all isopods. Many authors have alluded to a free telson in some genera of anthuridean isopods. The pre- sence of a free (unfused) sixth pleomere in some Anthuridea has been debated at least since Cal- man (1909). Wagele (1981, 19894) claimed that the sixth pleomere is always fused to the telson in anthurideans (thus a true pleotelson is always present). Bowman (1971) stated that the sixth pleomere was free in anthurideans, Kensley and Schotte (1989) stated, ‘Pleonites 1—5 free or fused, pleonite 6 partly or completely fused with telson’, In his diagnosis of Paranthura Poore (1984) stated, “Pleonites usually distinct from each other and fram telson,’ Poore and Lew Ton’s (1985a) diagnosis of Apanthura stated, ‘pleonite 6 free from others and from telson’, and their diagnosis of Cyathura (1985b) stated, ‘pleonite 6 free or fused to telson.’ However, Poore (pers. comm.) has most recently stated that he no jonger believes the sixth pleanite to ever be freely articulating with the telson in anthurideans, The sixth pleomere is clearly fused to the tel- son (forming a pleotelson) in many anthurideans (Pseudanthura), However, in many genera pleomere 6 appears to be free (Amakusanthura, Calathura, Exallanthura, Haliophasma, Heter- anthura, Leptanthura), In most species in these genera, under both light and scanning micro- scopy, pleomere 6 and the telson are clearly separated from one another dorsally by a deep groove (Poore and Lew Ton, 198&b, fig. 11a) and, using forceps, the telson can often be flexed against the sixth pleonite. This groove is often shown in drawings and electron micrographs of anthurideans (Fig. 12). Even in some species in which pleonites 1-4 are fused (medially or en- tirely). the sixth pleanite may appear free (Haltaphasma geminata). To resolve this Issue, we sectioned specimens 181 PHYLOGENETIC ANALYSIS OF THE ISOPODA qsny aRjnaiado ase] a10U osyy YIM g asawioayd jo uoIsny pue “uos]a] puke alawoayd ayeoipul smoly “spodoajd ‘juasaid aly SOUPIqWUOW Je]NdWIe OU PUR Sa} WOS say) s}aauUOD SuUaA0D JE]NIIWND snonuUOD B “Bunny aydsoq ‘uos|a) . g pur ¢ sarawoajd yo uorsny Suimoys uoad ysnosy) uONsas jeyTeS uRIpayy “(RapUNy UY) suBdaja DanysuBADY *E] “Old 182 MEMOIRS OF THE QUEENSLAND MUSEUM 24(0), 78, 79, 80, 81 16, 35, 39(0), 49, 54, 56 17, 22 48, 74 43, 77 7, 30(2), 55, 85 50(1) 39(0) 18(1), 57(0), Sete) 30(2), 31(1), 35, 91 30(2), 40, 44, 50(2) 30(1) 50(3) 36 39(0), 65 PHREATOICIDEA ASELLOTA MICROCERBERIDEA CALABOZOIDEA TYLOMORPHA LIGIAMORPHA VALVIFERA SPHAEROMATIDAE BATHYNATALIIDAE KEUPHYLIIDAE PLAKARTHRIIDAE SEROLIDAE PHORATOPODIDAE EPICARIDEA GNATHIIDEA LIMNORIIDAE LYNSEIIDAE CIROLANIDAE ANTHURIDEA ANUROPIDAE PROTOGNATHIIDAE CORALLANIDAE TRIDENTELLIDAE AEGIDAE CYMOTHOIDAE FIG. 14. Cladogram of the Isopoda (Nelson strict consensus tree, built from 16 equal-length trees). Length = 133; C.I.=0.75. Character numbers on tree correspond to character list in Appendix I. Synapomorphies of terminal taxa are not shown on tree (see Appendix III). of Paranthura elegans aspecies commonin San show unequivocally that no articular membrane Diego Bay. Under SEM and light microscopy, is present between the telson and the sixth this species appears to possess a free sixth pleonite (Fig. 12). In fact, the cuticle is even pleomere. However, our longitudinal sections thicker in the region of fusion than it is elsewhere 183 PHYLOGENETIC ANALYSIS OF THE ISOPODA “(sajoRIe YO VANRWOJUIUN Surpnjoxa £9°()) 8L°0JOT'D & YIM “Buoy sdajs GZ] a1 Saad] Yiog “(soulds Surjdnos jnoyyM ‘sa YILM OPUd [epadi]]Ixeut) GE Jo}OBIRYD 19A0 (16 ‘YS ‘SE ‘OE—-LZ SsojoereYd) Somnjeay Ie|NGipurW aziseyduid $991) aSay], :Payonsysuod sem (py “SIy) 994] SNsuasuOd oY] YOIYA WO] $991) YISUaI-Jenba 9] IY) JO OM], “ST ‘OL AVGIOHLOWAD avdidav AVGOIN1SLNAGINL AVGINVT1IVHOO AVGIHLVNDOLOYd AVGIdOUNNY VAGIHNHINV AvdaidOdOLVHOHd AVGINVIOHUID AVGINASNA1 AVGNYONAIT VAdGIIHLYNS vadluvold3a avaiouw3ss AVGIYHLYVAVId AVdINAHdNay AVGIIVLIVNAHLVa AVGILVWOYAVHdS VUASIATVA VHdYOWVISIT VHdHOWOTAL vadlozoavivo VACIHASHADOHOIN vLo11asv VAGIOIOLVAYHd s9 ‘(o)6e (2)0S ‘pe ‘Ov 9€ (e)os (Loe 16 ‘se ‘(L)LE (o)6¢ x4 (Los (2)0€ 9S ‘pS ‘6y ‘(0)6e ‘se ‘OL Le ‘08 ‘62 ‘82 ‘(0)pz AVGIOHLOWAD Aavdidav Avda LNadidt AVGINVTIVYOOD AVGINHLYNSOLOUd AVGIdOYNNY VAGIHNHLINV 3vdidOdOLVYOHd AVGINV1OHIS AVQIASNA1 SVGINYONWIT VAGIHLYND VAdIHVOlds avaiouwas AVGNYHLYVAV 1d AVdINAHdNAy AVGINIVLIVNAHLVS AVGILVWOYSVHdS VYasIATVA VHdHOWVISIT VHdYOWOTAL vadlozogvivo VAGIHagYHS00OHOIN vLo1IaSY VAdIDIOLVAYHd s9 “(0)6€ 9€ (e)os (Loe (z)0¢ ‘py ‘ov ‘(z)o€ 6 ‘se ‘(i )Le ‘(zoe (o)6€ (Los se ‘ss ‘(z)oe ‘2 LL ‘ep 9 2% ‘Lb ‘6S 9S ‘pS ‘6p ‘(0)6e ‘se ‘OL . te ‘08 ‘62 ‘82 ‘(0)bz onthe pleon. Although specimens of Paranthura have some flexibility between these two seg- ments, this is apparently duc to the deep fluting of the cuticle at the area of fusion, and nol due to a true articular membrane. This fluting is what creates the deep dorsal groove that is sa visible in this, and presumably other, species, Hence, unless additional observations of other species indicate otherwise, we take the conservative ap- proach and assume that anthurideans also possess a pleotelson. Although fusion of pleomere 6 to the telson occurs in. some specics in at least four peracarid suborders (tanaids, cumaceans, ther- mosbaenacedns, isopeds), it appears to have been derived independently in three, if not all four, of these groups. Only in the Isopoda do all species possess a pleatelson, Character 64 is: pleamere 6 [reely articulating with telson (0); pleomere 6 always fused with telson. forming a pleotelsan (1), Only isopods are scored (1). RESULTS AND DISCUSSION ANALYs18 PROCEDURE Our analytical strategy was as [ollaws. We as- sembled « data set based on the character analyses described above, and input data files were generated for HENNIG&6, PAUP, and MacClade, ‘The data were tirst analysed with PAUP and HEN- NIG86. A pool of multiple, equal-length trees was studied and all homoplasous characters were re- assessed. Scveral characters were climinated from the analysis at this stage because they were simply too high in homoplasy and/or their precise homolo- gies seemed questionable, e.g, sternal coxal plates, The fina! character list (the numbered characters noted in the previous section) and OTU-character data matnx are provided in Appendices | and IL. Trees were first constructed with the charae- ters polarised as indicated in the descriptive character analysis above. However, it quickly became evident that, duc to high homoplasy levels (especially reversals) unambiguous judy- ments could nat be made regarding character slate transformations. Hence, the final analyses were done with all characters unpolarised, i.c. programs sel to nonaddilive, and allowed to change in any direction. This procedure makes no assumptions as to what the primitive or derived stales are for any characters in the dala sel, In respect for the high levels of homoplasy inherent in such a large cata set (especially for arthropods), comparisons of trees generated from ordered and unordered characters js an MEMOIRS OF THE QUBENSLAND MUSEUM informative and cautious approach. In fact, bi- nary characters are treated no differently in ad- ditive (ordered) vs nonadditive (unordered) analyses (unless such a program option js specifically selected); the only way in which the nonaddilive analysis differs from the additive one is in its effect on multistate characters, The nonadditive analysis counts any character state change equally, as a single step, ¢.g. for a multi- state character, a change from State 0 to state 2, or state 2 lo state U, is still counted as one step. The non-additive analysis using the branch swapping algorithm of HENNIGS86 (mhennig + bb) found 16 equally short trees (length = 129 steps; C.1. = 0.78). The Nelson strict consensus tree of these 16 trees js 133 steps long (C.L = (0).75).and is shown in Fig. 14. This tree could nat be improved by application of the successive charagier weighting method to the suite of 16 trees from which it was derived. These results were verified by analysing the data with PAUP 3.0. The PAUP analysis, using the MULPARS option, found the same 16 trees and produced an identical strict consensus tree. All statistics were identical for the PAUP and HENNIGS6 trees, Our final data set and consensus tree were coded into MacClade format, along with the trees of Wagele (1989a), Schmalfuss (1989), and others, MacClacde was used to examine the cf- fects on tree parsimony and character placement of different tree topologies generated by manual branch swapping, and to determine precisely how other trees differed from our own by graphi- cally tracing character state changes for cach character, Tur CLADOGRAM OF IsaPODs. Inthe following discussion, character numbers (see appendix 1) are indicated parenthetically in boldface. Synapomorphies defining terminal laXa ure not shown on the tree (Fig. 14), but are listed in Appendix UI and were noted in the previous section (character discussions). In our consensus tree (Fig. 14), the Phreatoicidea un- ambiguously arises as the basal most mode, re- taining two key symplesiomorphies that are lost in virtually all other isopod suborders: coxal penes (48) and the large row of filter setae on the medial margins of the maxillae (74). The notian that phreatoicids might represent an ancient isopod group was first advanced by Chilton (1883) and repeated by several other workers in the carly part of this century, However, the specific hypothesis that Phreatoicidea are the most primitive living isopods has apparently PHYLOGENETIC ANALYSIS OF THE ISOPODA been previously suggested only by Schram (1974), Synapomorphies defining the Phreatoi- cidea include the upturned pleotelson (72) and clongale fifth pleomere (73). The most parsi- monious tree depicts the Joss of the antennal scale (25) at the origin of the isopod line, with its reappearance in the Asellota. An alternative, bul Jess parsimonious scenario posits the Joss of the antennal scale three times — in the Phreatoi- cidea, the Microcerberidea, and above the usel- lote-line in the cladogram. The Asellota-Microcerberidea and Oniscidea- Calabozoidea lines arise next. The asellotans and mictocerberids are sister groups. Among other things, they share the interesting attribute of a 6-articulate antennal peduncle (24), a feature that also occurs in mysidaceans, but is not seen in amphipods, mictaceans, tanuids, of any other isopod group, They also share the following additional syn SPOR PRIS: femules lack first pair of pleopods (78); male second pleopods with a small non-lamellar exopod and a large endopod modified into. a complex gonopod (79); pleomeres | and 2 free, 3-5 fused to pleotelson (80); and, male pleopod 1, if present, uniramous (fused and working with the second pleopads in sperm transfer in the higher Asellota) (81). All isopod taxa beyand the Asellota-Microcer- beridea line are distinguished by the presence of lateral coxal plates (43) and the absence of 2-ar- liculate exopods on all pleopods (77), The Ligi- amorpha and Tylomorpha are sister groups, supporting the contention that the Oniscidea is a monophyletic clade. The Calabozoidea is the sister group of the Oniseidea. (These three taxa ure united by at least six synapomorphies: char- acters 1, 35,49, 54, 56, and 39-reversal). All isopod taxa above the oniscidean line arc distinguished by three unique features: per- sopods 1-3 are directed anteriorly, and per eopods 4—7 are directed posteriorly (18); the telsonic region of the pleon is greatly elongated, positioning the anus and uropod articulation anteriorly on the pleotelson (56); and, the uropods are broad and flat (not styliform) (57), We refer to these taxa as the ‘long-tuiled’ isopods, The relationships of the long-tailed jsopod taxa cannot be unambiguously resolved with our data set. They comprise an unresolved 8-way poly- tomy on the consensus tree. Each of these § lines represents a distinct clade that appeared in all 16 primary trees. These & clades are: (1) Valvifers; (2) Sphacromatidac, (3) Phorutopodidae; (4) Cirolamdae; (5) Epicarides-Gnathiidea; (6) igs Limnoriidae-Lynsciidaec; (7) a clade of 4 flat- bodied families (Bathnataliiduc, Keuphyliidac, Plakarthriidae, and Serolidae); and, (8) a clade of 7 predacious-parasitic taxa, including the An- thuridea and 6 families currently recognised as Nabelhferans, The latter clade culminates in the Cymothoidae, hence we refer to this group as the “Cymothoid-line’, Greater resolution of the long-tailed clade ex- ists, Of course, in each of the 16 primary trees. These 16 trees differed little from one another, and only in regard to subtle rearrangements of the 8 long-tailed lines noted above, If preference is given to mandibular chatacters (characters 27-30, 35, 50) over those of the maxillipedal coupling spines (character 39), much more reso- lution is achieved. Figure 15 shows two such irees, In these two trees the Valvifera and Sphaeromiatidae are at the base of the long-tailed line. Of the long-tailed taxa, only these two groups retain the primitive grinding mandibular molar process (character 30); all taxa above Val- vifera and Sphaeromatidac have a blade-like slicing molar process (or the molar process is lost), According to our analysis, the ancestral isopod morphology ineluded a very short telsonic te- gion on the pleotelson, positioning the anus and styliform uropods terminally orsubterminally on the pleotelson. We refer to the groups that possess this shortened pleatelsonic morphology as the ‘shaort-tailed’ isopods (Phreatoicidea, Asellota, Microcerberidea, Oniscidea, and Cala- bozoidea), This condition also oecurs in extant tanaidaceans, although this could represen! a parallelism because some fossil tanaidaceans are known lo possess elongate telsons (Schram et al., 1986). These short-tailed forms are largely infaunal and are not strong swimmers. Most are herbivores or scavengers. The shift away from the short-tailed mor- phology to the long-tailed morphology (elongate telsoni¢ region, positioning the anus and uropods basally on the pleotelson) occurred subsequent to the appearance of the oniscidean line, This reversion to a broad mysid-like tailfan within the Isopoda (characters 57 and 58 on the trees) ap- pears to have corresponded to the emergence of isopods as active swimmers inthe Water column, However_as we noted earlier, isopods (and other non-mysidacean peracarids) lack the caridotd ‘escape behaviour’ and do not possess the mas- sive pleanal musculature seen in the true caridoid jaya, Thus, (he main effect of “re-inven- tion’ Of & lailfan in swimming isopods was not 186 for direct propulsion, but more likely to provide a planar surface or rudder during swimming. We have observed this apparent function in swim- ming Bathynomus, Cirolana, juvenile Cy- mothoidae, and others. Within the long-tailed line, a trend can also be seen for enlargement of the lateral coxal plates. This may serve to in- crease the hydrodynamic streamlining of the body, perhaps in the same fashion as the enlarged pleura on many swimming caridoid malacostra- cans. Furthermore, as Hessler (1982) has noted, enlarged lateral coxal plates were impractical in the Asellota (and Phreatoicidea) because the coxae are still mobile in these groups. Also within the long-tailed line is a trend away from primary herbivory (Valvifera) and scavenging (Sphaeromatidae), to active predation and even- tually parasitism. Within this lineage, only the Valvifera and Sphaeromatidae retain the primi- tive grinding mandibular molar process — all other taxa have a mandible modified more for carnivory, with the molar process (when present) modified as a slicing bladelike structure. Hence, emergence from the benthos appears to have been correlated with the evolution of a more active swimming lifestyle and carnivorous hab- its. Corroborating evidence for this cladogram comes in the form of embryological and ana- tomical data from other studies. According to Wiagele (1989a) the stomachs of phreatoicids and asellotans are the most primitive of the Isopoda, i.e. with straight, rather than curved, anterior filter channels. In addition, Strémberg (1972) has shown that the embryological median dorsal organs of isopods are of two types, one of which occurs in the Oniscidea, the other being restricted to the long-tailed taxa. Stromberg (1972) also demonstrated that the paired embry- ological lateral (= dorsolateral) organs of isopods are also of two types, one type in Val- vifera, Flabellifera, and Anthuridea, the second type occurring only in Phreatoicidea and Asel- lota. Furthermore, Hessler (1982) observed that, of the isopods he studied, only the phreatoicids and the Asellota retain a coxa with the primitive capability of promotion/remotion, including an arthrodial membrane and some musculature. CoMPARISON WITH WAGELE’S HYPOTHESIS Wiigele’s (1989a) tree (Fig. 4D) is consider- ably longer than our tree (length = 153, CI = 0.65). However, the two trees share some impor- tant similarities. Both trees place the Phreatoi- cidea at the base of the isopod line. However, MEMOIRS OF THE QUEENSLAND MUSEUM Wagele accepted Dahl’s (1954) conclusion that phreatoicideans were derived from a cirolanoid ancestor, thus forcing Wagele to derive the short- tailed condition (terminal anus and uropods) in the Isopoda three separate times — in the phrea- toicidean line, in the oniscid line, and in his asellote/calabozoidean line. Both our tree and Wagele’s derive the Asellota after the Phreatoi- cidea. However, Wagele concluded that the Cal- abozoidea is the sister group of the Asellota, whereas we regard the calabozoids to be either primitive oniscideans, or the sister group of the Oniscidea. Both trees also derive the oniscideans above the phreatoicid/asellote lines, and then recognize several large groupings of the remain- ing taxa (the long-tailed isopods, as we have defined them). Both trees were unable to satis- factorily resolve the relationships of the long- tailed line. Beyond these generalities, our tree differs markedly from that of Wagele. Wagele’s tree (1989a, fig. 107) depicts 9 taxa: Phreatoicidea, Calabozoidea, Asellota, Micro- cerberidea, Oniscidea, Valvifera, Anthuridea, *Sphaeromatidea’ (sic), and ‘Cymothoida’ (sic). Wagele’s Sphaeromatidea included 7 flabel- liferan families: Keuphyliidae, Lynseiidae, Lim- noriidae, Plakarthriidae, Sphaeromatidae, Serolidae, and Bathynataliidae. His Cymothoida included 8 flabelliferan families (Phora- topodidae, Protognathiidae, Anuropidae, Cirolanidae, Tridentellidae, Corallanidae, Aegidae, and Cymothoidae), plus the Gnathiidea and Epicaridea (Wagele reduces the latter sub- order to family as the ‘Bopyridae’). Wagele’s suggested new Suborder Sphaeromatidea was not defined by any unique synapomorphies, but was based on a general suite of body shape criteria that we regard as (1) incorrect, (2) not applicable to all the groups included in this taxon, or (3) also present in other isopod taxa. We have analysed most of the characters that Wagele used in his tree in our character discus- sions above, but we have coded/assigned many of them differently (and are thus not in agree- ment with Wagele’s assignments of characters to taxa), or we have opted not to use some of them because we feel they are too poorly understood or are inappropriate due to their high levels of homoplasy at this level of analysis. Many char- acter assignments in Wagele’s analysis appear to be incorrect, e.g. the synapomorphic suite used to define his Sphaeromatidea; scoring the phrea- toicideans as having laterally compressed bo- dies; assigning 2-articulate pleopodal exopods to Phreatoicidea but not Asellota; scoring the Asel- PHYLOGENETIC ANALYSIS OF THE ISOPODA lota as possessing an endopod on pleopod 1 of males; regarding Rocinela as having 2-articulate maxillipedal palps and protandric hermaphrodi- tism, or they represent convergences/paral- lelisms hidden within other character complexes (styliform uropods, shortened pleotelson, ver- miform body, etc.). Wagele (1989a, b) has argued that a hypothe- tical, primitive, long-tailed morphology in isopods gave way to the short-tailed morphology on numerous occasions, independently, as a con- vergent adaptation to avoid predation by fishes. Our analysis suggests just the opposite, that the primitive condition in isopods was the short- tailed morphology, inherited from peracarid an- cestors that already possessed a trend toward telson reduction and loss of the caridoid tailfan. Furthermore, it is the long-tailed isopods, not the short-tailed species, that are epibenthic and ac- tive swimmers and more often confront preda- tory fishes. The evolution of predator-avoidance strategies in isopods has not been extensively studied, but Brusca and Wallerstein (1979) and Wallerstein and Brusca (1982) provide compara- tive and experimental data suggesting that, at least for idoteids, they include features such as smaller reproductive size, cryptic colouration and body ornamentation, and certain be- havioural traits. STATUS OF THE CALABOZOIDEA It is evident from our observations of speci- mens of Calabozoa pellucida that it is not an asellotan isopod, but is either a primitive, aquati- cally-adapted oniscidean, or it is a unique crea- ture closely related to the Oniscidea. Van Lieshout’s (1983) and Wagele’s (1989a) at- tempts to unite the Calabozoidea and Asellota were based largely on incorrect homology argu- ments regarding the pleopods. Although the copulatory part of the calabozoan first pleopod could be the exopod, no one has shown the uniramous pleopods of the Asellota to be either the exopod or the endopod. Furthermore, the detailed structures of the male first pleopod in both taxa are completely different (Fig. 10B vs. 10D). The synapomorphies proposed by Wagele for a Calabozoidea-Asellota sister group are in- correct or are symplesiomorphies. For example: a similar telsonic reduction and uropod arrange- ment occurs in the Phreatoicidea and the Onis- cidea (hence these features should actually be symplesiomorphies on Wagele’s tree); female asellotans (and microcerberideans) lack the first pair of pleopods (they are present and biramous in Calabozoa); and, in asellotan males the sec- ond pleopodal endopod is always geniculate (it is styliform in Calabozoa). The male first and second pleopods of Calabozoa most closely re- semble those of oniscideans (Fig. 10). The pre- sence of all 5 pairs of pleopods in female Calabozoa, and the absence of a 6-articulate antennal peduncle and the typical asellotan pleonite condition (pleonites 1 and 2 well- developed and usually modified as a narrow ring, pleonites 3-6 fused indistinguishably with tel- son) further argue against any relationship to the Asellota. In addition, calabozoans possess both dorsally-fused lateral coxal plates and sternal coxal plates, conditions typical of oniscideans but never seen in the Asellota (Table 2), The pleopod morphology of Calabozoa shows many points of similarity to the highly modified copulatory structures found in the oniscideans (Fig. 10, Table 2). Male pleopods 1 and 2 possess elongate styliform gonopods, and the fused me- dian penes arise from the articulation between pereonite 7 and pleonite 1. Furthermore, the pleopodal endopods of Calabozoa are somewhat thickened and tumescent as in terrestrial isopods. The adaptations of a primitive oniscidean to an aquatic lifestyle could predictably result in the differences seen between a typical oniscidean and Calabozoa. The maxillipeds of Calabozoa are very similar to those of the Ligiamorpha. The one feature of Calabozoa that distinguishes it from typical oniscideans is its possession of primitive, unmodified, trilobed maxillae. In oniscideans the maxillae are reduced to simple bilobed plates, The totality of these data and the positioning of the Calabozoidea on the clado- gram suggest that this group represents either a very primitive, relict, aquatic oniscidean taxon, or a distinct taxon that has persisted from a line that led to the modern oniscideans. STATUS OF THE MICROCERBERIDEA Our analysis suggests a close relationship be- tween the Asellota and the Microcerberidea. The synapomorphies shared between these two taxa include the following: (1) antennal peduncle 6- articulate; (2) female pleopod 1 absent; (3) male pleopod 2 with endopod modified into a complex gonopod; (4) pleomeres 1-2 free, 3-5 fused to pleotelson; and, (5) male pleopod 1 uniramous, if present (fused and working with second pleopods in sperm transfer in higher Asellota). The Microcerberidea were regarded as an- thurideans by Karaman (1933), Pennak (1958), Kussakin (1973), and others. Wagele (1983b, (88 19894) reduced the Microcerberidea toa family of the asellote superfamily Aselloidea, along with Asellidac, Stenascllidac, and Atlantasel- lidue. Wiigele"s arguments for including the mi- erocerberids in the Asclloidea relied strongly on similarities in the setae of jhe first pereopod, as well as the characters already mentioned. Simi- lar setae, however, can be seen on the first per- eopods of the Phreatoicidea, so setation may not be a synapomorphy at this taxonomi¢ level. As Wiigele (1983b) noted, the Atlantasellidae (orig- inally included in the Aselloidea by Sket. 1979) have pleopads similar to the Microcerberidea, in which the second pair is absent in females and the {hird pair is uniramous and fused into a single piece that is operculate to pleopods 4 and 5 (in both sexes), Auantasellids and microcerberids also share the unique ‘tubular’ molar process on the mandible. We agree with W4gele (1983b) regarding the probable close relationship between Arlantasel- lus and the microcerberids. These two groups differ from each other primarily on the basis of features perhaps associated with body-size re- duction and the interstitial habitus in the micro- cerberids (reduction of the mouth appendages, cylindrical body form), and Adlaniasellus also bears several unique synapomorphies (inarticu- late uropeds, reduction of antennac). However, we consider these two groups to be distinct enough from the Asellota that we do nol recom- mend placing them in that suborder, nor do we regard Wiigele’s (19894) pulalive synapomor- phies of the superfamily Asclloidea to be justified, All Ascllota have a highly evolved male copulatory system, usually with a strongly geniculate endopod on the male second pleopod coupled with a short powerful exapod used for thrusting the endopod, Asellotans also have a distinct scale on the antenna, uniramous second pleopods in females, and a unique spermathecal duct; these features appear to be lacking in Mi- crocerberidea and Atlantasellidac. In the latter taxa, the male second pleopodal endopod is an elongate, convoluted, straight or curved struc ture, and the exopod is degenerate. In addition, the third pleopod is fused into a single piece in microcerberids and atlantasellids, whereas in most Asellota both rami and the protopod are separate and unfused articles. Many of the at- iributes seen in mictocerberids arid atlantasellids constitute reductions, although the male capula- tory pleopods of these groups are unlike anye thing seen in the Asellota. In conclusion, the most conservative approach MEMOIRS OF THE QUEENSLAND MUSEUM would be to simply transfer the Atlantascllidac to lhe Microcerberidea, allowing this suborder to stand as a sister group to the Asellola sensu stricto, We would recommend this working hy- pothesis until more data are available, purticu- larly regarding the possible presence of jhe asellotan spermathecal duct in microcerberids and atlantasellids, In addition, we see no justifi- cation for the view espoused by Wiigele (1983b) that the Microcerberidea evolved from aselloid ancestors in freshwater. STATUS OF THE PROTOGNATHIIDAF The only two described specimens of Protag- nathia (Schultz, 1977: Wiagele and Brandt, 1988) appear to be mancas, although Wagele and Brandt's (1988) definition of the family assumes that the specimens are subadults or adults. The drawing of this animal by Wagele and Brandi (1988, fig. 1) cven illustrates what appears to remnants of the embryonic yolk, typical of many isapod mancas. Wagele and Brandt claim that Protegnathia bathypelagica Schultz, 1977, is a “missing link’, or ‘intermediate between! the Cirolanidae and the Gnathiidea, Based on the published illustrations, we do not believe thal Wigele and Brandt (1988) were actually dealing with the same species as Schultz (1977). In any case, in our opinion Protegnathia only superti- cially resembles the Gnathiidea and more clasely approximates the manca of a large, predatory, cirolanid-like or anuropid-like creature. The ‘ar- liculating’, serrate, bladelike molar process on the mandible of Protognarfia is characteristic of the Cirolanidac and the cymothoid-line, and this Was no doubt the principal reason for Schultz's (1977) original assignment of P. bathypelagica to the genus Cirelana. The general body uspect is also similar tu juveniles of the genus Syscemus (Acgidae), another flabelliferan family jn the cymothoid-ling. The proposed Gnathiidea-Protognathia syn- apomorphies of Wagele and Brandt (1988) do not hold. First, the absence of the seventh per- eopod and the expandable ventral cuticle is typi- cal of isopod mancas. Second, the tailfan fs identical to that of some cirolanids and aegids, Third, the mandible of Protognathia is not at all like thal of the Gnathiidea, despite the possible similarity in function (predatory feeding}. Ho- mology arguments based on function alone should be viewed with caution, In fact, the mandible of Protegnathia has features typical of Cirolanidae/Anuropidae (the articulated, serrate, bladelike molar process) and the cymothoid-line PHYLOGENETIC ANALYSIS OF THE [ISOPODA in gencral (the acute bladelike incisor process of tridentellids, corallanids, uegids, and cy- mothoids), Fourth, the maxillae of Protegnathia afe quite different from those of gnathiids, in which they are highly reduced (males) or absent (females). The only derived feature that mightbe uniquely shared between Protegnaihia and the enathitds is the plumose setation an the maxil- lipeds. Protegnathia, however, has a similar selation on all of the other thoracopods us well, which is quite unlike the situation in gnathiids, suggesting thal the maxillipedal setation of Pro- tognathia is merely a reflection of segmental parallelism (or serial homology) in this animal and not a homologous synapomorphy shared with the gnathiids. Finally, gnathiids have but 5 pairs of walking legs, 6 free pereonites, 2 pairs of maxillipeds, and numerous other fundamental differences that suggest no close alliance what- soever to Protognathia. The above evidence forces us to conclude that Protognathia shares no synapomorphies with the Gnathiidea, Our phylogenetic analysis cor- roborates these arguments and further suggests that Profognathia is part of the cymothoid-line, The mandibles of Protognathiea and Anuropus are enlarged and have similar ‘articulations’, being oriented more transversely and ventrally than in most isopods, suggesting a possible close affinity between these two groups, The large size of jhe pelagic Protognathia manca is also sug- gestive of Anuropus, which may attain an adult size in excess of 70mm (a 6.6-13,0mm manca could fil within an anuropid developmental sequence). Better resolution of protognathiid af- finities must await the capture of adults of this group. Certainly Wigele and Brandt's (1988) claim that Protognathia is a ‘surviving primitive isopod’ js not correct; in both Wiigele’s (1989a) and our own tree, this taxon derives high up in the flabelliferan line. STATUS OF THE PLABELLIFERA Our analysis corroborates ihe hypothesis af Wivele (19894) and orhers that the Flabellifera, as it is.currenily recognised hy most workers, is not a monophyletic taxon, The Anthuridea, Gnathiidea, and Epicaridea appear to derive from within the flabelliferan complex, However, the two suborders proposed by Wagele, Cy- mothoida and Sphaeromatidea, are not sup- ported hy our analysis, Poore’s (1987) proposed sister croup relation- ship between the Lynseiidae aad the Limnorii- dae is corroborated by our analysis. The ungsual South Pacific genus Hadromastax is currently placed in the family Limnoriidae, However, as Bruce (1988) noted, it appears to lack two key limnoriid attributes — a waisted maxillipedal basis and hook-like uropodal rami. Bruce and Miller (pers. comm.) plan to remove this genus to its own family. However, judging by the man- dibular anatomy and other features, Hadro- mastax appears to be very closely related to the Limnoriidae/Lynseiidae clade. The close relationship shown in ourcladogram between Gnathiidea and Epicaridea is interest- ing and suggests thal the possible common an- cestor of these two groups might have been a hematophagous parasite. In addition to the syn- upomorphies noted on the eladogram, only in these twa groups of isopods are the digestive caeca reduced to a single pair (Stromberg, 1972), Strombere (1967, 1971, 1972) also recognised close ies between epicarideans, gnathiids, and flabelliferans, based on embryological data- Wagele's(1989a) alliance of the Epicaridea with the Cymathoidae appears unjustified, He united these taxa on the basis of five characters. Two of these characters are incorrecl — epicarideans are nol protandric hermaphrodites (they are faculla- tive hermaphrodites) and cymothoids do nat have quadrate uropodal peduncles. The third character, “adults parasitic’, 18 unlikely to be a homologous feature because cymothoids are parasites only on fishes and epicarideans only on crustaceans. The remaining two characters. are apparent convergences (discussed in the pre- vious section) resulting from the purasiti¢ life- style of these taxa — hooklike pereopodal dactyls and reduced antennae, Retaining the Epi- caridea as a Separate suborder for infraorder) has the further distinct advantage ol nol compressing the broad diversity of this group into a single highly heterogeneous family. as proposed by Wapele (1989), Recognition of the close relationships within a cymothoid-line (Fig. 14) is not a new idea. Brusca (1981) analysed jhis relationship for four of these families, and Bruce er al, (1982) and Delancey (1989) elaborated on this. The cy- mothoid-line (Pig. 14) is primarily carnivorous, emphasising predation and scavenging early on (Cirolanidae and Anthuridea), then largely pre- dation (Anuropidac, Corallanidae, and probably Protognathiidae), then obligale predation or tem- porary parasitism {[Aegidae and Tridentellidae), and finally obligate hematophagous. parasitism (Cymothoidae), We did not postulate any synapomorphies for | ox) the family Sphacromatidue, although four possible ones exist: pleonites 1-2 free (primi- tively), pleonites 3-6 fused to telson (with 0-3 pairs of lateral incisions demurcating fused somites); uropodal endopod more-or-less fused to peduncle and immovable; at least some max- illipedal palp articles expanded into lobes; and, pleolelson vaulted, with pleopods held in cham- ber. In addition, in most sphaeromatid genera at least some pleopods bear pleats and unique sqamiferous tubercles. However, because this family is so large and poorly understood, it is unclear whether these features represent true synapomorphies, i.e. are primitive forthe family, A cladistic analysis and taxonomic revision of the Sphacromatidae is greatly needed. Some flabelliferan groupings are not fully re- solved in our tree, suggesting thal some families may be paraphyletic or, more likely. that we have simply been unable to find satisfactory character suites to climinate all polytormes, This does not, however, affect the basic structure of the tree, or the sister group relationships of (he clades that depict the phylogeny of the group ws whole. If the relationships in our (ree (Fig. 14) are correct, the Flabellifera should be expanded to once again include the Anthuridea, Gnatniidea, and Epicaridea, or ij should he split into several separate new groupings. However, because of the unresolved nodes we do not recommend a classificatory change in the Flabellifera at this time. There seems littie doubt, however, thal the anthurideans, gnathiids, and ecpicarideans are derived from deep within the currently recog- nised Flabellifers, Classifying these three groups within the Flabellifera ts not, of course, a new idea, Indeed, Sars (1882) crealed the group ‘Plabellifera” specifically for those isopods with tail-fans composed of lateral uropods and an clongate pleotelson (hence the name). Stebbing (1893), Sats (1897), Richardson (1905), Smith and Weldon (1923), Menzies (1962). Naylor (14972), and many others generally followed Sars’ concept of Flabellifera, and included the anthurideans (and usually the ynathius) in this group. Sars (1897) was quite correct in his sum- mary of the situation nearly 100 years ago, when he stated, ‘It is not casy to give any exhaustive Giagnosis of this tribe (Flabellifera), as it com- prises isopods of extremely different structure. ‘The only essential character common to all the forms, is the relation of the uropads, which are ... lateral and arranged in such a manner as tu forms. with the last segment of the melasome, a caudal fan, simtlir to that found in same of the MEMOIRS OF THE QUEENSLAND MUSEUM higher Crustacea, the shrimps and lobsters.’ The only 8ynapomorphy we can add to Sars’ state- ment is the fact that a 3:4 functional pereapod grouping seems to have evolved in concert with the long-tailed condition, and shortly thereafter ihe blade-like mandibular molar process. UNRESOLVED PHYLOGENETIC PROBLEMS Although We recommend some taxonomic changes (sce conclusions), we do nol propose a new classification of the entire order at this time, We feel that our phylogenetic hypotheses are still not robust enough to do so — the precise phylogenetic placement of several groups can- not yet be resolved to our satisfaction. Specifi- cally, the relationships of the 8 long-tailed clades depicted in the consensus Itee (Fig, 14) remain somewhat enigmatic. We believe Wagele (1989) was premature in proposing his radical new classification of the Flabellifera, Because the long-tailed clade represents what appears to be a clearly monophyletic and easily-recognised group, with correlated anatomical and ecological attributes, we suggest that classificatory recop- nition of this clade is warranted and desirable. OTHER PosstBLe TREE TOPOLOGIES Because many workers have emphasised a hy- pothetical cirolanid-like (or flubellifera-like) an- cestor for the [sopoda, we built several alternative trees 10 compare to ours. Each of these alternative irees wis analysed with the program MacClade, with (he same dala set used to construct our tree (Appendices | and I), Trees identical to our cladogram (Fig, 14), bul with the Cirolanidac placed at the base, are 135 steps long. Trees with the entire long-lailed grouping placed at the base, rooted in the Cirolanidae are {35 steps long. Trees with the long-tailed line af the bottom, but otherwise with the taxa in that group arranged exyetly in our tree are 131 steps Jong. All of these trees are longer and less pursi- monious than the 16 shortest trees. (129 steps) summarised in our consensus tree (Fig. 14). Il should be noted that if trees just one step longer are included for consideration, it can require that seVeral hundred to several thousand new and different tree arrangements be considered. Thus selection of the shortest tree, even if it is shorter hy only one step, allows one to reject entire suites of alternative hypotheses, The ability to rule out these lurge suites of alternative trees is, of course, the strength of the method of logical parsimony. PHYLOGENETIC ANALYSIS OF THE ISOPODA Bioceocrapic ConsipERATIONS Our analysis suggests that the Phreatoicidea and Asellota derived early in the cvolution of the Isapoda, and are the most primitive living isopod taxa. According to Wagele (1981, 1983b), the uecurrence of some members of these two groups in fresh water suggests that theircommon ancestor was a freshwater form, and that perhaps the [sopoda as a whole arose in fresh waler, the marine environment having been invaded later. A more reasonable view, however, considers multiple invasions of fresh water from ancient marine stocks. There are several good reasons to accept this second alternative, First, the invasion of freshwater habitats has obviously occurred many times in the past, as evinced by the many unrelated isopod taxa that live in these habitats today, represcnting at least some genera in every suborder except perhaps the Gnathijdea (in addj- tion to phreatoicideans, asellotans, and microcer- hberids, freshwater species occur in at Icast the following genera: Calabozoidea (Calabozoa), among the Oniscidea, Brackenridgia, Cantabranis- cus, Mexioniscus, Typhlotrichotigioides, Xilisfonis- cus; among Anthuridea, Cruncgens, Curassaniara, Cyathura, Paranthura, anong Cirolanidac, Anap- silana, Antrolana, Bahalana, Bermudalana, Ciro- lanides, Faucheria, Haptolana, Mexilana, Speociralana, Sphaeromides, Turcalana, Typhloci- roleree; among Cymothoidac, Artystone, Asotana, Braga, Lironeca, Nerocila, Paracymothoa, Philos- tomella, Riggia, Telotha,; among Sphaeromatidae, Sphaeroma, Thermosphaeroma, among Valvifera, Austridotea, ldetea, Mesidotea, Notdotea, among Epicandea, Probopyrus; and many others). Second. fossil evidence (Schram, 1970, 1974) indicates that the Palaeozoic phreatoicideans, which are nearly indistinguishable from modern taxa, lived in marine environments, not freshwa- ter habitats. Modern Phreatoicidea and Asellota that live in freshwater are likely to be relies of a past lime when these groups were diversifying and invading many differentenvironments, Oul- group data also suggest that the Isopoda prab- ably evolved in a marine environment, because amphipods, mictaceans, and tanaidaceans are al! primary marine groups, The fossil record is very sparse for isopods, There'are no known asellotan fossils, The oldest isopod fossils are phreatoicid- cans: Hesslerella shermani Schram, 1970, from middle Pennsylvanian marine deposits of Narth Arnerica: Permian fossils from several marine or brackish-waler localities of Laurasia; and Trias- sic material from Australia (ftesh water). Thus, although phreatoicideans are restricted Widay to 19) freshwater habitats in South Africa, Australia, New Zealand. and India. they must have had u broad global marine distribution during the Paleozoic. A few flabelliferans and presumed epicarideans are known from Mesozoic straja, while oniscideans and valviferans have been found only in Tertiary (Oligocene) deposits. Very few specific biogeographic relationships reveal thenisclves in an analysis at this level, However, there are two striking patterns that are evident. First ts the strong Gondwanan ties of the long-tailed clade. Many of the long-tailed lines are strictly or primarily Southern Hemisphere in distribution: Keuphyliidac is known only from the Australian region; Bathynataliidae from the southern Indian Ocean and Australia; Plakar- thrijdae from the Southern Hemisphere; Phora- topodidae from southern Australia; the Valvifera is probably Southern Hemisphere in origin (Brusca, 1984); and species of Serolidae occur primarily in the Southern Hemisphere. In addi- tion, the majority of species of Cirolanidae and Sphaeromalidae also are probably known fram (he Southern Hemisphere. Interestingly, the ear- liest derived Ascllota not restricted to fresh water are also largely Southern Hemisphere in dis- tribution (Pscudojaniroidea, Stenetripides, and the shallow-water Janiroidean families Para- munnidae and Santiidae). Secondly, all of short-tailed lines on the clade- gram show strong reliciual patterns of distribu- tion. The Phreatoicidea, which were once widespread globally in marine environments, are now restricted to a few Gondwanan freshwater habitats. The higher Asellota (Janiroidea) are found primarily in the deep sea, where they have undergone 4 massive radiation to exploit an en- vironment only recently invaded by other isopod groups. The Microcerberidea are interstitial forms. The Calahozoidea so-far are known only from fréshwater wells (phreatic systems) in Venezuela. And the Ligiamorpha and Tylomor- pha are, of course, the only crustaceans to have successfully radiated into al! terrestrial environ- ments. Beyond these generalisations, the data are not vel availible co discern clear historical patterns or tes! specific bingeographical hypotheses at the suhordinal/family levels. Testable phylogenctic and biogvographic analyses are needed for each suboruer. and each af the long-tailed clades, in order to. determine putative ancestral geographic ranges for cach of these groups (wz, Brusca. 1984) hefare more general statements can be 12 made regarding the biogeographic history of the Isopoda. Future RESEARGE Despite an extensive examination of available morphological characters, it is clear thac the available data base needs to be expanded by the addition of new characters and by resolution of homology complexes in others. Useful new characters almost certainly exist in patterns of frontal lamina and clypeus design, details of mandibular anatomy (especially of the lacinia and spine row region), oostegiie morphology, nature of the sternal coxal plates, and internal anatomy, bul the existing literature is insufficient ty assemble a data base on such features and additional direct observations are necessary. These data will be needed to further resalve the relationships within the long-tailed isopod clade. A phylogenetic analysis of the Sphacromatidac is alsa needed and would provide valuable infor- mation for continued refinement of the flabel- liferan taxa. CONCLUSIONS I, The Isopoda js a monophyletic group de- fined by the following synapomorphies: (a) ses- sile eyes; (b) complete loss of free carapace folds (carapace reduced to a cephalic shield); (c) thoracopods entirely uniramous: (d) antennae uniramous, without a seale (a ‘scale’ has either reappeared in the Asellota, or it was lost twice, once in the Phreatoividea and again in all other non-Asellota); (c) pleomere 6 fused to telson, forming a pleotelson; (f) biphasic moulting; (g) heart thoraco-abdominal; (h) branchial structures abdominal; (i) gut tube entirely ectodermally derived, without a [rue midgut region; (j) striated muscles with unique myofibril ultrastructure: (k) loss of the maxillulary palp; (1) antennules uni- ramous, without a scale (scales reappear in the cirolanid genus Bathynomus, in the Limnoriidac. and perhaps in the Lpicaridea); and, (m) uropo- dal rami always uniarticulate. Synapamorphies ‘a+ appear to be convergent in isopods and amphipods, although a strong corroboration of this must await further analyses of ull peracarid suborders, Synapomorphy ‘c’ may (or may not) be convergent to the condition in many tan- aidaceans. Synapomorphies 'f-m* are unique to the Isopoda. 2. The Phreatoicidea is the earliest derived taxon of living isopods. 3. The Microcerberidea is the sister group of MEMOIRS OF THE QUEENSLAND MUSEUM the Asellota, but cannot be considered part of the Ascellota unless the definition of the latter ts expanded, which we do not recommend at this lime, 4. The Oniscidea constitutes a monophyletic group. 5, The monotypic taxon Calabozoidea (Cala- bozoa) should be classified as primitive Onis- cidea, or us the sister group of the Oniscidea (Calabozoa is neither an asellotan nor a sister group of the Asellota). 6. Isopods with broad, flat uropods and clon- gate telsonic regions (well-developed tailfans) arose subsequent ta the appearance of the phrea- toicid/asellote/microcerberid/oniscidean lines. The apparent ‘caridoid’-like tailfan of these jong-tailed isopods is thus not a primitive isopod feature, but is secondarily derived within the Isopoda and not homologous with the candition secn in the mysidaceans and other truce caridoid crustaceans 7. The evolution of the long-tailed morphology may have corresponded with the emergence of isopods from infaunal environments and a sub- sequent radiation as active epifaunal swimmers. Paralleling this trend was a shill from a primary scavenging/herbivorous lifestyle to active pred- atory habits, and eventually parasitism. Also par- alleling this trend was an enlargement of the lateral coxal plates, perhaps functioning to in- crease hydrodynamic streamlining of the body. 8, Three taxa usually ranked at the subordinal level (Anthuridea, Gnathiidea and Epicaridea) had their phylogenetic origins within the lincage of families currently regarded as Flabellifera, Thus, the definition of Flabellifera must cither be expanded to accommodate these taxa, and/or the suborder Flabellifera should be reorganised into several separate groups. 9, The Protognathiidae is part of ihe ‘cy- mothoid-grcup’ of families and may be closely related to the families Cirolanidae and Anuropidae. The Protognathiidae is not the sister group of the Gnathiidea. 10. The recently proposed new suborders of Wagele (19894), Sphacromatidea and Cy- mothvida (sic), are not corroborated by our phy- logenetic analysis, Wigele's proposition that the ancestral isopod was a long-tailed form (flabel- liferan, or cirolanid-like) js not supported by our analysis, Our analysis indicates that the ancestral isopod was a short-jailed form, with a shortened telsan and styliform, terminal uropods. The Gnuthiidea and Epicaridea should be retained al the subordinal ranking until further analyses bet- PHYLOGENETIC ANALYSIS OF THE ISOPODA ter resolve the relationships of the flabelliferan families. 11. All of the primitive, short-tailed isopod taxa (Phreatoicidea, Asellota, Microcerberidea, Oniscidea, Calabozoidea) exhibit what may be viewed as relictual distributions, in isolated freshwater habitats, in ground waters, in the deep sea, or in terrestrial habitats. The most primitive living isopods, the Phreatoicidea, also have the oldest known fossil record (middle Pennsyl- vanian) and a modern Gondwanan distribution (Australia, Tasmania, New Zealand, southern Africa, and India). However, fossil phreatoicids are known from North American and European marine deposits, suggesting that the present-day freshwater Gondwanan pattern is a relict dis- tribution. 12. Unambiguous sister group relationships cannot be hypothesized for all isopod taxa with the current data base, and additional data are being sought in the form of new characters. A new formal classification of the Order Isopoda must await better resolution of the phylogeny based upon an expanded data set. ACKNOWLEDGEMENTS We would like to thank the organising com- mittee of the International Crustacean Confer- ence (Brisbane, July 1990) for the invitation and financial support provided to one of us (RCB) to be a Plenary Session speaker. That invitation provided the impetus for writing this paper. We are most grateful for the opportunity to have shared our ideas with colleagues at that confer- ence. We also thank Gary Poore (Museum of Victoria, Melbourne) for organising a highly valuable isopod workshop prior to the main con- ference; this workshop was fertile ground for scientific exchange and led to the refinement of some data and ideas presented herein. We are especially grateful to J.L. Barnard, Tom Bow- man, Gary Brusca, Niel Bruce, Gary Poore, Fred Schram, Jurgen Sieg, and Regina Wetzer for their extremely helpful reviews of our manu- script; and to J.L. Barnard, N. Bruce, T. Bow- man, R.R. Hessler, J. Just, B. Kensley, G. Poore, J. Sieg, W. Wagele, R. Wetzer, and T. Wolff for many insightful discussions on peracarid mor- phology and phylogenetics during the course of this research. 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Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex (L.). Zool- ogisches Jahrbuch (Anatomie) 77: 51-110. WILSON, G.D. 1976. The systematics and evolution of Haplomunna and its relatives (Isopoda, Ha- plomunnidae, new family). Journal of Natural History 10: 569-580. 1980a. Superfamilies of the Asellota (Isopoda) and the systematic position of Stenetrium weddel- lense (Schultz). Crustaceana 38(2): 219-221. 1980b. New insights into the colonization of the deep sea: Systematics and zoogeography of the Munnidae and the Pleurogoniidae comb. nov. (Isopoda; Janiroidea). Journal of Natural History 14: 215-236, 1986a. Pseudojaniridae (Crustacea: Isopoda), a new family for Pseudojanira stenetrioides Bar- nard, 1925, a species intermediate between the asellote superfamilies Stenetrioidea and Janiroidea. Proceedings of the Biological Society of Washington 99: 350-358. 1986b. Evolution of the female cuticular organ in the Asellota (Crustacea, Isopoda). Journal of Morphology 190: 297-305. 1987. The road to the Janiroidea: the comparative morphology and evolution of the asellote isopods. Zeitschrift fiir zoologische Systematik und Evolutionsforschung 25: 257-280. 1989. A systematic revision of the deep-sea sub- family Lipomerinae, of the isopod crustacean family Munnopsidae. Bulletin Scripps Institu- tion of Oceanography (University of California) 27: 1-138. 1991. Functional morphology and evolution of isopod genitalia. 228-245. In R. Bauer and J. Martin (ed.) ‘Crustacean sexual biology’. (Uni- versity of Columbia Press). WILSON, G.D. AND HESSLER, R.R. 1974. Some unusual Paraselloidea (Isopoda, Asellota) from the deep benthos of the Atlantic. Crustaceana 27: 47-67. 1981. A revision of the genus Eurycope (Isopoda, Asellota) with descriptions of three new genera. Journal of Crustacean Biology 1: 401-423. WILSON, G.D., THISTLE, D. AND HESSLER, R.R. 1976. The Plakarthriidae (Isopoda: Flabellifera): deja vu. Zoological Journal of the Linnean Society $8: 331-343. ZENKEVITCH, L.A. AND BIRSTEIN, J.A. 1961. MEMOIRS OF THE QUEENSLAND MUSEUM On the problem of the antiquity of the deep-sea fauna. Deep Sea Research 7: 10-23. 1969. On the geological antiquity of the deep-sea bottom fauna. Okeanologia (Moscow) 1: 110- 224. [In Russian]. APPENDIX 1. CHARACTERS USED IN THE PHYLOGENETIC ANALYSIS 1. Eyes stalked and basally articulated (0) — Eye stalks reduced, lobe-like, but sometimes with basal articulation (1) — Eyes sessile (2). 2. Carapace covers all 8 thoracomeres and laterally covers the bases of the maxillae and maxillipeds (0) — Carapace reduced, lateral carapace folds still cover the bases of the maxillae and maxillipeds (1) — Carapace reduced to only a head shield, without lateral carapace folds (2). 3. Monophasic moulting (0) — Biphasic moulting (1). 4. Heart entirely thoracic (0) — Heart thoraco-abdom- inal (1). 5. Branchial structures cephalo-thoracic (0) — Branchial structures abdominal (1). 6. Pleomeres 4-6 not divided into two separate functional units (0) — Pleomeres 4-6 forming a functional unit (the urosome), and pleopods 4, 5, and 6 modified as uropods (1). 7, Body not unusually broadened and flat (0) — Body extremely broadened and flat, with large, expanded coxal plates, and with the cephalon deeply im- mersed in or surrounded by the first pereonite (1). 8, Gut tube with endodermally derived midgut (0) — Gut tube entirely ectodermally derived, without a true midgut region (1). 9. Striated muscles of typical malacostracan type (0) — Striated muscles with unique myofibril ultra- structure (1). 10. Second thoracomere (pereonite 1) free, not fused to cephalon (0) — Second thoracomere entirely fused to cephalon, with its appendages (the py- lopods) functioning with the cephalic appendages and acting as a second pair of ‘maxillipeds’ (1). 11. At least some thoracopods with exopods (0) — Exopods absent from all thoracopods (1). 12. Hatching stage not a manca (0) — Hatching stage a manca (1). 13. Without a praniza stage (0) — With a praniza stage (1). 14, Adult females bilaterally symmetrical (0) — Adult females with loss of symmetry (1). 15. Adults not parasitic on other crustaceans (0) — Adults obligate parasites on other crustaceans (1). 16. Without cuticular tricorn sensilla (0) — With cuticular tricorn sensilla (1). PHYLOGENETIC ANALYSIS OF THE ISOPODA 17. Withoul complex campound sensillar structures of the oniscidean type at the lips of the antennae and uropodal rami (0) — Complex compound sensillar structures at the lips of the antennae and urapodal rami (1). 18. No functional pereopodal grouping (0) — Functional pereopodal grouping 3:4 (1) — Functional! pereopoda!l grouping 4:3 (2) — Functional pereopodal grouping 2:5 (3). 19. Seventh pereonite present and wilh pereapods (()) — Seventh pereonite reduced and without per- eopods (1). 20. Antennule biramous, or with scale (0) — Anten- nule uniramous, without scale (1). 21, Antennular peduncle 3-articulate with an un- divided third article (0) — Antennular peduncle 4-articulale, presumably by way of subdivision of third article (1), 22. Antennules arise above (anteradorsal lo) antennae (0) — Antennules arise on same plane as antennae. directly between them (1). 23. Antennules not as described in the following (0) — Antennules greatly modified, 2-articulate, with second (distal) arlicle greatly expanded and scal- loped (1). 24. Antennal peduncle 6-articulate (0) — Antennal peduncle 5-articulate (1). 23. Antennae biramous, or with a vestigial second ramus Orscale (0) — Antennae uniramous, without vestigial second ramus or ‘scale’ (1). 26. Antennae well developed (0) — Antennae ves- ligial (1). 27, Mandible without lamina dentata (0) — Mandible with lamina dentata (1). 28. Mandibles ‘normal’ (0) — Mandibles. of adult males grossly enlarged, projecting anteriorly. for- ceps-like (1). 29. Mandibles present in adult females (0) — Mandi- bles lost in adult females (1). 30. Molar process of mandible a broad, flat, grinding structure (()) — Molar process of mandible an elon- gale, thin, blade-like, slicing structure (often at- tached to body of mandible by a flexible ‘articulation’, and often bearing marginal denticles or leeth) (1) — Molar process of mandible absent 2). i Maxillule present (0) — Maxillule reduced or vestigial inadults (1) — Maxillule lost in adults (2). 32. Maxillule with a palp (0) — Maxillule withaul a palp (1). 33. Maxillae not fused to paragnath (0) — Maxillae reduced, minute. fused to paragnath (or Jos! en- tirely) (1). 34, Maxillae outer lobe undivided (0) — Maxillae outer lobe divided into two lobes (1). 201 35. Mandible with a palp (0) — Mandible without a palp (1). 36. Maxillae not modified as follows (0) — Maxillae modified into stylet-like lobes with recurved apical (hooklike) setae (1). 37, Maxillipeds separate (0) — Left and right maxil- lipeds fused together (1), 38. Coxue of maxillipeds not Fused to head (0) — Coxae of maxillipeds fused to head (1). 39. Maxillipedal endile without coupling spines (0) — Maxillipedal endite with coupling spines (1). 40, Head sunk into first pereonite, flexing dorsoven- trally bul not freely rotating (left to right) (0) — Head set off from pereon and freely rotating (1). 41. Maxillipeds with 2-3 endites (0) ~ Maxillipeds with only 1 endite (1). 42. Maxilliped biramous (0) — Maxilliped uniramous (1). 43. Without lateral coxal plates (0) — With lateral coxal plates (1). 44. Basis of maxilliped nol elongate and waisted (0) — Basis of maxilliped elongate and waisted (1). 45. With lateral epipods on pereopods (0) — Wilhout lateral epipods on pereopods (1). 46. Without medial epipods on pereapods (0) — With medial epipods on pereopods (1). 47. No special cuticular spermathecal ducts known to occur (0) — Unique spermathecal cuticular organs present (1). 48. Male penes on coxae (0) — Male penes on sternite (1). 49. Penes on thoracomere 6 (0) — Penes on pleamere 1, or on the articulation between thoracomere 8 and pleomere 1 (1). 50. Mandibular incisor process broad and multiden- tate (0) — Mandibular incisor process with teeth reduced to form serrate or crenulate margin (1) — Mandibular incisor process with teeth lost (or fused 2) to form conical projection with basal ‘rasp and file” (2) — Mandibular incisor process modified into recurved or hoaklike, acute or subacute, pierc- ing-slicing structure (3). 51. Embryos curve ventrally (0) — Embryos curve dorsally (1). 52. Primary adult excretory organs are antennal glands (0) — Primary adult excretory organs are maxillary glands (1). 53. With narrow, multisegmented pleopodal rami (0) — With broad, flat, ]- or 2-articulate pleopodal rami (1). 54, Male pleopods | and 2 not as follows (0) — Male pleopod endopods | and 2 (only 2 in Ligiidae) elongate, styliform, and participating together in the copulalory process (1). 55. Uropods arise from anteroventral margin of 202 pleotelson (0) — Uropods arise on posteroventral surface of pleotelson, in shallow grooves or chan- nels (1). 56. Both pleopodal rami thin and lamellar (0) — Pleopodal exopods broad and opercular; endopods thick and tumescent (1). 57. Uropods broad and flattened (0) — Uropods styl- iform (1). 58. Telsonic region of pleotelson well-developed, with anus and uropods at the position of pleomere 6 (at the base of pleotelson) (0) — Telsonic region greatly reduced and shortened, anus and uropods positioned terminally on pleotelson (1). 59. Uropodal rami multiarticulate (0) — Uropodal rami always uniarticulate (1). 60. Uropodal exopod not folded dorsally over pleotel- son (0) — Uropodal exopod folded dorsally over pleotelson (1). 61. Uropods not modified as follows (0) — Uropods modified as a pair of opercula covering entire pleopodal chamber (1). 62. Uropods not modified as follows (0) — Uropods form ventral operculate chamber covering anal re- gion (1). 63. Uropods unlike pleopods; associated with pleotel- son (0) — Uropods directed ventrally; identical to, and functioning with, pleopods (1). 64. Pleomere 6 freely articulating with telson (0) — Pleomere 6 fused with telson, forming a pleotelson (1). 65. Pereopods 2-7 not prehensile (0) — Pereopods 1-3 (or 1-7) prehensile (1). 66. Adults not obligate and permanent parasites on fishes (0) — Adults obligate and permanent para- sites on fishes (1). 67. Uropodal endopods not claw-like (0) — Uropodal endopods claw-like (1). 68. Uropodal exopods not claw-like (0) — Uropodal exopods claw-like (1). 69. Pereonite VII not as follows (0) — Pereonite VII tergite indistinct dorsally, shortened and largely or entirely fused to pereonite VI (1). 70. Pleopod 5 not reduced to a single plate (0) — Pleopod 5 reduced to a single plate (1). 71. Uropods not modified as follows (0) — Uropods modified as elongate, clavate structures with re- duced rami (1). 72. Apex of pleotelson not curved dorsally (0) — Apex of pleotelson curved dorsally (1). 73. Pleomere 5 not markedly elongate and much longer than all others (0) — Pleomere 5 markedly elongate, manifestly longerthan all other pleomeres (1). 74. Medial margin of maxilla with row of large filter MEMOIRS OF THE QUEENSLAND MUSEUM setae (0) — Medial margin of maxilla without row of large filter setae (1). 75. Female pleopod 2 biramous (0) — Female pleopod 2 uniramous (1). 76. Male pleopod 2 not as follows (0) — Male pleopod 2 exopod modified to function in concert with large geniculate endopod in sperm transfer (1). 77. Exopods of at least posterior pleopods biarticulate (0) — No pleopods with biarticulate exopods (1). 78. Female pleopod 1 present (0) — Female pleopod 1 absent (1). 79. Male pleopod 2 with lamellar exopod (if present) and endopod either lamellar or modified (0) — Male pleopod 2 with small non-lamellar exopod and a large endopod modified into a complex gonopod (1). 80. Pleomeres not as follows (0) — Pleomeres 1 and 2 free, 3-5 always entirely fused to pleotelson (1). 81. Male pleopod 1 biramous, lamellar (0) — Male pleopod 1, if present, uniramous (fused and working with pleopod 2 in sperm transfer in higher Asellota) (1). 82. Female pleopod 2 present (0) — Female pleopod 2 absent (1). 83. Female pleopod 3 biramous, not fused into a single piece (0) — Female pleopod 3 uniramous and fused into a single piece forming an operculum over pleopods 4 & 5 (1). 84. Male pleopod 2 not as follows (0) — Male pleopod 2 exopod reduced to a simple, 1- or 2-articulate ramus, apparently not involved in copulation or sperm transfer; endopod complex and highly varia- ble in shape, straight, curved, or slightly bent (but not fully geniculate) (1). 85. Lateral coxal plates 2—7 (if present) fused to their respective pereonites and not articulating (0) — Lateral coxal plates 2-7 (if present) not entirely fused to their respective pereonites (1). 86. Pleomeres 1 & 2 not reduced to sternal plates (0) — Pleomeres 1 & 2 reduced to sternal plates only (1). 87. Uropodal rami free (0) — Uropodal rami fused to peduncles (1). 88. Posterior pereopods ‘normal’ (0) — Posterior pereopods oar-like, with dactyls greatly reduced or absent (1). 89. Body not as follows (0) — Body deeply inflated (1). 90. Not parasites on gelatinous zooplankton (0) — Parasites on gelatinous zooplankton (1). 91. Mandibles not modified as follows (0) — Mandi- bles modified as elongate scythe-like structures with serrate cutting edge (I). 92. Maxillule not as follows (0) — Maxillule of a single elongate stylet-like lobe, with the apex form- ing an acute recurved piercing stylet (1). Mysidacea 0000000000 Mictacea 0000000000 Tanaidacea 0000000000 Amphipoda 0000000000 Phreatoic. 0001000000 Valvifera 1001000000 Epicaridea 0001100000 Gnathiidea 0001000000 Anthuridea 0001000000 Tylomorpha 0101000000 Ligiamor. 0001000000 Asellota 0001000000 Calabozo. 0001000000 Microcerb. 0001000000 Aegidae 0001100000 Anuropidae 0011000000 Bathynat. 0001000000 Cirolanid. 0001000000 Coralland. 0001000000 Cymothoid. 0001110000 Keuphylid. 0001001000 Limnoriid. 0001000100 Lynseiidae 0001000001 Phoratopd. 0001000000 Plakarth. 0001000000 Protognat. 0001000000 Serolidae 0001000010 Sphaeromt. 0001000000 Tridentll. 0001000000 Synapomorphies of terminal taxa. Note: this is not an exhaustive list of synapomorphies unique to each terminal taxon; it is a list of only those present in the data set used for the current analy- sis (see Methods section and Appendix I). Re- PHYLOGENETIC ANALYSIS OF THE ISOPODA APPENDIX II. THE DATA MATRIX 0000000000 0000000000 0000000000 0000000000 0000700000 00 1120000770 0100000300 0001000000 000000?000 0000700000 00 1100000100 0100000200 0000000000 0000000000 0000700000 00 2200010000 1000000200 0001100000 0000000000 0000100000 00 2211100110 1100000201 0001100000 0110000000 0000700000 00 2211100110 1100000101 0001100000 0001001000 0000000000 00 2211100110 1101100100 0001110002 0001001000 0000000000 10 2211100111 1110000111 0001100112 0001001000 0000000000 10 2211100110 1100000101 0001101001 0001001000 0000000000 00 2211100110 1100011701 ?101100000 0001001000 0000000000 00 2211100110 1100011701 ?101100000 0001001000 0000000000 00 2211100110 1100000201 0000000000 0001110111 1000700000 00 2211100110 1100010201 0701100000 0001001000 0000011000 00 2211100110 1100000201 0000100000 0001001111 1111700000 00 2211100110 1100000101 0001100001 0001001000 0000000000 00 2211100110 1100000101 0011100001 0001001000 0000000011 00 2211101110 1100000101 ?001100002 1001001000 0000100000 00 2211100110 110000010? 0007100001 0001001000 0000000000 00 2211100110 1100000101 0001100001 0001001000 0000000000 O1 2211100110 1100000101 ?001100001 0001001000 0000000000 00 2211101110 110000010? 0001100002 0001001000 0000100000 00 2211100110 1100000100 0007100002 0011001000 0000000000 00 2211100110 Oe a ee A anes 0001001000 0000000000 2211100110 1100000101 *1001100001 0001001000 0000000100 00 2211101110 1100000701 0001100002 0001001000 0000100000 00 2211100110 1100000101 0007100001 0001001000 0000000000 00 2211101110 1100000101 1001100002 0001001000 0000700000 00 2211100110 1100000101 0001100000 0001001000 0000000000 00 2211100110 1100000101 0001100001 0001001000 0000000000 00 APPENDIX III 0000000000 0101000010 0001000010 0000001000 0101000010 0101000010 2107100010 110?100010 01172000100 0101100000 0101100000 0101000010 0101100000 0107000000 0107010000 0107000070 0101000010 0101000010 0107010000 0107010000 0101100010 0107000011 0101100001 0101000010 010?000000 0107000000 0101000000 0101000010 0107010010 0000000000 1100100000 1100100100 0110110100 1100100000 1110100110 111010010? 111010010? 1110100100 1110100110 1110100110 1100101100 1110100110 1100100100 1110100103 1110100103 1110100100 1110100100 1110100103 1110100103 1110100101 1111100102 1111100102 1110100170 1110100101 1110100273 1110100101 1110100100 1110100103 indicated by parentheses. Anthuridea: 27, 33, 38, 39(0), 60. Anuropidae: 23, 63, 89, 90. Asellota: 24(0)[?], 47, 75, 76. Bathynataliidae: 71. 203 0000000000 1710007000 1110001100 0000001000 1110001110 1110000010 1110000010 1110000010 1110000011 1111010110 1111011110 1110001110 1111011110 1110001110 1110000010 1110000010 1110107010 1110000010 1110000010 1110000010 1110100010 1110007010 1110000010 1110000010 1110100010 1110000010 1110?00010 1110000010 1110000010 versals and multi-state character changes are 204 Calabozoidea: 86, 87. Corallanidae: 39(0), 92. Cymothoidae: 66. MEMOIRS OF THE QUEENSLAND MUSEUM Microcerberidea: 39(0), 77, 82, 83, 84. Phoratopodidae: 21, 88. Phreatoicidea: 72, 73. Epicaridea: 14, 15, 20(0), 26, 31(2), 65. Protognathiidae: 39(0). Gnathiidea: 10, 13, 19, 28, 29. Serolidae: 21, 69. Keuphyliidae: 35, 67. Tylomorpha: 57(0), 62. Limnoriidae: 20(0), 68, 73. Valvifera: 49, 61 Lynseiidae: 35, 39(0), 70. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum THE IMPORTANCE OF TAXONOMY AND MUSEUMS IN THE 1990S RAYMOND B, MANNING Manning, R.B. 199) 09 01: The importance of taxonomy and museums in the 1990s, Memoirs of the Queensland Museumn 31; 205-207. Brisbane, ISSN 0079-5835, Much of the basic research on taxonomy 1s carried oul in museums, traditional primary sources of information on species. Museums are characterized by their collections — archival holdings of organisms, field and historical data associated with those organisms — and library facilities, usually in volumes far beyond those available to individuals in other kinds of research laboratories. These characteristics of museums can only increase their value and the importance of the roles they play in the fulure, given our critical need to understand our environment and its components, especially species. Some problems facing Museums are discussed, and illustrations of same of the kinds of research carried Oulal museumsare given [rom ongoing research on geryonid crabs. (] Museums, taxonomy, systematics, biadiversity, funding. Raymond B. Manning, Department of Inverrebeqte Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20500, USA; 6 July, 1990, Systematics or taxonomy is the study of natu- ral diversity, better known today by the catch- word biodiversity, thanks to the efforts of E.O. Wilson and others (Wilson, 1985, 1988; Black e/ al, 1989), and it is the kind of research charac- teristic of museums. Systematic research is basic to any other kind of biological study involving species, whether it be fisheries or molecular bi- ology. ecology, behaviour, or zoogeography. Inthe 1990s we seem ta have reached the point where both individuals and organisations outside the systematic community, including en- vironmentalists, legislators and sources of re- search funding, recognise the fundamental importance of knowledge of species diversity, museum collections which represent bascline data over time, and traditional systematic work, and appear to be beginning to appreciate the need for museum collections and systematics. more than at any time in the history of systematic research, a time period spanning almost 300 years, Museums and the systematic prolession in general, instead of being prepared for such a momentous change. are facing a crisis: we ap- pear to be losing systematists and systematic organisations, including museums, Part of the problem is that the science of sys- tematics has never been accorded the stature it deserves among all sciences. “Strange as jl may seem, there is less allention and regard paid to systematic work at the present time than ever before.’ This is not a quote from an editorial published in 1990 in ‘Science’ or ‘Nature’. [twas published by Waldo Schmitt in 1930, and it is just as valid today, 60 years later. Further, even though museums are primary sources of information on species and even though we are in the ‘information age,’ automat: ion of museums’s major sources of information on species, their collections and their libraries. lags a generation or more behind current tech- nology. Any major department store chain has in its data inventory specific information on in- dividual items of clothing, such as a pair of slacks, including size, fabric, colour, manufac- turer, and location. This volume of information on species of shrimps, even commercial shrimps, is generally unavailable from any museum col- lection, large or small, in machine retrievable form. Even grocery stores routinely use bar-code technology to check-out groceries and prepare bills (invoices). Museums prepare invoices the old fashioned way, as our ancestors did, by hand. The technology needed by museums has exisled for years. The funding and the expertise needed to implement the technology is not yet available to most museums, which in consequence are unable to manage the vast amounts of informa- tion on species available to them. In the past 30 years we have seen a dramatic increase in numbers of recognised species of crustaceans, especially in decapods, results of the work of a generation of specialists. In gery- onid crubs, for example, specimens identified with Geryon affinis Milne Edwards and Bouvier and Geryon quinguedens Smith now have been assigned to af feast 18 different species. Al- though this may not be true for other crustacean groups, we are about to lose a generation of giants in decapod crustacean systematics, The 206 list of deeapod specialists now retired or near retirement includes Fenner A. Chace. Jr. Mi- chéle de Saint Laurent, Jacques Forest, John Garth, Janet Haig, Horton H, Hobbs, Jr. LB, Holthuis, R.W. Ingle. 8. Mivake, Isabel Pérez- Farfante, Austin B, Williams, and John Yaldwyn. When Ingle retires next year, the British Museum will have one crustacean spe- cialist on its staff, Geoffrey Boxshall; it will be without a decapod specialist for the first time this century. The Japanese crab specialist, Tune Sakai, passed away several years ago, as did Richard Bott, Ch. Lewinsohn, and Raoul Seréne. There appear to be few replacements available for these specialists, all of whom worked al the regional or international level. There are many decapod specialists today who work at the national or local level, and perhaps we are seeing a trend away from a few specialists working world-wide to numerous specialists working nationally. This trend could result in more pres- sure on museums to provide information on the literature as well as on species. Not only are we losing people, in¢luding many great systematists, we are lasing institutions. The Allan Hancock Foundation, one of the large, active museums in the United States with a long tradition of research, is in the process of transfer- ring its crustacean collections to the Los Angeles County Museum. The British Museum is de-em- phasising monographic work and work on local faunas, even though one of its new areas of emphasis is biodiversity. The government of New Zealand has disestablished the biosyste- matics programme of the New Zealand Oceano- graphic Institute, leaving Des Hurley and Elliot Dawson without jobs. One bright spot is here in Australia, where the Australian Biological Resources Study, now in its 10th year, anticipates a 12.5% budget inerease for 1990 (ABRS, 1990). A wide variety of reports on the needs in and importance of systematics, prepared for a variety of organisations over the past four decades (Anonymous, 1953, 1968; Mayr and Goodwin, 1956; Michener et al, 1956; Steere, 197 1a, 19716; Stuessy and Thompson, 1981; see also Brusca, 1990), all have common themes. Sys- tematics is important, there aren't enough trained systematists, systematics as a discipline ranks somewhere under flatworms in impor- tance, and muscum collections need more sup- port. Yet the situation may be worse today than in 1953. I don’t pretend to have the solution to this MEMOIRS OF THE QUEENSLAND MUSEUM dilemma, but I do know it will take an effort to raise the level of understanding of the fundamen: tal importance of systematics, a much higher level of funding thun is now available for sys- tematics and collections, the development of na- tional and international forms of recognition tor systematic work, 4 cooperative effort by those in ucademia and museums to interest people in systematic fields and to train them, and some long-range planning by museums, planning that includes training and jobs for future generations of systematists, Unless the effort includes creat- ing permanent jabs in systematics, includin many more Support positions, the situation wi not improve. Karl Schmidt (in Anonymous, 1953) made many of the same points in an article published in 1952, and noted that E. Ray Lankester had made them in the 1880s. LITERATURE CITED ABRS. 1990. Australian Biological Resources Study. ABRS Biologue 10: 1-12. ANONYMOUS. 1953, ‘Conference on the impor- tance and needs of systematics in biology, April 22. 1953’. (National Academy of Sciences, National Research Council: Washington, D.C.), S5p. 1968. ‘Systematic biology: 4 survey of federal programs and needs'- (Punel on systematics and Taxonomy, Committee on Environmental Qu- ality, Federal Council on Science and Tech- nology: Washington, D.C.).148p. BLACK, C. et al. 1989." Lass of biological diversity: A global crisis requiring international solutions’. (National Science Board: Washington D.C.). 19p. BRUSCA, R. 1990. Science in the museum, Science and natural history museunts, Part IL. Upstairs 3: 35. MAYR, E., AND GOODWIN, R, 1956, Preserved materials and museum collections. Biological Materials, Part f. National Academy of Sciences ~ National Research Council Pub, 399; 1-20, MICHENER, C.D. er al. 1956. ‘Systematics in sup- port of biological research’. (Division of Bi- ology and Agriculture, National Research Council: Washington, D.C.). 25p. SCHMITT, W.L. 1930. The study of scientific mate- ral in the museum, The Museum News 8(12): 8-10. STEERE, W.C. 1971a. ‘The great collections: (heir nature, importance. condition, and future. The systematic biology collections of the United States: an essential resource, Part 1°. Report to the Nalional Science Foundation by the Confer- TAXONOMY AND MUSEUMS IN THE 1990’S 207 ence of Directors of systematic Collections. (The ‘Trends, priorities and needs in systematic bi- New York Botanical Garden: NewYork). ology’. A report to the systematic biology pro- 1971b. ‘The great collections: statistical informa- gram of N.S.F. (Association of Systematic tion. The systematic biology collections of the Collections: Lawrence, Kansas). United States: an essential resource, Part 2’, WILSON, E.O. 1985. The biological diversity crisis. Report to the National Science Foundation by Bioscience 35: 700-706. the Conference of Directors of systematic Col- 1988. The current state of biological diversity. 3— lections. (The New York Botanical Garden: 18. In E.O. Wilson and F.M. Peter (eds) ‘Biodi- New York). 52p. versity’ (National Academy Press: Washington, STUESSY, T.F. AND THOMPSON, K.S. 1981. D.C.). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum NEW TECHNIQUES TO INVESTIGATE THE. ONTOGENY OF SCALPELLID BARNACLES, AND THEIR PHYLOGENETIC IMPLI- CATIONS Sca}pellid bamacles (Thoracica; Lepadomorpha: Sealpel- lidne) are stalked. with a capitulum bearing more than five calcified or partly calcified plates. They are poorly known and have been rare in museum collections, Species descriptions ate often based on one or few specimens. It is often difficult ta assign species lo many of the proposed scalpellid genera, This paper describes lechniques being developed to provide compre- hensive descriptions of tecent rich Australian collections. As some species are known by only a few Individuals, emphasis has been placed on techniques which minintise (raunta lo the specimen, Conchological techniques, described as destructive, semi-destructive and non-destructive, are used to examine the culcarcous Capilular plates, since the arrangement of these is of systematic, ontogenetic and phylogenetic signilicance, Con- sideration is also given tu Ssidining (echniques, since descrip- tions of morphological details of ttuphi, cieri and camplemental oe dwar males (if present) are Jacking for many species. Conchological Techniques Destructive techtiques, These are the convennonal dissee- ton techniques. In some scalpellid species the capitular plales are covered by or embedded in athick, often opaque membrane, and removal of the membrane andor dissection of the plates is necessary, These destructive techniques may he acceptable if several specimens are available. They are nor suitable Wf only a few specimens exist, of for ontogenctic studies. The inherent possibility exists that plates may be lost inadvertently during dissection and the possibility of damage to fragile plates is also very real, Semi-destructive techniques. A. Bisection of the specinen. followed by back-lighting, provides ay aucurate represenianon of the relative positions of the capitular plates. The success of (his technique depends on the relative thickness of the capitilar plates, their proximity to one another, and the thickness of the investing, membrane, B. Cleared (transparent) and stained specimens are widely used for vertebrate osteolagical studies, Preparation of such specimens involves tissue maceration in alkaline solulans (KOH or NaQH), or ussue digestion by proteolytic enzymes (e.g, irypsin), Bones ate then stained tor maximurt definition and visibility. Thoracicans exhibit shells composed of Cat’Ox, mainly in the form of calcite, with little phosphale or organic maller, The calcareous portion of the thoracican shell appears during metamorphosis of the eyprid larva into the young bumucle. Vertebrate clearing and staining lechniques Were applied, wilh modifications, lo scalpellid specimens, Fresh and newly pre- served material was successfully clearéd tiscd KOH, but the technique can be unpredictable and difficulties. arose with specimens stored in various. preservatives far any length of time, The proteolytic enzyme digestion method was more sliccessful. It was easier 10 prepare small, delicate specimens. and capitular plates were not so easily damaged, distuned wy lost, It was also easier to elear old matenal, although results were not always predictable. However, mutenal properly pre- served prior lo enzyme digestion generally yielded woud Lrans- MEMOIRS OF THE QUEENSLAND MUSEUM parent study Specimens, Enzyme Uigestion is less hurtful i the specimens than alkaline maceration, Maximum sitis- factory enzyme uctivily occurs al pit 7.5 or above. For all except very small specimens we removed the prosoma before processing because this enables the most rapid enzyme digestion to occur and minimises injury to the capitulum, Difficulties encountered using (he enzyme lech- que Are! (1) determination of the length of time for tissue digestion, a8 specimens will fall apart and/or disintegrate if over-exposed, und (ii) the lengit of the tolal process (up to 2 months in endyine solution). The majo’ advantage of the jechWique is a permanent, three-Uimensional record of the capitular plate architecture. Non-destructive techniques. Sealpellid specimens were X-rayed (another vertebrate osteolagical technique) with the assumption that the calcareous capitular plates would be radio-opaque, The technique ts quick, economic and easy to adapi to a variety of sizes of specimens. A permanen| record is obtained of the relative positions of the plates. The tech- nique is excellent for both uniological and comparative siu- dies, An advantage of (he process is that the whole animal may be kepl intuel, which is important when only ane or a fow specimens are known. However, we have found it pref- erable fo use bisected specimens to prevent ‘shadowing! of paired plales an the X-ray image, which can sometimes hinder conchological interpretation, Soft-part Morphology We have adapted methods previously employed by cir- tipede workers. A variety of biological stains were used ta examine external and internal morphological details (fast green, methyl blue, lignin pink, chlorgeol black, solophenyl ble), We obtained excellent results with gain pink and solophenyl blue. Suitably stained material was mounted ia corm syrup diluied 50:50 with distilled water. Conclusion In the Specimens studied consistent morphalogsea) and conchological differences are recognizable between “te major subtamili¢s of the Scalpellidae (seiisu ZeVina, 1981). At the supra-specific level there appear ta be fow gross differences in appendages between species bul difterences in the form of the cupitular platvs ure demonstrable. Criteria for the presently proposed genera need to be more entically defined, especially in the Arcoseslpellinae, with due tegard to ontogenctic variations. in morphology and body anatomy, complemental and dwart Males anatomy, as Well as geographic and bathymeme distributions. Much more sustained, deep-water collecting nocds to be done, nov only in Australia but elsewhere, before a proper understanding of taxonomie variation in the Scalpellidae can be reached, Only then will their phylogeneticevalution be elucidated, Literature Cited Zevins, G.B, 1981. Cirriped crustuceans of the Suborder Lepadomorph (Citripedia. Thoraciea) of the Pacific Goean, Part 1, Family Scalpellidae., Opredelitel) Faune SSSR 127: 1-394, [in Russian, Diana S. Jones, Western Australian Museum, Perth, Wesrerv Australia 6000, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM SYMPATRIC OCCURRENCE OF TWO SUBSPECIES OF PANULIRUS LONGIPES MILNE EDWARDS, 1868 (DECAPODA;: PALINURIDAE) AND BIOCHEMICAL EVIDENCE OF INTERBREEDING Panulirns longipes, acommon trapical lobster in the Inda- ‘West Pacific region belonging to the Japonicus group, wats distinguished by George and Holthius (1905) intn two forms based on the colour pattern of the legs. the “spotted” and ihe ‘sttiped', Furthermore, they suggested that these torms be designated as subspecies, the ‘spotted’ fourm, P. /angisres fongipes, inhabiting the western part of the species range und the ‘striped’ form, P. Jongipes femorisrriga, found im the eastern part. These workers. however, noted that the wa forms could not be sharply separated because intermediate forms With striped and spotted legs occur. This paper reperts the sympatric occurrence of the ‘spotted’ and ‘striped’ forms and the observation of intermediate forms bearing stripes with spots, Using the clecirophorelic methodology, 1 was investigated whether or not the Philippines represenis a tran- sition area where both subspecies intergrade and interbreed, While undertaking research or-some aspects ol the biology of Philippine spiny lobsters, both ‘striped’ and ‘spotted’ forms of P. fongipes were caught in the reefureas around San Vicente. Cagayan (18"30.6"N and 122°08"E) in the north- eastern-most part of Luzon Island, Philippines. comprising 12% and 3% of the landed catch, respectively. Surveys in Guiuan, Eastern Samar (10°44°N and !125'43"B) also re- vealed that both subspecies are sympatric in these areas. The “striped” form, P, fongipes Jemeristriga has not heen reported previously in Philippine waters while P. longipes longipes had been previously reported (rom Zamboanga and Palawan (George and Holihius, 1965). In this swdy, P, longipes longipes was found to be commonly caught from waters off Eastern Samar. Pangasinan, Zambales, Cavite, Batangas, Mindoro, and Cebu. The ‘spotted’ and ‘striped’ forms are morphologically similar in all body characters except for the markings on the legs and on the abdomen. The ‘spotted’ form collected from Rolinao, Pangasinan and Calatagan, Batangas typified that described by Gearge and Holthius (1965). Five white spots are obvious on the dorsal surface of the legs which are situaled al the distal regions of the propodus, carpus and merus with the two remaining spots in the central region of the merus: these spots interrup! an orange longitudinul line, The abdomen is spolted with large white dots. The ‘stnped” form collected from San Vicente, Cagayan has thin. almost continuous longitudinal line on the dorsal surface of the mierus, carpus and propodus; the abdomen is spotted with smaller dots. Intermediate forms collected from San Vicente. Cagayan and Guiuan, Samar exhibiled variable patlern com- binations: clear white spois on the fifth leg anc blotches on the other legs: two longitudinal lines on the dorsal surface of dhe merus and carpus interrupted by white spots: all variable Specimens had large white spots on the abdomen. Electrophoretic analysis af “spotied’ samples trom Boly- nao (n=!6) and Calatspan (n=4) and striped” samples from San Vicente (n=30) showed that al ]4enzyme loci examined, both forms shared alleles in 13 bul diverged in a single locus. glyceraldehyde-3-phosphate dehydrogenase (Gapdh. F.C, 209 No. 1.2.1.12). The ‘spotted’ form displayed a faster fixed allele with @ relative mobility of 150 compared to the ‘striped’ form (rm 125), On the other hand, intermediate torms examined fram San Vicente, Cagayan (n=7) were polymorphic forbath alleles. This divergence even ala single loeus is sufficient evidence of the existence of independent Bene pools (Shaklee ef al., 1982) and therefore they can be tightfully considered subspecies at least, The polymorphism observed in intermediate forms is a sirong indication of interbreeding between the two P, longipes subspecies. In- traspecitic Variations in P. echinatus (Vianna, 1986) con- sisting, of “large-spalied’. ~small-spotied’ and intermediate forms, might be a similar phenomenon, As mentioned earlier, P. longipes femoristriga is reported ta inhabi! the eastern portion. of the species’ range from Japan. the Mollucas. Papua Now Guinea. northeastern Australia 19 Polynesia (George and Halthius, 1965) and (throughout ihe American Samoa, Guam and North Mariana Islands (MacDonald, 1979). Ibis conceivable that larvae from islands in the Central Pacific (e.g. Palau) may be transported by the North Pacific Equatorial Current which branches to the north us the Kuroshio and to the south as the Mindanao current off Luzon at latitude 13-14°N (Nitani, 1970). Con- sidering this, s¥mpalric occurrences and interbreeding of these subspecies may also be the case in other localities parlicularly along the Philippine Pacific coast, Acknowledgements We wish 16 (hank Mr Nemesio Cabutin and his Fishermen, Mx Justierie Melquiades-Granalie, and the personnel of the Bureau of Fisheries and Aquatic Resources who rendered assistance in collecting the lubsler samples. Literature Cited George, RW. and Holihius, L.B. 1965. A revision of the Indo-Wesi Pacific spiny lobsters of the Panulirus japan cus group. Zoologische Verhandelingen, Leiden 72: 1-36. MacDonald, C.D. 1979. Management aspects of the spiny lobster, ?. marginatus, P. penicillatus, P, versicolor, and P. longipes femoristriga in Hawaii and the Western Pacific, Western Pacific Regional Fisheries Manage- ment Commission, Hawaii, Terminal Report. 46p, Nitani, H. 1970, Oceanographic conditions in the sea east of the Philippines and Luzon Strait in summers 1965 and 1966, 213-251. In J.C. Marr (ed.) *The Kuroshio’. (Fast- West Center Press: Honolulu). Shakice, J.8,, Tamaru, C.S., and Waples, R.S. 1982. Specia» lion and evolution of marine fishes studied by the etec- irophoretic analysis of proteins. Pacific Science 36: 141-157, Vianna, ML. $986. On the ecology and intraspecific vana- tion in the spiny Jobster, Panulirwy eckinates Smith, 1800, (Decapoda, Palinundac) from Brazil. Crustaceans S50 25-36 Antoinette R, Juinia, Julie M. Macaranas, and Edgardo D. Gamez, Marine Setence Institute Box 6, University of the Philippines, Diliman, Quezon Ciny 71101, Philippines. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum GENETIC POPULATION SUBDIVISION IN THE COCONUT CRAB, BIRGLS LATRO {ANOMURA: COENOBITIDAE) The coconut crab (Birgus Jatra), the largest and most terrestrial land crab. is found only on relatively isolated tropical islands in the Indian and Pacific Oceans, In recent years, Birgus populations have declined rapidly or disap- peared in most parts of their range, due largely ta over- harvesting for food, It is clear that a management program Is required to protect the future survival of individual popula- tions of this species. Information about population structur- ing within the species is crucial to the development of a suitable management program, This project is using genetic techniques to study the population structure of Birgus throughout its distribution to determine if distinct sub-popu- lations exist and, if so, the location of their boundaries (Lavery ecal., in press), Allozyme electrophoresis was. used (0 examine over 300 specimens of Birgus from eight locations: Christmas Island (Indian Ocean), the Salomon Islands. Nive, the Cook Islands and four jslands in Vanuatu (Tegua, Hiu, Loh and Espiritu Santo). Initially 76 enzyme systems were screened for genetic variation, resulting in the detection af $4 monomor- phic loci and 7 polymorphic loci. These polymorphic Tuci were analysed for allele frequency differences between loca- lions using contingency chi-square analyses. Analyses were performed al different levels of the sampling hierarchy. Al the lowest level of the hierarchy, between adjacent islands (the Torres Islands in Vanuatu: Tegua, Hiu and Loh), no significant difference in allele frequencies was found. Simi- larly, no significant differences were found al the next two levels of the sampling hierarchy, i.e. between islands in a group (the Toftes Islands and Espinitu Santo m Vanuatu) and between adjacent island groups (Vanuatu and the Solamon tslands). However, when all the Pacific Ocean samples were compared, there was significant variation in allele trequen- cies (P<0.01), with individuals from Nive being most vanant. Finally. a comparison of samples from the Pacific with those from Christmas Island showed highly significant genetic differences (P<0.001), A good summary of the genetic differences between loca- lions is Shown in a dendrogram of genetic distances (Fig. 1), This clearly shows that all the islands in the Vanuatu and Solomon Islands groups are quile similar. The Cook Islands and, in particular, Niue, are somewhat different from the Vanyartu/Solomon Islands group, but this level of dillerentia- tion is much smaller than that with Christmas Island, The population genetic structure of Birgus is also being analysed using mitochondrial DNA (mtDNA) variation. Sa far, the mtDNA of approximately 50 individuals from four locations (Christmas Island, the Philippines, the Solomon Islands and Niue) has been analysed using 9 different restric- lion enzymes. Preliminary analysis shows that aver 20 differ- MEMOIRS OF THE QUEENSLAND MUSEUM CHMATMAN F SOLOMONS Alu TEGUA santo On cooK |S MWe ae id og Rogers Genetic Distance FIG. 1. Dendrogram of genetic relatedness of Birgus-collec- tions. ent haplotypes exist among these individuals and, signifi- cantly, no haplotype has been found tw occur in more than one location. The phylogeny of these haplotypes also sug- gests that (here exists significant geographic structure in the mtDNA variation. Such information ahoul genetic differ- ene-s between sub-populations may be interpreted in terms of the level af genetic drift or the rates of larval migration between sub-populations. Lising the allozyme data alone, and injerpreting these dala by Slatkin’s private alleles method, a migration rate between Christmas Island and the Solomon Islands of 03 individuals per generation was calculated. As the Birgus generation rime may be 12 years, this would represent a migration of one individual every 40 years. In comparison, the tate of migration berween the Pacific Islands was calculated (o be approximately an order of magnitude less, al 3 individuals per generation, or about one individual every four years, Although this study is not yet complete, the findings so far suggest that significant genetic population subdivision exists in Birguy. This may have important consequences for bath the fulure management of the species and also any. future artificial rearing of the coconut crab. In addition, the pattern of larval dispersal found in Birgus may be closely related to that of other species in this region with planktonic larvae. Acknowledgements This research has been supported by the Australian Centre for International Agricultural Research, Considerable thanks go toall the mdividua!s who have assisted in the difficull task of acquiring specimens. Literature Cited Lavery,'S., Fielder, D.R. and Brown, 1.W. In Press, Popula- tion genetics of the coconut crab Bireus latre. In D. Fielder and I. Brown (eds) ‘Monograph of the coconut erab Birgus larro’. (ACIAR: Canberra). Shane Lavery, Zoolagy Department, University of Queensland, St Lucia, Queensland 4072, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 211 NEW OR RARE CRUSTACEANS FROM FRENCH POLYNESIA (CRUSTACEA: DECAPODA) Since 1974, the F.R,V_ ‘Marara’ has been used by the French Service Mixte de Controle Biologique (SMCB) to carry out a biological survey, throughout the Fishery Conser- vation Zone of French Polynesia, Among the fishing activi- ties, traps are set on the outer slopes of the islands in depths ranging from 100to 1000m. This has led to the discovery and description of several new species of decapod crustaceans, Some rare or recently described species have also been caught. This paper gives a list of the species concerned and the depth distributions of some of them. A list of genera of new species, now under study, is also given to emphasize the richness and high degree of endemicity of this poorly known area. The details of the gear operations and the yields of Pandalidae shrimps are given in Poupin eral, (1990). Results Species Described from the Catches of the ‘Marara” Pandalidae: Plesiontka fennert Crosnier, 1986: Plesionika carsini Crosnier, 1986, Enoplometopidae; Hoplometopus gracilipes De St. Laurent, 1988. Xanthidae: Progeryon mararae Guinot et Richer de Forges, 1981. Goneplacidae: Beuroisia manquenet Guinot et Richer de Forges, 1981; Marhildella maxtma Guinot et Richer de Forges, 1981. Rare or Recently Described Species Pandalidae: Heterocarpus amacula Crosnicr, 1988; Her- erocarpusparvispina de Man, 1917; Heterocarpusensifer A, Milne Edwards, 1881. Homolidae: Hypsophrys personata Guinot et Richer de Forges, 1981; Hypsephrysinflaia Guinot et Richer de Forges, 1981, Leucosiidie: Randallia serenei Richer de Forges, 1983, The depth distributions of the three recently named Herer- ocarpus, formerly tegarded as H. ensifer and H-. ensifer parvispina (Crosnier 1988), are clearly defined and are pre- sented together in Fig. 1. Genera of the New Species, now under Study Pandalidae: Plesionika sp. (three species, Crosnier). Palaemonidae: Periclimenes sp.(Bruce, in press). Enoplometopidae; Enoplometupuy sp. (De St Laurent). Purapaguridae: Trizopagurus sp. (lwo species, Forest). Paguridae: Solilariopdgurus sp. (Forest). Galatheidae: Eumunida sp. (De St Laurent); Munida sp. (two species, De St Laurent). Majidae; Cyrromaia sp, (two species, Guinot et Richer de Forges). beberecor po Mean Inds /Trep 40 60 | FES amgcula parvispina Gh ensifer Vapth Cm) FIG, |. Depth distributions of three close Heterocarpus spp. belonging to the group “ensifer’ (H. parvispina: abundance x 5: H. amacula: abundance x 13). Parthenopidae: Parthenope/Platylambrus sp. (Garth). Grapsidae: Euchirograpsus sp, (Tirkay): Intesius sp. (Guinot and Richer de Forges). Cancridae; Cancer spp, (four species, Davic). Acknowledgements We thank Alain Crosnier of the Muséum National D'His- toire Naturelle, Paris, for his enthusiastic help in sorting and distributing our catches to taxonomists. Literature Cited Crosnier. A, 1988. Sur les Heterocarpus (Crustacea, De- capoda, Pandalidae) du sud-oquest de l’océan Indien. Bulletin Muséum national d'Histoire naturelle, Paris. (4th Ser.) 10 (sect, A n°1); 57-103, Poupin, J., Tamarii, T. and Vandenboomgaerde, A. 1990. Péches profandes aux casiers sur les pentes extermes des iles de Polynésie Francaise (N/O Marara, 1986/1989). Notes et Documents d’ Oceanographic ORSTOM Tahiti 42; 1-100. J. Poupin, SMCB SP 91427, Tahiti. B. Richer de Forges, ORSTOM Nouméa, Nouvelle Calédonie. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 212 PHRONIMIDAE (CRUSTACEA: AMPHIPODA; HYPERIIDEA) OF THE EASTERN PACIFIC A total of 466 samples of phronimids collected from the upper 200m layer of the eastern equatorial Pacific (20°N— 20°S and E of 126°W) and coastal waters of California (33-35°N und E of 122°W) were examined, All species of the Phronimidae were found in the eastern equatorial Pacific where Phronima dunbari Shih (1991) and P. bowmani Shih (1991)(formerly E. Pacific Form of P. stebbingi and P. colletti respectively [Shih, 1969]) dominated, Only P. seden- laria (Forsk&l, 1775), P. atlantica Guerin. 1836, and P. stebbingi Vosseler, 1900, occurred in the coastal waters of California. Thesympatric distibutian of morphologically similar spe- cies pairs (analogous species, Shih, 1986a) is common in the eastern. equatorial Pacific, eg. Phronima stebbingi-P. dun- bariand P. colletti-P. bawmani of the present study, and there are examples of chaetognaths, euphausitds and copepods in the literature. This plankton distribution pattern is probably related to the complex oceanic circulation of the area where six Currents converge ot diverge (Wyrtki, 1967). Eddies from main oceanic currents bring enclosed water from one waler mass to a new environment surrounded by another water mass, The best known examples are cold core tings of the Gulf Stream (The Ring Group, 1981), The entrained plankton population is subjected to continuous decay of the core water duc to increasing dilution by water of the surrounding environment and is under tremendous physiological stress (Boyd et al., 1978: Wiebe and Boyd. 1978). Pupulations of planktonic species are known to be different in genetic structure (Bucklin and Marcus, 1¥Y&5)and to be distributed patchily (Wiebe, 1970). Unusual environ- mental stress may affect the genetic structure of a population: some copepod species in the castern equatorial Pacitic ex- hibithigher genetic heterogeneity than those in the equatorial and tropical central Pacific (Afnas’ yev ef al., 1989), The oceanic condition in the eastern equatorial Pacific, the general knowledge of oceanic eddies, the biology of 4 popu- lation entrained in an eddy, and diversification of genetic structure in planklon, strongly support the hypothesis of planktopatric speciation in marine zooplankton (Shih, 1986): 1. entrained population is subject to a different set of biotic and abiotic stresses; 2. modification of genetic Structure occurs ina segment of the entrained population as a result of adaplalion Lo new environmental stress; 3. successful propa- gation of the genetically modified segment of population leads to formation of a new taxon lollawing ‘succeeding teproductive isolation. Thus planktopatric speciation probably is the answer to why there are so many analogous plankton species in the eastern equatorial Pacific. MEMOIRS OF THE QUEENSLAND MUSEUM Literature Cited Afanas yev. K.1., Flint, M.V. and Fetisoy. A.N. 1989, Popu- lation genetics of two mass species of Pacific Ocean capepods. Oceanology 29; 225-231, Boyd, S.H.. Wiebe, P.H. and Cox, 1.L. 1978. Limits of Nematescelis meaalops in \he northwestern Atlantic in relation to Gulf Stream cold core rings. II. Physiological and biochemical effects of expatrialion. Journal of Marine Research 30; 143-159. Bucklin, A. and Marcus, N.H. 1985, Genetic differentiation of populations of the planktonic copepods Labidacera aestiva. Marine Biology 84: 219-224. Shih, C.-t., 1969. The systematics and biology of the family Phronimidae (Crustacea: Amphipoda). Dana Report 74: 1-100, 1986a. Longitudinal distribution of oceanic calanoids (Crustacea: Copepoda): an example of murine biagea- graphy. In G. Schriever, H.K. Schminke and C.-1. Shih (eds) ‘Proceedings of the Second International Confer- ence on Copepoda’. Syllogeus 58: 105-114. 1986b. Biogeography of oceani¢ zooplankton, In A.C. Pier- rol-Bults, §. van der Spoel, B.J. Zahuranéc and R.K. Johnson (eds) ‘Pelagic biogeography”. Proceedings of un International Conference, the Netherlands, 29 May—5 June 1985. UNESCO Technical Papers in Martine Science 49: 250-253, 1991, Description of twa new species of Phronima Latreille, 1802 (Amphipoda: Hyperiidea) with a key to all species of the genus. Journal of Crustacean Biology 14(2): 322-335, The Ring Group, 1981, Gulf Stream cold-core tings: Their physics, chemisiry and biology. Science 212; 1091- 1110. Wiebe, P.H. 1970. Small-scale spatial distribution in oceanic zooplankton. Limnology and Oceanography 15: 205- 217. Wiebe. P.H. and Boyd §.H. 1978, Limits of Nematascelus meoalapsin the northwestern Atlantic in relation to Gulf Stream cold core rings. |. Horizontal and vertical dis- tribution, Journal of Marine Research 36; 119-142, Wyrtki, K. 1967. Circulation and water masses in the eastern eyualorial Pacific Qeean. International Journal of Oceanology and Linmology 1: 117-147. Chang-tai Shih, Canadian Museum of Nature, P.O. Box 3443, Statien D, Orawa, Ontaria, Canada K1P 6P4, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM CLADISTIC ANALYSIS AND CLASS- IFICATION OF THE GECARCINIDAE (CRUSTACEA: BRACHYURA) The land crabs of the family Gecarcinidae constitute a circumtropical group of eighteen species belonging to the genera Cardisoma Latreille, 1828, Epigrapsus Heller. 1862. Gecarcoidea H. Milne Edwards, 1837, and Gecarcinus Leach, 1814. The main goals of this work were: (1) to provide a phylo- genetic reconstruction for the genera of the Gecarcinidae and the species of Gecarcinus; (2) to use phylogenetic informa- tion to improve the classification of the group, and attempt to clarify the relationships between the families Gecar- cinidae, Grapsidae and the genus Ucides Rathbun, 1897. Sixty-eight morphological characters were selected and analysed. These are available from the author upon request. Six species belonging to different subfamilies of Grapsidae were selected as the out-group. The cladistic analysis was undertaken using the ‘Hennig 86 vers. 1.5° program. Relationships within Gecarcinidae The species of Gecarcinidae probably evolved from an ancestor that had the dactyli of the pereiopods armed with rows of spines; branchial and hepatic regions strongly in- flated, and carapace transversely oval. The cladogram in Fig. 1 shows that the first cladogenetic event split the genus Cardisoma from the group Epigrapsus + Gecarcoidea + Gecarcinus. The majority of the characters analysed are plesiomorphic to Cardisoma, and do not show great morphological modification from the typical Grapsidae facies. Its sister group Epigrapsus + Gecarcoidea + Gecar- cinus exhibit, on the other hand, several synapomorphies concerned with the buccal region. One character however (pterygostomian region densely setose) suggests a conflicting hypothesis for the position of the genus Epigrapsus in the phylogeny, as this character is shared by Cardisoma and Epigrapsus and could be inter- preted as synapomorphic for them. There are however seven other homoplasic characters (shared by the group Epigrapsus + Gecarcoidea + Gecarcinus). Thus, the mote parsimonious hypothesis is that which admits the homoplasy of the densely setose pterygostomian region character. The next cladogenetic event split Epigrapsus from the group Gecarcoidea + Gecarcinus, which have deep modifi- cations in the frontal, orbital, suborbital, pterygostomian, antennal, antennular and abdominal regions. The third cladogenesis split Gecarcoidea and Gecarcinus. CARDISOMA EPIGRAPSUS GECARCOIDEA GECARCINUS \ ‘ \. \ \ \ . ‘ \ \ \ \ FIG. 1, Phylogenetic relationships within Gecarcinidae. 213 subgenus Gecarcinus | malpilensis planatus weilleri lagostoma lateralis quadratus ruricola subgenus Johngarthia FIG. 2. Cladogram illustrating the artificial assemblage (Johngarthia) within the genus Gecarcinus. These two genera remain rather conservative in relation to the changes in the morphology observed during the previous cladogenetic event. The strongest morphological changes occur in the orbital and buccal regions (Fig. 1). Phylogeny of the Genus Gecarcinus and its Implica- tions for the Classification of the Group The species of Gecarcinus probably evolved from an ancestor which had the orbit closed by the intra-orbital spine and the palp of the third maxilliped concealed beneath the maxilliped. Gecarcinus malpilensis proved to be the more external branch of a symmetric cladogram, and was followed in a sequence by G. planatus and the group formed by G weileri + G. lagostoma. The maxillipeds were the principal morpho- logical structures affected during the evolution of these spe- cies/groups. The three last branches of the cladogram in Fig. 2 correspond to G. lateralis; G. quadratus and G. ruricola, which show, beside the modifications to the maxillipeds, strong modifications of the pleopods. Tiirkay (1970) created the subgenus Gecarcinus s.s. (for G. lateralis, G. quadratus and G. ruricola) and Johngarthia (for G. malpilensis, G. palanatus, G. lagostoma and G. weileri). The subgenus Johngarthia from my results, how- ever, appears to be a paraphyletic assemblage which em- braces the four initial branches of an asymmetric cladogram with seven terminal taxa (Fig. 2). Literature Cited Tiirkay, M. 1970. Die Gecarcinidae Amerikas. Mit einem anhang tiber Ucides Rathbun (Crustacea: Decapoda). Senckenbergiana Biologica 51: 333-354. Marcos S. Tavares, Universidade Santa Ursula, Rio de Janiero. Present Address: Laboratoire de Zoologie (Arthropodes), Muséum National d'Histoire Naturelle, 61 Rue de Buffon, 75231 Paris Cedex 05, France. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum INDIVIDUAL RECOGNITION AND SUPPRESSION OF AGGRESSION AGAINST FORMER MATES IN GONODACTYLUS BREDINI (CRUSTACEA: STOMATOPODA) In laboratory tests, gonodactylid stomatopods use in- dividual recognition to mediate intra- and interspecific ag- gression (Caldwell, 1985), Intruders identify the odour of previous opponents and decide whether to fight based on experience with them, However little is known of stoma- topod use of recognition systems in the field. Gonodactylus bredini is a common stomatopod on the Atlantic coast of Panama where this study was conducted. Reproduction is synchronised, Breeding pairs form a few days prior to the full moon, sharing a crevice for several days, Within hours of the female spawning, the male leaves. She remains in the crevice, brooding the eggs and larvae for four weeks until they enter the plankton. Empty cavities are rare and males, after leaving their mates, may have to evict a crevice resident to secure a home (Caldwell, 1986), While searching for a crevice, a male might encounter his former mate and attempt to usurp the breeding crevice. This would jeopardise her offspring, which, in all probability, are also his. Here, I report that formerly mated G. bredini recognise one another and avoid fighting for several days after males leave the breeding crevice and while females are still brooding. Procedures Fifteen G. bredini male-female pairs were collected in the field, placed in artificial cavities of appropriate volume, and housed in individual aquaria. They were checked daily to determine when the female spawned and the male left the crevice, after which time he was placed in a separate con- tainer. Thirteen days later, the female, with her eggs, was placed in a similar crevice in another aquarium. At the same time, a second brooding female, matched for size and egg development, was established in a separate tank in an iden- tical crevice. The next morning, either the paired female’s original mate, or another male matched to his size, was introduced into her aquarium and all agonistic behaviors recorded (Caldwell, 1985). Contests were terminated when one animal avoided the crevice. The next day, the other male was introduced into the paired female’s container and their interaction scored. The paired male was tested against the unfamiliar brooding female on the same day that the paired female was being tested against the unknown male. This comparison was completed for 12 of the 15 pairs. In the other three, the paired males died prior to testing, but their females were compared against unpaired males. Results One or more aggressive acts occurred in only one of the 12 interactions between members of former pairs while ag- gression took place in 17 of 27 interactions between non- pairs (G = 10.9, P<0.001), Contests between non-paired animals escalated rapidly. In 14 of the 17 contests between non-pair members inyolving aggression, the first act (either MEMOIRS OF THE QUEENSLAND MUSEUM by male or female) after the male approached was a threat, lunge or strike. Eight of these contests ultimately escalated with one or both participants delivering potentially damaging strikes, The one aggressive interaction between members of a former pair involved a single lunge-threat by the female and did not escalate to physical contact (G = 7.0, P<0.01). Only one of the previously paired females responded aggressively toward her former mate. When meeting unknown males, this female, plus 2 others, were aggressive (McNemar Test, P>0.1). None of the paired males acted aggressively toward their former mates, but 6 were aggressive to unknown females (McNemar Test, P<0.05). Discussion Reduced aggression between former pair-members de- monstrates that individuals recognise and remember one another for at least two weeks without intervening contact. Competition for cavities and the possibility that males en- counter their former mates while searching for a home have probably shaped this ability. Should a male injure and/or evict his former mate while she is still brooding, the offspring probably would be lost, reducing his fitness as well as hers. Since females occasionally move their eggs to another crev- ice, males must recognise a specific individual and not just the brood chamber. Brooding females appear hesitant to initiate attacks against any intruding male, making it difficult to determine if females recognise their former mates. On the other hand, males did not attack former mates, but attempted to evict other brooding females; demonstrating that it is not simply the presence of eggs that causes a reduction in aggression. When eggs were removed from females and their former mates introduced, there was no aggression. This makes it unlikely that males fail to attack because they recognize the eggs as their own (Caldwell, in prep.). Whether recognition is chemically or visually mediated is unknown, but intense initial bouts of antennulation by males suggest that they are using chemical cues. Acknowledgements Logistical support was provided by the Galeta Marine Laboratory of the Smithsonian Tropical Research Institute. Funding provided by NSF Grant BNS85-17573. Literature Cited Caldwell, R. L. 1985. A test of individual recognition in the stomatopod Gonodactylus festae. Animal Behaviour 33: 101-106. 1986. Withholding information on sexual condition as a com- petitive mechanism, 83-88. In L.C. Drickamer (ed.) ‘Be- havioral ecology and population biology’. (Privat: Toulouse). Roy L. Caldwell, Department of Integrative Biology, University of California, Berkeley, CA, 94720, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum NITROGENOUS EXCRETION IN AQUATIC AND TERRESTRIAL CRUSTACEANS PETER GREENAWAY Greenaway, P, 1991 090): Nitrogenous excretion in aquatic and terrestrial crustaceans. Memoirs of the Queensland Museum 31: 215-227. Brisbane. ISSN 0079-8835. For water-breathing animals the most economical nitrogenous excretory product in enerectic terms isammonia(ium)and thisis generally excreted across the gills. In terrestrial situations most animals produce less toxic materials, notably urea and purines, which are eliminated by the excretory organs. Crustaceans are predominantly an aquatic group and marine and freshwater species conform to the above pattern in excreting ammonia (ium), Most amphibious species generally have frequent recourse lo water and show little change in the basic aquatic pattern of excretion, The small terrestrial forms, notably Amphipoda and lsopoda and the crab Geograpsns grayi, retain ammonia excretion but eliminate it as a gas, The gecarcinid land crabs excrete NHq"* in the urine whilst Birgus latro excretes uric acid in the faeces. Many terrestrial and some aquatic species store purines and may have purine synthetic ability. The role of stored purine is unclear but it may act as a N Tesetve, an jon store or as a non-toxic buffer when normal ammonia excretion is inhibited. Urea is Nol an important excretory product and crustaceans appear to lack a complete urea cycle. Exctetory pallerns are discussed in relation lo the evolutionary history of the group. (] Nitrogenous excretion, Crustacea, ammonia, terresirial Crustacea, uric acid Peter Greenaway, School of Biological Science, University of New South Wales, P.O. Box I, Kensington, New South Wales 2033, Australia; 6 July, 1990, The form in which animals excrete waste nitro- gen and the route, or mechanisms, by which it is eliminated are quite labile, but there arc several underlying factors which strongly affect the mechanism employed, Firstly, metabolism of protein yields ammonia’, typically from trans- amination and deamination reactions, and the metabolically cheapest form of excretion ts am- monia. Secondly, ammonia is toxic to animals, especially higher vertebrates (Campbell, 1973).. although less so to crustaceans which may main- tain ammonia concentrations appreciably higher than in vertebrates (Table 1). Thirdly, NH, is highly diffusible and cannot be contained or concentrated by cells, but in the ionic form il can be concentrated and transported by the usual ion transport mechanisms. In body fluids most am- monia is protonated (NH,*) and within the usual range of pH only around 1% will be present as NH,. Elevated [NH,*] however, leads to eleva- tion of [NH] with resultant toxic effects, so that ammonia concentrations must be kept within a tolerable range. Rapid excretion into Jarge volumes of water avoids any build up in concen- tration, For these reaSons, ammonia excretion is considered to be the preserve of water-breathers ' In this review NH3 tefers to molecular ammonia. NH4* to ammonium ions, and ammonia to the sum af both (=total ammonia). which can economically excrete their waste in the form in which it is produced. Other forms of waste nitrogen are also elimi- nated by animals. chiefly purines and urea, bur these have several selective disadvantages. They are more complex molecules and their synthesis requires energy and also elaborate enzyme sys- tems (Hartenstein, 1968). This extra metabolic cost is only outweighed under conditions con- sidered inudequate for safe excretion of am- monia, i.e, on land, especially in mesic and xeric habitats where water availability is limited. The generalised pattern seen in animals then is as follows: water-breathers are ammonotelic ex- creting NH,/NH,° across suitable surfaces, usu- ally the gills; terrestrial forms (particularly arthropods) excrete purines or, less commonly, urea, and any NH,/NH," excretion is small and is often primarily a function af acid-base regula- tion. The Crustacea are predominantly an aquatic proup with the major radiation in the sea but with a substantial number of species in freshwater and only a few on land. Most species have spent their whole evolutionary history in water and am- monotelism is expected to be the standard pat- tern of excretion, The terrestrial forms would be expected to excrete one of the more complex, less. toxic, compounds, The extent ta which these predictions hold is examined below, Whilst water availability in the habitat is normally an 216 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. The concentration of ammonia in the haemolymph of a range of crustaceans. Ammonia mmol.L! Species 0.39 0.011 NH3 0.82 NH4* Carcinus maenas 0.9 Uca pugilator 20.0 Cardisoma carnifex 1.6 Geograpsus grayi 2-3 Gecarcoidea natalis 2-4 Cherax destructor 0.1 Notostomus gibbosus 217 Porcellio scaber 1.5 Callinectes sapidus Callinectes sapidus over-riding determinant of the excretory mecha- nism employed, there are certain other factors which may be important in determining ex- cretory rates and patterns in Crustacea. These include the moult (at which time there is consid- erable catabolic and anabolic activity involving proteins), the nitrogen content of the diet and metabolic rate (including effects of temperature and season). Additionally, where ammonium is excreted in exchange for cations in the water the salinity of the latter may be important as osmoregulatory requirements may conflict with those for nitrogenous excretion. This may affect migratory species such as Eriocheir sinensis and prawns as well as species subject to fluctuating salinities (Regnault, 1987). The taxonomic in- heritance in terms of available metabolic path- ways and the length of time a species has spent in a particular habitat can also exert a major influence. This review is directed towards the effects of adaptation to terrestrial habitats on excretory mechanisms. EXCRETION IN AQUATIC HABITATS The formation, detoxification and elimination of ammonia by aquatic crustaceans has been the subject of several recent reviews (Kormanik and Cameron, 1981a; Evans and Cameron, 1986; Regnault, 1987) and whilst the subject is far from being totally understood available data are well documented. In consequence, nitrogenous ex- cretion in aquatic crustaceans will be reviewed to provide a basis for the logical treatment of terrestrial groups. Cameron and Batterton (1978) Kormanik and Cameron (1981b) Binns (1969) Green et al, (1959) Wood et al. (1986) Greenaway and Nakamura (in press) Greenaway and Nakamura (in press) Fellows and Hird (1979) Sanders and Childress (1988) Wieser and Schweizer (1972) AMMONIA FORMATION Ammonia for excretion originates overwhelm- ingly from the catabolism of amino acids but minor amounts will result from the degradation of purines, pyrimidines, and urea of which the latter may originate from a high intake of ar- ginine (Fig. 1). Before the carbon skeleton of an amino acid can be utilised in the citric acid cycle its amino group must first be removed. Most commonly this is achieved by transamination, the transfer of the nitrogen containing a-amino group to an a-keto acid. The general reaction is as follows amino acid L-a-amino + a-ketogluterate < >a-keto acid + L-glutamate transaminase These reactions do not release ammonia but pass it on to an a-keto acid to form L-glutamate. Certain amino acids possess other N groups and these may be removed by deamination followed by transamination of the amino nitrogen e.g. the amide groups of asparagine and glutamine. asparaginase Asparagine + H2O > Aspartate + NH3 glutaminase Glutamine + H20 >L-glutamate + NHa These pathways are believed to be utilised in some crustaceans (Krishnamoorthy and Srihari, 1973; King et al., 1985). Despite some contro- versy it is clear that glutamate itself can undergo oxidative deamination in crustaceans (Chaplin et NITROGENOUS EXCRETION Aapiraypine Aral vetdy Aa Garden amp Porthe | Synthesis Advoosine = Gianavioe t yad Inpelne Coamardines b-wlatumale Hyposanihine we, Urle acid Albanian Alanine weal Ure 4 \ | vitirew eyele FIG. 1. Metabolic pathways producing ammonta in cTustaceans., Arginine Pyrimidines NMG al., 1965; Bidigare and King, 1981; Batrel and Regnault, 1965; Regnault and Batrel, 1987). GDH : L-glutamate +H20 < ==> o-ketoglutaraie + NHy Indeed as glutamate is the only amino acid from which the a-amino group can rapidly be removed to release ammonia and the enzyme, glutamate dehydrogenase is very important in ammoniogenesis. In many animals, the direction of the reaction is determined by the co-factor so that oxidative deamination (NH, release) is stimulated by NAD* whilst the reducing reaction (NH, uptake) requires NADPH (Lehninger, 1982). GDH Hi0+L-glutamate+NAD < > NHj+ NADH +H o-ketoglutarate GDH o-ketoglulursie + NADPH +H + NHI In crustaceans the relative concentration of NAD* and NADH, and substrate concentrations may determine whether formation or deamina- tion of glutamate occurs (Batrel and Regnault, 1985; Regnault and Batrel, 1987). In most cases N is transferred to glutamate and its oxidative deamination will release ammonia into the cell, Ammonia may also be generated by cata- > NADP + 1.0 + L-glulamate 217 bolism of other nitrogenous compounds. Thus purine and pyrimidine nucleotides may be broken down to yield ammonia (Fig. 1), although the amounts involved are likely to be very small given the presence of scavenging pathways. Di- etary intake of these components may necessi- late some nitrogenous excretion, depending on the animal's requirements. In actively working skeletal muscle, the deamination of AMP results in ammonia production. Whilst AMP-deaminase has been identified in certain crustaceans its function is yet ta be established (Regnault, 1987) and the importance of the pathway in overall ammonia production in crustaceans is unknown. All these pathways lead to utic acid which may then be excreted as urate, stored or degraded to urea OF ammonia. Ammonia may also be produced from urea via urease, but as a complete synthetic pathway for urea is lacking in the crustaceans examined (Har- tenstein, 1970; Claybrook, 1983; Regnault, 1987) available urea is likely to be restricted to that produced from dietary arginine via arginase which is present in the midgut gland and gills of many crustaceans. arginase Arginine + H20 urea + ornithine Arginine is an essential amino acid in crustaceans that have been investigated (Zandee, 1966; Claybrook, 1983) so that urea from this source represents a dietary excess rather than a controllable form of N excretion. Urea will also be formed as an intermediary compound in uri- colysis. Thus the possible generation of am- monia from urea is small, AMMONIA DETOXIFICATION In aquatic Crustacea, the major site of excre- tion is the gills (Kormanik and Cameron, 1981; Evans and Cameron, 1986) so the ammonia gen- erated in metabolising cells must be transported there for elimination. As the concentration of ammonia in haemolymph is high (Table 1), con- siderable amounts may be carried in this form. However, if production was high or excretion was discontinuous, a non-toxic molecule would be necessary for transport or temporary storage of nitrogenous Waste. The obvious candidates are glutamate, the end product of transamination reactions, and glutamine which offers the advan- tages both of readily crossing cell membranes and of doubling the amount of NH, carried. In vertebrates, glutamine synthetase forms glu- Oe ee Se — ee see ee LD i cient Nal —_— ol naan _ 3) te Made pludanate | METATINDISIAG FT RLES He LETTE nt HOTT E TARTU Pen ' ROPER! fF gta annpere huranine ullis warra FIG. 2. A pathway for ammonia detoxification and transport m aquatic crustaceans (aller King ef al. 1985). ‘amine in the peripheral tissues and in this {orm waste is transported to the site of elimination (liver). There is evidence for a similar glutamine detoxificatlon pathway in the crabs Cancer and Carcinus (Fig. 2) (King ct a/., 1985), High levels of glutaminase in the gills of these crabs are presumed to release NH,” [rom glutamine for elimination whilst at the site of ammonia genera- tion (muscle), the levels of glutamine synthetase and glutamate dehydrogenase are high. Glu- tamine also appears to be an important vehicle for ammonia transport in Paratelphusa hy- drodromous in freshwater (Krishnamoorthy and Srihari, 1973). This pattern does not hold forall crustaceans, however, as King et al, (1985) found hitle evidence to indicate glutamine detoxification in cither Hamarus or Pandalus. Evidence favours GDH as the controlling step in ammonia excretion (summarised in King er al., 1985), The formation of alanine as a detoxification and transport molecule is also possible as crustaceans possess the necessary enzyme (alanine transaminase) and indeed show high levels of alanine synthesis in vive (Claybrook, 1983). There is at present no specific evidence indicating its general use for detoxifica- lion/transport purposes in crustaceans although it is important in vertebrates (Lehninger, 1982), Serine has been implicated as the main route of detoxification in the crayfish Cherax destructor (Fellows and Hird, 1979) and a serine cycle has been suggested in other animals (Bishop, 1976). Other major routes of detoxification com- MEMOIRS OF THE QUEENSLAND MUSEUM monly seen in animals are de novo synthesis of purines and urea production. As the crustaceans Jo nol appear to possess a functional urea cycle (Claybrook, 1983), synthesis of this compound from ammonia is unlikely. Although many crus-: taceans show periodically high levels of urea in the haemolymph (up to 28 mmol/L in Holthui- sana transversa, P, Greenaway, unpublished) and excrete some urea, it is generally a minor component of total output. The ability to synthe- sise purines de nova is also thought to be lacking in aquatic crustaccans. The midgut gland 1s re- ported ta form and excrete spherules of uric acid in several species of aquatic decapods (Fischer, 1926), The small amounts of uric acid excreted or stored are generally thought to be derived from purine catabolism rather than synthesis but this may need to be examined more closely. ELIMINATION OF WASTE NITROGEN AQUATIC CRUSTACEANS There is conclusive evidence from whole ani- mal studies that ammonia is the chief excretory product of aquatic crustaceans and that the site of excretion is the gills. Gills provide a large and well ventilated surface and the respired water carries. away excreted ammonia, preventing development of gradients adverse to excretion, Waste nitrogen may arrive at the gills as am- monia (usually 99% NH,” and 1% NH,) or in detoxified forms such as glutamine and perhaps other amino acids (see above). The processes by which ammonia is excreted have altracted considerable attention, although much of it has been concerned with osmoregula- tory mechanisms rather than excretion (Evans and Cameron, 1986; Schoffeniels, 1976). Whilst the possible mechanisms of elimination of am- monia are now fairly clear, the actual mecha- nisms used by particular species are seldom so. itis often extremely difficult technically to dis- tinguish between potential excretory mecha- nisms, and it is frequently unclear whether apparent mechanisms are primarily osmoregula- tory or excretory in function as the two systems may be closely linked. Available data for crusta- ceans are often fragmentary and patterns gener- ally have to be constructed from inadequate data by comparison with better understood mecha- nisms in fish. Potential mechanisms of excretion are presented in Fig, 3 and discussed below. The high diffusibility of NH, allows loss to the water by diffusion down its partial pressure gradient cither through or between the epithelial NITROGENOUS EXCRETION Haemolymph Gill Ex Epithelium NU, NAy—=Ni,! he (dutamine wenn! Sertoy fg ene: 2nd cn an a a FIG. 3. Diagram summarising possible mechanisms pf ammonia elimination in aquatic crustaceans, cells. The driving gradient will be small as NH, forms only a small portion of total ammonia in the haemolymph (Kormanik and Cameron, 1981a). Only a small proportion of waste is likely to be lost in this way unless the gradient can be increased locally by active means (see below), Nevertheless, diffusive loss appears. to be the major mechanism in the crab Callinectes sapidus in seawater (Kormanik and Cameron, 1981b). Ammonium ions may also be lost directly from the haemolymph by diffusion down their electro- chemical gradient. Passive, transmembrane dif- fusion may be impeded by the electrical charge of the ion and the pathway taken is probably paracellular, i.e. through intercellular channels and the apical junctions (Kormanik and Cameron, 1981a). There is no information on the importance of this route in crustaceans but it is likely to be minor, As passive loss. of ammonia seems to explain only a small portion of the total excretion of ammonia, the bulk must involve an active com- ponent of transport either into or out of the epidermal cell. Entry into the epithelial cells of the gill could be as NH;, NH,", or detoxified ammonia (amino acids). The neutral amino acids (glutamine particularly, serine and alanine if used) would cross. the cell membrane readily bul the negatively charged glutamate may require a 219 I ’ + “Mediu (Tansport mechanism. Ammonia could then be generated by removal of the amide N of glu- tamine, deamination of serine and transamina- tion of other amino acids. NH,” could be transported directly into the cell by Na/K acti- vated ATPase with NH,* substituting for K~ (Towle and Holleland, 1987). NH, could enter by diffusion if the gradient were suitable but with active generation of ammonia in the gill epithelium the gradient may well be adverse. The next step is the elimination of ammonia from the gill epithelial cells. The mechanisms proposed to account for this rely on amiloride sensitive entry into the cell of Na* fram the water via Sodium channels in the apical membrane (Kirschner, 1983). This is thought to create a potential gradient which favours efflux of either NH,* or H’, again through apical ion-selective channels or antiport mechanisms (Fig. 3) and results i in a coupled 1:1 exchange of Na* with NH,” or H*. The ultimate driving force is the operation of basolaterally located Na/K ATPase (Towle and Kays, 1986) which maintains a low intracellular [Na] which allows continued apical influx of Na. Where Na*/NH,* exchange occurs, the ammonia would be eliminated directly. Inthe case of Na‘/H* exchange the loss of protons would 1 encourage the dissociation of NH,’ yield- ing H* and NH, and the latter would be lost to the water down its partial pressure gradient (Fig. 3). If osmoregulatory requirements for uptake of Na* exceeded the supply of H* excretory am- monia, additional protons could be provided from bicarbonate via the activity of carbonic anhydrase. There is evidence for Na’/NH,* exchange (but nat for Na*/H*) in the marine crabs Cancer and Petrolisthes although it docs not account for all the ammonia ¢xereted (Hunter and Kirschner, 1986). In Uca tangeri, there is evidence for an apical H* pump (Krippeit-Drews ev al., 1989) whilst Bigalke (1986) has demonstrated a Na‘/H* exchanger in Eriecheir sinensis, A Na*/NH,” exchange has also been suggested in freshwater crayfish (Shaw, 1960). In Eriocheir sinensis, & small component of sodium influx apparently exchanges for NH, (Gilles and Pequeux, 1986) butin the absence of whole body flux data for Na* and NH," it is not clear what proportion of total N excretion this could repre- sent, [f nitrogenous excretion is normally much lower than Na influx perhaps all N could exit by this mechanism. In seawater-adapted E. sinensis, howewer, sodium influx was absent, so that am- monia in seawater animals must have been elim- 221) MEM@IRS OF THE QUEENSLAND MUSEUM inated by other means (Gilles and Pequeux, 1986), presumably diffusion. In Callinectes sapidus, here isno evidence of Na*/H* coupling (Pressley efa/., 1981) and ammonia efflux is also insensitive to amiloride indicating a lack of Na*/NH,° coupling (Kormanik and Cameron, T9B1b), It is suggested thal ammonia outpul in lhis species is by diffusion of NH,. There are then, numerous possible routes by which waste ammonia can be removed, and con- siderable variability in the way these routes are actually used by particular crustaceans or even within a single species under different condi- lions. The osmoregulatory requirements for Na* transport may well determine which pathways are used and, in curyhaline species, salinity may determine which is used at.a particular time. A probable pattern for freshwater crustaceans is described ubove utilising electrical coupling of Na* and H*, but in marine crustaceans where there is no osmoregulatory requirement for Na® a different pattern might be expected, OTHER FORMS OF EXCRETION Although ammonia is the dominant excretory product there are some data indicating low levels of excretion of other materials by aquatic Crustacea. Thus uric acid spherules are formed in cells of the midgut gland and excreted into the gui lumen in several species of crabs, the anomuran Percellena and in Panulirus (Fischer, 1926), In Callinectes sapidus exposed to low temperature and salinity, crystals of uric acid appear in the cells and lumina of the labyrinth and bladder of the exeretory organs (Johnson, 1980), Whether this uric acid is derived from an excess of other purines or synthesised by the animals is unknown. Urea appears to be produced in response to elevated salinity in some crustaceans (Sharma, 1966, 1968, 1969; Krishnamoorthy and Srilvari, 1973) und Horne (1968) has suggested that Car- disama guanhumé may excrete urea, Further stu- dies are required on the metabolic capabilities of jhese animals. TERRESTRIAL CRUSTACEA In ferresitial arthropods the major excretory products are purines and clearly \here has been strong selective pressure for purinotelism in the terrestrial habitats. {t might be expected that the {erresttial crustaceans would conform to this pat- tern but the limited information available indi- cales thal thts is nol generally the case. ISOPODA The isopods are the most successful of the terrestrial crustaceans with approximately 1000 species ranging {rom supralittoral to desert hab- itats. Like their aquatic relatives, they are pri- marily ammonotelic but with the important difference that much of the ammonia excreted is in gaseous form (Dresel and Moyle, 1950; Har- tenslein, 1968; Wieser et al, 1969; Wieser and Schweizer, 1970; Wieser, 1972b). Surprisingly, there have been no comprehensive investiga- tions either on the partitioning of excretion be- tween the possible routes or the proportions of various compounds eliminated by cach route. Dresel and Moyle (1950) partitioned faecal non- protein nitrogen in several species. Ammonia was the main nitrogenous product, uric acid made up 5-10%, amino acids 1-6% with anly traces Of urea, Faecal ammonia in Percellio scaber, however, comprises only 10% of total ammonia excretion, the other 90% being re- leased as a gas (Wieser and Schweizer, 1970). No data are available either for the urinary flow rate nor the concentration of nitrogenous ex- eretory products of urine. Nevertheless, the over- all dominance of gaseous NH, excretion is clear, Interestingly, excretion of NH, is nol continu- ous but varies diurnally with peak excretion coinciding with periods of minimal activity. It is argued that this allows excretion whilst the ani- mal is resting in a moist microclimate thus min- imising water loss during volatilization of NH, (Wieser ef al., 1969; Wieser, 19725), This diur- nal pattern of excretion may be endogenous in isopods as itisalso seen in aquatic species (Kirby and Harbaugh, 1974), Excretion in terrestrial isopods also shows scasonal patierns and is af- fected hy (emperature, presumably via the effect on general metabolism (Wieser ef al., 1969; Wieser, 1972a, b). Although it has been known for 40 years that volatilisation of NH, is the principal method of nilrogenous excretion in terrestrial isopods. the exact nature of the mechanism involved remains obscure. Given that excretion of NH, is not continuous, storage of ammonia between peri- ods of elimination must occur and some method of detoxification of ammonia is indicated, How- ever, dala for routine levels of ammonia (e¢. 15 mmol.L7) andamino acids (¢. 2 mmol,L') iy the haemolymph are available only for P, seaber, While ammonia concentrations of 1-17 mmol.L and glutamate and glutamine of 6-7 mmol-L* are reported in homogenates of the body wall of P. scaber (Wiescr and Schweizer, 1972), Infor- NITROGENOUS EXCRETION a2) mation on detoxification mechanisms is lacking for terrestrial isopods but the presence of glu- famine and glulaminase in the body wall ol P. seaber indicates # capacity for generation of ammonia from glutamine at this site (Wieser. 1972c; Wieser and Schweizer, 1972). Thus glu- tamine may be involved in ammonia detoxifica- tion and transport as indeed may other mechanisms suggested above for aquatic crusta- ecans. Further investigations are nceded on this matter, Hartenstein (1968, 1970) provided some evidence for oxidative deamination in Oniseus asellus but.amino-oxidase activity was concen- trated in the hepatopancreas which ts not suitably located for volatilisation of resultant NEL, As ammonia generated will be largely iomsed at normal pH levels, the next mater for con- sideration is its conyersion to NH. One possi- bility is that NH, is generated in the tissues, at the point of climination, by local alkalinisation and the NH, diffuses out into the air down its partial pressure gradient. Alternatively, NH,” may be eliminated into urine in the excretory organs or across the body wall into fluid (urine or pleopod fluid) which is then made alkaline {Wieser, 1972b) forming NH, which is lost to the air. This could be achieved by reabsorption of protons, This would presumably require ion {ransport across. the epidermis lining the chan- nels. although it could also occur across. the pleopods which have an appropriate ion-trans- porting epithelium (Kuemmel, 1981), A potential mechanism for production of gascous NH, which utilises the latler form of elimination was suggested by Hoese (1981). The terrestrial isopods possess a network of water- conducting channels which carry urine, Urine released into this system, from the miaxilliary glands, flows along the channels on the dorsal and ventral surfaces and over the pleopous before being re-ingesled af the anus (Hoese, 1981, 1982) and it was suggested that volatilisa- tion of NH, would be effected during this circu- lation, If release of urine occurred during periods of inactivity in retreats, water loss from the sys- tem by spillage and evaporation would be mini- mised, This hypothesis is based on observations of micro-anatomy and fluid Now and requires physiological evidence to substantiate it, Thus i} must be shown that the urine released contains adequate amounts of NH," to explain measured rates of NH, release. Secondly, it must be de- monstrated that the {uid in the channels actually becomes alkaline as gaseous NH, cannot be re- leased otherwise. The jerrestrial isopods examined all have deposits of uric acid in the body (Dresel and Mayle, 1950), There are no specific issues im which this is located, as in the freshwarer Aselles (Lockwood, 1959), and in Onisews aselles deposits are reported as being located in the ‘body wall’ (Hartenstein, 1968). The highest level reported is in Armadi/lidium (c, Sumal.e! wel weight) whilst levels in QO. asellus and P. scaber are almost an order of magnitude lower (Drescl und Moyle, 1950; Hartenstein, 1968). Et is nol clear whether these deposits represent excess dietary intake of purines or if they have been synthesised de novo but there are no data suggesting the presence of synthetic pathways and Hartenstein (1968) considered synthesis an- likely. As uricolytic enzymes are present in OQ. asellus (Hartenstein, 1968) storage of uric acid cannot be considered obligatory and must per- form some useful metabolic role. AMPHIPODA There are numerous species of terrestrial am- phipods. in the Family Talitridae. ranging from supra-littoral to fully terrestrial, The latter are best represented in the Southern Hemisphere. particularly Australia and New Zealand (Hurley, 1968) where they are extremely abundant in forest and grassland habitats well mland. Know!l- edge of their nitrogenous excretion is pour. Ly the supra-littoral Grchresta, ammonia makes up the major portion of faecal non-protein nitrogen (Dresel and Moyle. 1950) bat it is not known What portion of Latal nitragea excretion this rep- resents. Neither ts it clear from this work if Orchesiia excretes gaseous NFL,, Further work is necded on this group, particularly on the ter- resirial species, In the freshwater cave dweller Niphargus, spherules of uric acid are Stored in special cells on the pericardial septum where the urates bind a variely of anions and cations (Graf and Mi- chaut, 1975). These are considered to be reserves of purine and ions for metabolic usage rather than deposits of waste nitrogen derived trom protein cajabolism {Graf and Michaut, 1975)- Data are lacking for terrestrial species. ANOMURA The Anomura are represented on land by the Coenobitidae, and include the Robber Crab, Bir- gus latro, and twelve species of shell-carrying hermit crabs. Coenobia, some of which nccupy supra-littoral niches whilst others. range inka (Hartnoll, 1988), Nitrogenous excretion hats ho MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 2. The chief excretory products and their routes of excretion in Gecarcaidea natalis, Geograpsus grayi and Birgus latro. % Total N output Gecarcoidea natalis Faeces P Gas Total Geograpsus grayi Faeces P Gas Total Birgus latro Faeces P Gas Total 96.2 0.0012 3.5 been studied only in B. Jairo (Greenaway and Morris, 1989), B. latro is uricotelic and solid uric acid, ex- creted in the faeces, comprises about 50% of total non-protein nitrogenous excretory waste. The remaining faecal excretory nitrogen is largely ammonium (11.9%) with some free amino acids and urea (Greenaway and Morris, 1989). Loss of nitrogen in the excretory fluid or as gaseous NH, is insignificant (Table 1). Uric acid appears as separate white portions of the faecal string, quite separate from the brown faeces comprised of food residues. Excretion is episodic with uric acid released into the gut in distinct bouts of excretion. Homogenates of the midgut gland contain xanthine oxidase, the enzyme responsible for the final step in the con- version of purine bases to uric acid and the midgut is presumed to be the active site in the final stage of uric acid production. &. faire can synthesise purines de novo but nothing is known of the metabolic pathways concerned. Starved B. fatro excrete uric acid at an un- diminished rate and may metabolise protein during inanition. The observed output could also result from excretion of uric acid stored within the body (see below). Large amounts of uric acid are stored by B. latro patticularly in laboratory-maintained ani- mals (Greenaway and Morris, 1989). Extensive white deposits occur in all tissues but it is not clear whether the urate is free in the haemocoel, % N Output as Ammonia % ™ Output as Uric acid or is contained in special ‘urate’ cells as de- scribed for the amphipod Niphargus (Graf and Michaut, 1975). White deposits have also been observed in Coenobita brevimanus (P. Greena- way, unpubl. obs.). The functional significance of urate reserves is unknown but, given that B. latro can excrete utic acid, their maintenance must perform some useful metabolic role. This may be to act as a mobilisable nitrogen reserve for synthesis of amino acids or perhaps as an ion store prior to ecdysis or modulation of haemolymph ions during dehydration. BRACHYURA The land crabs are drawn from some 16 differ- ent families and range from amphibious to highly terrestrial in habit (Bowman and Abele, 1982; Hartnoll, 1988). GECARCINIDAB. Early work on Cardisoma guanhumi discounted the urine as a significant vehicle for excretion (Horne, 1968; Gifford, 1968). Subsequent work has confirmed low uri- nary nitrogen concentrations (Wolcott and Wolcott, 1987a; Wolcott D.L., pers. comm.; Greenaway and Nakamura, in press) but this has little relevance to excretion as urine in land crabs is not the final excretory fluid and 1s passed into the branchial chambers. Here it may be exten- sively modified before being released as a final excretory fluid (P) (Wolcott and Wolcott, 1984, 1985; Greenaway et al., 1990) in which [NH,*] is considerably elevated (Wolcott and Wolcott, NITROGENOUS EXCRETION 1987b; Greenaway and Nakamura, in press), This NH,” must be added to the urine during its residence in the branchial chambers, presumably via the gills but the mechanism is unknown, Anv of the mechanisms described above for aquatic crustaceans could be utilised with the urine pro- viding ions for exchange (Fig. 4). The maximum [NH,*] recorded in P of G. natalis was 73 mmol.L!, but the average was much lower ate, 1] mmol.L! (Greenaway and Nakamura. in press) and similar values are reported for other gecarcinids (Wolcott, D,L., pers, comm), In Gecarcoidea naralis, the chief excretory product is ammonia which makes up 92% of the non-protein nitrogen excreted. Thisiseliminated largely in the exeretory fluid (70%) and the remainder exits a8 gaseous NH, and faecal nilro- gen (Greenaway and Nakamura, in press; Table 2). The small amount of excretion of gaseous NH, (Table 2) may well have originated from faeces and/or P by direct volatilisation. No sig- nificant excretion of gaseous NH, was reported from C. cariifex (Wood and Boutilier, 1985) and while Horne (1968) reported considerable gaseous excretion by C. guan/numi no supparting data were offered. Routine excretion in gecarcinids is as NH,” in the final excretory fluid. Total nitrogen excretion is relatively low (Horne, 1968; Gifford, 1968: Wolcott and Wolcott, 1987b; Greenaway and Nakamura, in press) and the [NH,"] of P is normally low enough lo avoid toxicity problems although blood levels are quite high (Table 1). All species. of gecarcinids studied contain deposits of uric acid (Gifford, 1968; Wood and Randall, 1981; Greenaway and Nakamura, in press), Amounts are very variable but appear to be related to diet and accumulation is greatest in laboratory specimens (Wolcott and Wolcott, 1987b). Gifford (1968) considered that uric acid deposits exist free in the haemocuvel but histo- logical evidence forthis is fucking. The origin of the deposits is unclear but it is unlikely that they are derived solely from excess dietary purine compounds and de nove synthesis must be a possibility. As with Birgus faire some useful metabolic function of the reserves must be as- sumed as most crustaceans possess urpoolylic enzymes and could degrade the deposits and excrete ammonia, GRAPSIDAE. The only other land crab in which nitrogenous excretion has been studied is Gee- grapsus grayi, @ small Carnivorous species with a relatively high tate of nitrogenous excretion (¢. 100 umot-ke'. bh!) (Greenaway and Nakamura, in press). G, gray7 is also ammonotelic but differs from the gecarcinids in excreting most of its waste nitrogen as gascous NH, (Table 2). Re- lease of gas is not continuous and the crab alter- nates between bouts of excretion lasting several days and similar periods of minimal excretion. It is probable that protein catabolism ts ongoing so ammonia must be detoxified and temporarily stored between bouts of exeretory activily. Possible metabolic pathways were outlined above. Exeretion of gaseous NH, by starved animals is similar to that of fed crabs indicating continued catabolism of protein during starva- tion (Greenaway and Nakamura, in press). Elimination of NH, probably occurs in the branchial chambers where the gills provide a large surface area of epithelium with an ultra- Structure suiled for ion transport (Greenaway and Farrelly, 1990) and the urine again could provide a source of ions to fuel any exchange processes which may be involved. Ammonia could be lost directly in gaseous form ar passed into the P as NH,° and lost as NH, following alkalinisation. The possibility af conflicts between ion regu- latory requirements and nitrogen excretion should be considered in brachyurans. The mech- anisms of elimination of ammonia described above (Fig. 4), depend on activity of basolateral Na/K-ATPase and the entry of sodium ions from the fluid bathing the gills (in this case urine), In salt replete animals, sodium is not reabsorbed from the urine (Walcott and Wolcott, 1985; Tay- lor, Greenaway and Morris, unpubl. data) and this could block ammonia excretion, Greatest difficulty would be experienced by animals on a diet rich in both salt and nitrogen, Dehydration, too, could cause exeretory problems as reduction and cessation of flow of excretory fluid would first elevate [NH,”], perhaps ta toxic levels, and finally eliminate excretion. Such reduction in urine flow occurs during desiccation in the ge- carcinids (Kormanik and Harris, 1981). In Car- disoma carnifex, ammonia excretion ceases during desiccation but is elevated on rehydration sugpesting interim storage in non-toxic form (Wood et al., 1986). Uric acid, amino acids or protein could be utilised for this purpose, These problents could also occur in isopods ifexcretion relies on ammonium being excreted into the urine or across the gills into a urine or water film. ASTACIDEA There are numerous species of senti-lerresirial freshwater crayfish in Australia and N. America 24 which may spend lone perods without tree water, ¢.e. Engacus, Cherax, Nothing 1s known of their excretory patterns during aerial expo- sure. CONCLUSIONS In aquatic crustaceans, the main excretory pro- duct is ammonia which is excreted across the gills into the respiratory water streani and carried away, This ensures that the extemal ammonia concentration is always low and there is a favourable gradient lor excretion and no prob- lems of toxicity, By contrast terrestrial arthro- pods, other lhan crustaceans, ure mustly urinotelic and the overriding selective fuctor avouring this, is believed to have been the con- servation of body water, Purines may be excreted in crystalline form in the faeces with minimum accompanying water loss, an important factor in the maintenance of waler balance of smal! ani- mals in a desiccating environment. Of the ter- restrial crustaceans examined Only ane species is clearly purinotelic (Birews faire) and, although many more species seem Lo have an active purine metabolism, their dominant exeretory product is ammonia. Comparatively few terrestrial species have been examined and while further work may reveal a few additional purinotelic species, the group appears to be predominantly am- monotelic, [Lis of interest to consider how far the various groups of terrestrial crustaceans have diverged from the typical aquatic pattern and moved towards the terrestrial system. In this we are hampered by the relative lack of information on excretion in terrestrial groups. The gecarcinid crabs appear to have diverged least from the aquatic pattern. They continue to excrete ammonium across their gills and us res- piratory Water is not available they utilise the excretory fluid from the antennal organs, The volume of urine produced is limited, however, und this necessitates quite high concentrations of ammonia in the branchial chambers and may result in an adverse electrochemical gradient across the gill epithelium. Urine flow is tied to overall water balance rather than excretory re- quirements and this may cause exeretory diffi- culties necessitating temporary storage of waste nitrogen in negative water balance. Geograpsus grayi and terrestrial isopods have departed further from the aquatic pattern und have solved the loss of the respiratory water as an excretory vehicle in a different manner, They MEMOIRS OF THE OLIFENSLAND MUSEUM Telyin the respiratory medium as a vehicle for excretion by releasing gaseous NH, Air flow over (he body or through the branchial chambers effectively prevents the buildup of ammonia next lO the excretory surface maintaining a favourable gradiem for excretion, Until this mechanism of excretion is better understood it will not be possible to say how much inde- pendence from water it allows. Actual elimina- tin of NH, may first require transport of NH,* into the excretory (uid for conversion to NH, or may be direct from the excretory epithelium, Excretion of gascous NH, may be seen as an advance in terrestrial adaptation over that shown by gecarcinids, Exeretion in Birgus /atro shows a complete break from the aquatic pallern of ammmonolelism. The elimination of nitrogenous waste as uric acid and the associated ability to synthesise purine is a major evolutionary advance ald places this species al a similar level of adaptution to the other major groups of terrestrial arthropods. Why have terrestrial crustaceans retained am- monotelism whilst other terrestrial arthropods have not? The main considerations may be the restricted metabolic pathways present at the onset Of terrestrial life and the period of cvalu- tion spent on land. As aquatic species are am- monotelic and probably lack synthetic pathways for both purines and urea, colonists would thus begin terrestrial life excreting ammoniunracross the gills and this would be expected to influence both behaviour and habitat selection, Moist mi- croclimates such as leaf litter and rainforest would be favoured and activity restricted to moist conditions so that adequate excretory fluid would be available for elimination of ammonia. Such habitats are characteristic of terrestrial am- phipods, isopods and crabs, and although several species live in Xeric habitats, their activity is restricted and the animals have a humid retreat or burrow, It would be naive, however, to assume that limitations of the excretory system are re- sponsible for the restricted habitats occupied e.g. Birgus latro has a system well tailored for ter- restrial life but occupies similar habitats to other terrestrial crabs. Limitations of the reproductive and osmoregulatory systems under terrestnal conditions could equally well affect distribution. Given the habitat in which the animals are found, exeretion of various forms of ammonia is feasible and may be advantageous as it carries a minimal energetic cost and requires only small changes to existing systems whilst efficiently excreting waste nitrogen NITROGENOUS EXCRETION The apparent lack of synthetic pathways for excretory materials may mean that a long period of evolution on land and strong selective pres- Sure to penetrate drier habitats is necessary before typical terrestrial patterns of excretion can be developed, Fossil evidence. although fragmentary, suggests that most groups of ter- restrial crustaceans are relatively recent (and in some cases ongoing) colonists of land (Warner, 1977; Little, 1983). The mechanisms of detoxification, transport and elimination of nitrogenous waste all require further study, particularly in the terrestrial spe- cies. In particular the significance of uri¢ acid deposits is far from clear and we need to clarify both this aspect and the origins of the uric acid (dietary or synthesised?), The occurrence of purinotelism should also be investigated and in- vestigations of the xeric-adapted forms such as the desert isopods Hemilepistus and Venezillia, the hermit crabs Coenobita clypeatus and C. rugosus, and the brachyurans Holrhuisana trans- versa and Potamon potamios may be rewarding, Additionally, some terrestrial groups have not been studied at all (Amphipoda and crayfishes) and should reward future investigation, ACKNOWLEDGEMENTS The work was supported by ARC grants A893083 and A1861299. LITERATURE CITED BATREL, Y. AND REGNAULT, M, 1985. 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Nitrogen metabolism in the terrestrial isopod Oniscus asellus, American Zoologist 8: 507-519. 1970, Nitrogen Metabolism in Non-Inseet Arthro- pods. 299-385. In J. W. Campbell (ed.) “Com- parative biochemistry of nitrogen metabolism, Vol. 1, The invertebrates’. (Academic Press: London and New York), HARTNOLL, R.G. 1988, Evolution, systematics and geographical distribution. 6-53, In WW. Burg- pren and B.R. McMahon (eds) ‘Biology of the land crabs’. (Cambridge University Press; New York). HOESE, B. 1981. Morphologie und Funktion des Wasser-Leitungssystems der terrestrischen Isopoden (Crusiacea, tsopoda, Oniscoidea), Zoomorpholagy 98: 135-167. 1982. Der Ligia-Typ des Wasserleitungssystems bei terrestrischer Isopoden und seine Entwicklung in der Familie Ligiidae (Crustacea, Isopoda, Onis- coidea), Zoologische Jahrucher Abteilung Fur Anatomie und Ontogenie der Tiere 108: 225-261, HORNE, F.R. 1968. Nitrogen excretion in Crustacea. 1, The herbjvorous land crab Cardisoma guan- humi(Latreille). Comparative Biochemistry and Physiology 26: 687-695. HUNTER. K.C. AND KIRSCHNER, L.B. 1986. Sodium absorption coupled 10 ammonia excretion in osmoconformning marine invertebrates. Amer ican Journal of Physiology 251; R9S7-RY62, HURLEY, D.E. 1968. Transition from water to Jand inamphipod crustaceans. American Zoologis| 8: 327-353. JOHNSON, P.T, 1980, ‘Histology of the blue crab, Callinectes sapidus. A model for the Decapoda’. (Praeger: New York). 440p, KING, F.D., CUCCS, T.L. AND BIDIGARE, R.R- 1985, A pathway of nitrogen metabolism in marine decapod crabs. Comparalive Biochemis- try und Physiology 80B: 401-403. MEMOIRS OF THE QUEENSLAND MUSEUM KIRBY, P.K. AND HARBAUGH, R.D. 1974, Diur- nal patterns of ammonia release in marine and lertestrial isopods. Comparative Biochemisiry and Physiology 47A: 1313-1321. KIRSCHNER, L.B. 1983. Sodium chloride absorp- Non across the body surface: frog skins and other epithelia. American Journal of Physiology 244; R429-R443. KORMANIK, GA. AND CAMERON, IN, 1981a. Ammonia excretion in animals that breathe water; a review. Marine Biology Letters 2: 11-23. 1981b, Ammonia excretion in the seawater blue erab (Callinectes saptdus) occurs by diffusion, and not Na’/NHa+ exchange. Journal of Com- purative Physiology 141B: 457-462. KORMANIK, G.A. AND HARRIS, R.R. 1981. Salt und waler balance and antennal gland function in three Pacific species of terrestrial crab (Gecar- coidea lalandti, Cardisoma carnifex, Birgus latre |, Urine production and salt exchange in hydrated crabs, Journal of Experimental Zoolagy 218: 97-105. KRIPPEIT-DREWS, P,, DREWS, G. AND GRASZYNSKI, K. 1989, Effects of ion substitu- tion on the transepithelial potential difference of the sills of the fiddler crab Uca tangeri: evidence tor a H*-pump in the apical membrane. Journal of Com- parative Physiology 1S9B: 43-49. KRISHNAMOORTHY, R.V. AND SRIHARI, K. 1973, Changes in the excretory patterns of the freshwater field crab Paratelphusa hydrodro- mous upon adaptation lo higher salinilies. Marine Biology, Berlin 21: 341-348, KUEMMEL, G, 1981, Fine structural indications of an osmoregulatory function of the gills in let- restnal isopads (Crustacea: Oniscoidea Cell and Tissue Research 214: 663-646. LEHNINGER, A.L, 1982. ‘Principles of Biochemis- try”, (Worth Publishers Inc.: New York). 1011p. LITTLE, C. 1984. ‘The colonisation of land, Origins and adaptations of terrestria) animals’. (Cam- bridge University Press: Cambridge). LOCKWOOD, A.P.M. (959, The extra haemolymph sodium of Asellus aquaricus (L, Journal of Ex- perimental Bivlogy 3, 562-565, PRESSLEY. T.A.,GRAVES, 1.8. AND KRALLJ.R. 1981 Amiloride-sensitive ammonium and sudium luxes inthe blue crab. American Journal of Physiology 244: R370-R378. REGNAULT, M. 1987. Nitrogen excretion in marine and freshwater Crustacea. Biological Reviews 2; 1-24. REGNAULT, M. AND BATREL, Y. 1987. Gluta- male dehydrogenase of the shrimp Crangon erangon L. Effects of shrimp weight and season NITROGENOUS EXCRETION 227 upon its activity in the oxidalive and reductive function. Comparative Biochemistry and Physi- ology 86B: 525-530, SANDERS, N.K. AND CHILDRESS, J.J, 1988, Lon tepalcement as a buoyancy mechanism in a pelagic deep-sea crustacean. Journal of Experi- mental Biology 138: 333-343, SCHOFFENIELS, E. 1976. Adaptations with respect io salinity. Biochimica Biophysica Acta 41; 179-204. SHARMA, M. 1966. Studies on the sources and mech- anisms of increased urea production by Orconectes rusticus under osmotic stress. Comparative Bio- chemistry and Physiology 24: 55-60. 1968. Studies on the changes in the pattern of nitrogenous. excretion of Orconectes rusticus under osmotic stress. Comparative Biochemis- try and Physiology 19: 681-690, 1969, Trigger mechanism of increased urea produc- tion by the crayfish, Orconectes rusticus, under osmotic stress. Comparative Biochemistry and Physiology 30; 302-321, SHAW, J. 1960. The absorption of sodium ions by the crayfish Astacus pallipes (Lereboullet U1). The effect of other cations in the external solution, Journal of Experimental Biology 37: 548-556. SPEEG, K.V. AND CAMPBELL, J.W, 1968. Forma- tion and volatilization of ammonia gas by ter- restrial snails. American Journal of Physiology 214: 1392-1402. TOWLE, D.W. AND HOLLELAND, T. 1987. Am- monium ion substitutes for K* in ATP-depend- ent Na’ transport by basolateral membrane vesicles. American Journal of Physiology 252: R479-R489, TOWLE, D.W. AND KAYS, W.T. 1986. Basolateral localization of Na* * K* - ATPase in gill epithelium of two osmoregulating crabs, Cal- linectes sapidus and Carcinas maenas. Journal of Experimental Zoology 239: 311-318. WARNER, G.F. 1977. *The biology of crabs’, (Elelk Science: London). WIESER, W, 1972a. O/N ratios of terrestrial isopods attwo lemperatures, Comparative Biochemistry and Physiology 43A: 859-868, 1972b, Oxygen consumption and ammonia excre~ tion Ligia beaudiana M,-E. Comparative Bio- chemistry and Physiology 43A; 869-876. 1972c. A glutaminase in the body wall of terrestrial isopods. Nature 239: 288-290, WIESER. W. AND SCHWEIZER, G, 1970. A teex- amination of the excretion of nitrogen by ter- restrial isopods. Journal of Experimental Biology 52: 267-274. 1972, Der gehal! an ammoniak und freien amino- suren sowie die eigenschaften einer glutaminase bei Parcellio scaber (Isopoda), Journal of Com- parative Physiology 81: 73-88. WIESER, W., SCHWEIZER, G. AND HARTEN- STEIN, R. 1969. Patterns in the release of gaseous ammonia by terrestrial isopods. Oeco- logia 3: 390-400. WOLCOTT, D.L. AND WOLCOTT, T.G, 1987a. Reprocessing urine at the gill augments nitrogen excretion in the land crab, Gecarcinus lateralis (Latreille), American Zoologist 27: 6A. 1987b, Nitrogen limitation in the herbivorous land crab Cardisoma guanhumi. Physiological Zoology 60: 262-268, WOLCOTT, T.G. AND WOLCOTT, D.L. 1984. Extra-renal urine modification for salt conserva- tion in the land crab Cardisoma guanhumi. American Zoologist 24: 78A. 1985. Extrarenal modification of urine for ion con- servation in ghost crabs, Ocvpode quadrata Fab- ricius, Journal of Experimental Marine Biology and Ecology 91: 93-107. WOOD. C.M. AND BOUTILIER, R.G. i985. Osmoregulation, ionic exchange, blood chemis- iry and nitrogenous waste in the land crab Car- disoma carnifex: a field and laboratory study. Biological Bulletin of the Marine Biological Laboratory, Woods Hole 169: 267-290, WOOD, C.M., BOUTILIER, R.G, AND RANDALL, DJ. 1986. The physiology of dehydration stress in the land crab, Cardisoma carnifex. respira- tion, ionoregulation, acid-base balance and nitrogenous waste excretion. Journal of Experi- mental Biology 126; 271-296. WOOD, C.M. AND RANDALL, D.J. 1981. Oxygen and carbon dioxide exchange during exercise in the land crab Cerdisoma carnifex. Journal of Experimental Zoology 218; 7-22. ZANDEE, D.I. 1966. Metabolism in the crayfishAsta+ cus astacus (L. 1. Biosynthesis of amino-acids. Archives Internationale de Physiologie et Bio- chimie 74; 35-44. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 228 THE ROLE OF CRUSTACEANS IN NITROGEN RECYCLING IN A HIGH ENERGY SURF ZONE ECOSYSTEM The Sundays River surf zone (33°58'S,29"19'F) in the Eastern Cupe South Africa is considered jo function as & semi-clased coasystem (McLachlan, YS) with phe outer boundary at the edge of the surf cell circululton patiern and the landward boundary at the dnft line, Surt zones exist in three major energy states: a high energy dissipalive state. = low energy reflective state, and a trange of intermediate states (Shortand Wright, 1983), The Sundays Riversurl cone exists in the intermediate longshore har trough energy state for Yer of the yeat, moving fo a high energy dissipalive sauce during storms and lo.a lowerenergy intermediale Iramsverse bar rip state during calm periods. The major mechanism tor the return Mow oF waler tothe nearshore is Vid rip currents, Three types of rips operate in the surf zone: non exchunge rips which do nol break through the breaker line and serve i circulme Water within the inner surf gone, exchanwe rips which carry water ftom the inner lo the outer surf zone and mega rips Which operate during storm conditions and dis- charge water kilometres out to sea. Half tumover rime for walter in the innerand whole surl zone is in the orderuft hours and days, respectively (Talbot, 1986). The unix of enviren- ment used \n surf Zone studies is A Metre sinp of surl zone from the drift line to the 10m depth contour 500m offshore which encloses a volume of 2500m" (McLachlin and Bule, 1984), Phytoplankton (mainly the diatom Anaalus auyeralis) are (he major primary producers iq he surl gone forming dense accumulations usually in association with rip currents. Phytoplankton accumulations are a function of die} vertical migration pullerns, offshore-onshore migratiun and the storm calm cycle. These phytoplankton accumulations fuel three distinet food chains; the macroscopic: interstitial; and microbial Joop, The macroscopic food chain consists of benthos, zooplankton, fish and birds, Benthos form 46% of tofal macrofaunal biomass with filer fecding bivalves the most important component. Crustaceans (mainly the three sporswimming crab, Ovalipes puncratas) contribute anly 1% of benthic biomass. Zooplankton ure @ major component of the macroscopic food chain forming 40% of macrotaumal biomass with aumbers and biomass dominated by crustaceans. Small penaeid prawns (Macropetasma: afri- canis) and mysids (Mesapadapsis slabberi and Gastrosac- cus psammodytes) contribute >90% uf zooplankton biomass (Romer, 1986), The role of crustaceans in the recycling of Nifrogen in the Sundays River surf zone was determined trom detailed laboratory and fleld studies on the nitrogen require- ments of surf zone phytoplankton and the nitrogen dynamics of (he major macrofaunal specios, The nitrogen requirements of the surt zone Were calculated directly from the estimates of phytoplankton primary production, Primary production was measured using Cl" uptake and O° evolution, A marhe- matical model incorporating temperature, light, beach stale, and photo-inhibition was used to estimate annual primary production. The partion of assimilated carbon involved in cell doubling was calculated and divided by the C/N rand of A. australis (C:N ratio= 6.8), Using this metiod the nitrawen requirements of the surf zone (inner and outer) are calculated at 13.200 gN.m !.y!. (Campbell, 1987). The forms of nilro- wenexcreted and (he effects of mass, lemperalure, starvation, dict and presence/absence of sediment On excretion rates MEMOIRS OF THE QUEENSLAND MUSEUM were determined for M. afritaans (Cockeroft and MclLach- Jon, 1487) and the mysids M. slabber! and G, psentmtodyres (Cockerot) efaf, 1988), Information on populition structure, abundance, diet and feeding hehaviour collected over a de- cade of fesourch in this area was combined with nitrogen excretion data to construc! population pilrogen budgets for these speci¢s. The amounts of nilrogen recycled by the less abundant crustacean components (crabs and small zaoplank- ton farms} were obtained from population nitrogen budgets using lileraiure values for nitrogen excretion tates (Cock- troty, 1985), Cruslaceans recycle 2626 yNon iy? in dis- soived Inorganic form (mally ammonia) Which comstitutes TUS oF the dissolved \morganic nitrogen excreted by the macrotaunal food ehain, Large zooplankton forms (prawns and mysids) supply the bulk of this recycled nitrogen. This represents 20% of total surf zone phytoplankton nilragen requirements assuming that phytoplankton utilise dissolved inorganic nitrogen only. Crustaceans also contribute 1839 BNom Ly! or 64% of the dissolved und particulate organic nilrogen (mainly faeces) excreted by the mucrofsuna. This represents 17% of total nitragen requirements estimated for the mucrobial loop (Romer and MeGwynue, pers, euram,), Crustaceans therefore play an important role in surf zone nitrogen recyeling both in terms of phytoplankton require- ments and as a Jink benween the macroscopic and microbial loap food chains, Literature Ctted Campbell, B.E. 187. "The estimation of phytomass and pomaty production of a surf zone’, Ph.D. Thesis, Uni- versity of Port Elizabeth. 33Up. Cockermfi, A.C JU88. “The role of macrofauna in qitogen recycling in a high energy surf zone’, Ph.D. Thesis, University of Port Elizabeth. 285p, Cockcroft, A.C, and McLachlan, A. 1987, Nitrogen re- generition by the surf gone penusid prawn Macro- pemsma africamis (Balss). Marine Biology 96: 343-348, Coekerofl, A.C, Webb, P, and Wooldridge, T. 1988, Nitro- gen regeneration by two $urt zane mysids, Mesopodap- ws slabber! and Gastrosaecus psanimadyies, Marine Biology 99: 75-82. McLachlan, A. 1980. Exposed sandy beaches as semi-closed ecosystems. Marine Environmental Research. 4; 39-63. McLachlan, A. and Bate, G, 1984. Carbon budget for s high energy surf zone, Vie Milieu 34: 67-77. Romer, G.S. 1986, ‘Paunal assemblages and tood chains associated wilh surf zane phytoplankton blooms’, M.Se. Thesis, University of Port Elizabeth. 194p. Shon, A. and Wright, L.D, 1983, Physical variability of sandy beaches, (33-144, In A. McLachlan and T. Er- asmus (eds) ‘Sandy beaches as ecosystems’. (Junk: The Hague). Talbot, M.M,B, 1986, ‘The distribution of the surf diatom Anaulas birastratus in relation (6 thé nearshore circula- lion in an exposed beachisurfzone ecosystem’. PlD- ‘Thesis, University of Port Blizabeth, 356 p Andrew C. Cockcroft, Deparment of Zaalagy, University of Port Elizabeth, Box 1600, Part Elizabeth, South Africa, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum INTEGRATION OF CELLULAR, ORGANISMAL, AND ECOLOGICAL ASPECTS OF SALT AND WATER BALANCE DONNA L. WOLCOTT Wolcott, D.L. 1991 09 01: Integration of cellular. organismal, and ecological aspects of salt and water balance. Memoirs of the Queensland Museum 31: 229-239. Brisbane. ISSN 0079-8835. Crustaceans occupy habitats ranging from hypersaline through freshwater and terrestrial, and differing in variability of temperature. salinity, and moisture over periods of hours to months, Even in stable, isosmolic environments, they must expend energy in maintaining their internal osmotic and ionic milieu. The impetus for maintaining a constant internal environment can be traced to the deleterious effects of volume changes in individual cells, with the resulting structural and functional changes in proteins. Organisms employ a combination of inorganic ion transport and organic osmolyte deployment to match intra- cellular and extracellular osmolalities, thus reducing the energy required to maintain cell volume. In multicellular animals, such as crustaceans, changes in external salinity are countered by two strategies. In the first. the osmolality of the internal fluid tracks that of the external medium, transferring osmotic work to the individual cells. The second strategy involves regulation of the osmolality of the imernal fluid. The work of osmo- and iono-regulation is concentrated in surfaces in contact with the external medium, such as the integument and gut. Water regulution is relegated to specialised excretory organs, such as (he antennal gland, and ion transport lo spatially restricled and specialised tissues, such as the gills of crabs and sal! glands of Arfemnia. A number of ion transport systems important in iono- and osmoregulation have been identified in crustaceans. Many of these systems are integral to acid-base balance und nitrogen excretion as well. In addition to sharing common enzymatic palhways, ion regulation frequently occurs on morphological struc- tures with multiple functions. Thus, the gills of decapad crabs serve gas exchange, nitrogen excretion, and ion exchange. Constraints caused by the limited number of physiological mechanisms and morphological options result in integrated responses of salt and water balance, acid-base balance, gas exchange and intermediary metabolism. Examples are given from aquatic decapods. Some terrestrial crabs employ 4 single behavioural modifi- cation, urine recycling atthe gill, that addresses several concurrent physiological problems, such as ion depletion, water limitation and nitragen excretion. In crustaceans in general, behavioural adaptations permil occupation of habitats that would be untenable based on physiological and morphological capabilities alone. To describe the water and salt balance of a particular organism, if is therefore necessary to integrate information from cellular mechanisms, organismal responses, and field observations. (] Osmoregulatian, ianoregu- lation, ion transport, volume regulation, erustaceans, terrestrial crabs, osmalytes. Donna L. Wolcott, Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Raleigh, N.C. USA; 6 July, 1990, Cell function is supported only within a narrow range of ionic and osmotic conditions. If uncam- pensated, chemical changes resulting from me- tabolic processes would inexorably move the cell from the dynamic equilibria optimal for enzyme function. Such constancy of the internal environment that exists must be maintained through dynamic, energy-requiring transport of ions, aided, and also thwarted, by passive water and ion fluxes. The energetic cost of osmo- and iono-regulation differs in degree, but is incurred by marine, brackish, freshwater, and terrestrial organisms alike. The physical laws of thermodynamics ulti- mately dictate the movements of solvent and solutes across the cell membrane between the external and internal media. The forces involved, and the equations that describe them, are well reviewed in Mantel and Farmer (1983), with additional information on water fluxes in a ter- testrial environment found in Greenaway (1988). Enhanced fitness of organisms that maintain proper solute and water relations in the interior of individual cells drives evolution of osmo- and iono-regulatory systems. When cells are ex- posed to fluids that are anisosmotic (not isaos- malic) to the cell’s interior; they tend to shrink or swell, depending on whether the flulds are hyper- or hypo-osmotic to the cytoplasm. Cell volume can be restored by the active extrusion or uptake of inorganic solutes, such as Na”. and by manipulating the concentration of organic osmolyies, such as free amino acids (Hoffman and Simonsen, 1989; Chamberlin and Strange. 1989; Pierce, 1982). Cells of organisms that show volume regulation are able fo return to their normal volume by matching the internal osmotic pressure to the new extracellular regime. Volume regulation under anisasmotic condi- tions involves a number of processes, In the short term, inorganic ions are pumped into or out of the cell to bring the fluid compartments on either side of the cell membrane into osmotic balance, restoring cell volume. However, the conforma- tion of proteins, and hence their function, ts intimately dependent on the presence and con- centration of particular ions. Therefore, for long- term gsmotic adjustments, organisms employ a variety of organic osmolyles. Organic osmo- jytes, although metabolically expensive to de- ploy, have a distinct advantage over inorganic jons in that they do nol compromise protein function even when present in high concentra- tions (Yancy er al., 1982), Organic osmolytes are selected for their com- patibility with enzyme and other physiological functions, and on the basis of their metabolic or environmental availability (Hochachka and Somero, 1984: Gilles and Pequeux, 1983; Gool- ish and Burton, 1989), Across the entire spec inim of living creatures, organic osmolytes include suyars, polyols, amino acids, methyl- amines, und urea, Crustaceans employ all but the last (wo, With non-essential free amino acids being most common (Gilles and Pequeux, 1983; Chamberlin and Strange, 1989). For both rapid volume adjustments and pen- eral oc!l function, mavement of inorganic ions acecurs through ton-specific channels and pumps, and via a variety of exchangers. and cotransport- ers. Paramount among the transport sysiems is Na’/K*-ATPase, responsible for pumping Na” from the cell: The inwardly-directed electro- chemical gradient for Na” thus created provides the motive foree for the movement of ather ions against their concentration gradients. The cou- pled movement of CI and Na’ is an example of cotransport. Most cotransport sysiems described so far involye coupled transport of cations and anions whose charge balance is zero. Such sys- tems are clectroncutral, or elecincally *silent’. Their operation neither affects the membrane MEMOIRS OF THE QUEENSLAND MUSEUM potential nor is affected by it (Hoffman, 1986), Like cotransport systems, exchange syslems (e.g. HCOs- for Cl) can also be electroneutral. Because ion transport and water balanee are problems around which life evolved, the mech- anisms are fairly universal. lon transport mech- anisms identified in other organisms are found to operate in crustacean tissue as well (Table !)(Chamberlin and Strange, 1989). Some of the conflicting data surrounding the Na*/H* ex- changer in crustaceans may be resolved, now thal (he presence of an electrogenic, 2Na*:1H™ exchanger has been identified, both in crab gill (Callinectes sapidus, Towle and Baksinski, 1989) and in Jobster antennal gland (Homarus americanus, Franco and Ahearn, 1989), Some progress is being made in the search for the signals and sensors whereby individual cells detect volume changes (Chamberlin and Strange, 1989). Ton channels have been iden- ufied that respond directly to the changes in hydrostatic pressure resulting from the efflux or influx of water during anisosmotic conditions by allering the transport of specific ions, Such streich-activated ion channels respond to changes as small as 5 mmHg. The amount of membrane stretch resulling from a volume ins crease of even 1% would be sufficient to activate the K* channel in Necturus proximal tubule cells (Sackin, 1987). The cytoskeleton may play a role in stimulating stretch activated channels by amplifying volume-induced stretch, Stretch in- activated channels have been identified cocx- isting in the same neurons as stretch activated channels (Morris and Sigurdson (1989), Cham- berlin and Strange (1989) speculate that coordi- nated activation of transporters active in Volume regulation and deactivation of resting conduc- tances would permit more rapid and energeli- cally efficient volume regulation, Once cells receive input signalling a change in asmeotic conditions, cither physically, through hydrostatically-transmilted information, e.g, stretch activated receptors, or chemically, e.g. by 4 variety of intracellular second messengers which integrate the cells. osmoregulatory re- sponse, Several intracellular signals have been impli- cated in cell volume regulation, including cyclic AMP, leukotrienes, protein kinases, und Ca~*, with the possible involvment of calmodulm (Chamberlin and Strange, 1989), Current evi- dence confirms that cyclic AMP is an intracellu- lar modulator of ion transport in crustaceans as well (Bianchini and Gilles, 199()), SALT AND WATER BALANCE The permeability of cells to water and ions is affected by (he kinds and quantity of lipids pre- sent in the cell membrane, Changes in the qu ality and yuanrity of membrane and blood lipids. including cholesterol, correlate with changes in permeability (Chappelle and Benson, 198: Spaargaren and Mors, 1985; Subramanyam and Krishnamoorthy. 1983) and link osmoregulation with lipid metabolism, Since the metabolic processes discussed so far require energy, iono and osmo-regulation are interdependent with respiration and those physi- cal and biotic factors which effect it, Tn the context of multicellularity, the interac- tion of an organism with ils environment is changed in fundamental ways. For a given amount of cytoplasm, the proportion of mem- brane exposed to the environment is reduced, e.g, every organism small cnough to depend solely on diffusion for transport of oxygen and nutrients, and for release of metabolic wastes (approximately | mm maximum effective thick- ness, Graham, 1988) only needs to cantrol per- meability and to transport ions over a small proportion of its total plasma membrane. Concurrent with evolution of larger body form is the development of interior fluid reservoirs and circulatory systems.to enhance transporl of gases and solutes, The major and initial response to variations in the environment is still confined to the integument, but the organism has the op- lion of controlling the composition of the interior fluid spaces. Again, the driving force 1s the main- tenance of an intracellular ionic and osmotic environment optimal for cell function, Crusta- ¢eans employ two options in dealing with salin- ity fluctuations. One is to allow the fluid bathing the cells, the haemolymph, to track external sa- linity, thus transferring the work required during anisosmotic regulation to the cell, Alternatively, they may manipulate haemolymph composition during salinity changes to minimise the osmotic work that the cells must do. The former option, osimoconformity, restricts organisms to habitats where the osmotic concentration is fairly high and stable, or commits them to volume regula- tion by cells during adverse osmotic conditions. The second pattem, osmoregulation, permits oc- cupation of ionically or osmotically extreme oF variable habitats, Osmoregulation and osmocon- formity can exist in the same organism over different parts of the salinity scale, For instance, in marine organisms occasionally exposed to fresh water input, conforming at high salinities and hyper-osmoregulating al low salinities would be aduplive. However, the impetus fur Mainlaiing & conslant jonie concentration in coelomic fluids ts still ta reduce the need for volume regujation by individual cells. The regu- latory options adopted by different organisms are reflected in the familiar categories of asmoregulation; osmoconformity, hyperregula- tion. and hyporegulation, and the combinations thereot (Mantle and Farmer, 1953), As external sulinity varies, the effects on cell volume will depend on the type of osmoregulation available, both at the organism's surface and at the cel! (Gilles and Pequeux, 1983). In larger organisms, and those adapted to yuri- able habitais, tissue that regulates transport of ions and water is highly localised, with the rest of the surface tairly impermeable, thus passively restricting exchange with the environment. Rather than being uniformly deployed in the cell membrane, certain ion-transporting enzymes are restricted to or concentrated on a particular sur- face. For instance, Na‘/K*-ATP-ase is highly concentrated in the basal-lateral membrane of the gill epithelial cell, where it appareotly fone- tions La transport cations, including NH4+, be- tween the cell interior and the haemolymph (Table L) (Towle and Kays, 1986; Towle and Holieland, 1987), Both the activity and quantity of this enzyme inercase dramatically with changes in salinity (Kirschner, 1979; Towle, 1984), On the apical surface, Na” is exchanged for H* (Table 1). Commonly, respiratory, feeding, and loco motory functions are Combined al the same sur- face, as ys ton and solute transfer. Water flow created by feeding and locomotory currents en- hances exchange of solutes across the integu- ment by reducing the boundary layer. Most aguatic phyla are dependent on integumental gas exchange al some point im their life history (Graham, !988). Among crustaceans, individu- als depend on integumental exchange during development us eggs and larvae. Salt and water balance are intertwined with acid-base balance, gas exchange, and through changes in free amino acid concentrations, inter- mediary metabolism and fluxes of ammonia. The links are forged by the commonality of biochemical mechanisms and morphological structures involved in these processes, Synthesis and catabolism of free amino acids during fluc- Wations in salinity links osmoregulation, nitra- gen metabolism, and excretion, Use of common pathways alsa interconnects ion regulation and acid-base balance. 232 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. Examples of ion transport pathways identified in crustaceans. LOCALISATION REFERENCES TRANSPORT MECHANISMS SPECIES Na*/K*-ATPase Artemia salina Callianassa jamaicanse Callinectes sapidus Carcinus maenas Eriocheir sinensis Gecarcinus lateralis Homarus gammarus Procambarus clarkii Uca minax U. pugilator U. pugnax U. tangeri metepipodites + head, maxillary gland, gut larval salt glands larval salt glands larval stages gills NH “activation NH, ‘substitutes for K* basolateral membrane gills basolateral membrane gills larval stages antennal gland gills 5 and 6 gills 5 and 6 basolateral gills 5,6 Holliday, 1985a Ewing et al., 1974 Lowy and Conte, 1985 Felder et al., 1986 Mantel and Olson, 1976 Towle et el., 1976 Towle and Holleland, 1987 Neufled et e/., 1980 Towle and Kays, 1986 Siebers et al., 1982 Towle and Kays , 1986 Pequeux andGilles, 1977 Mantel and Olson, 1976 Thuet et al., 1988 Sarver and Holliday,unpubl. Wanson et al., 1984 Graszynski and Bigalke, 1987 D’Orazio and Holliday, 1985 Holliday, 1985b Graszynski and Bigalke, 1987 Pressley et al., 1981 Burnett and Towle, 1990 Taylor and Harris, 1986 Grayzynski and Bigalke, 1987 Pequeux and Gilles, 1988 Grayzynski and Bigalke, 1987 Na‘/H* C. sapidus gills, apical Corophium curvispinum | amilioride sensitivity Eriocheir sinensis gill membrane vesicles Uca tangeri 2 Na*/H* C. sapidus posterior gill vesicles Towle and Baksinsk,i 1989 Homarus americanus antennal gland vesicles Franco and Ahearn, 1989 ee ee resicubal si aba gee Carbonic anhydrase | C. sapidus Neufeld et al., 1980 (CO,+H,0 < H"+HCO, ) gills Burnett et al., 1981 gills 6-8 Henry and Cameron, 1982 cytoplasmic+membrane Henry, 1988 Cardisoma carnifex gills Randall and Wood, 1981 Cardisoma guanhumi gills 6-8 Henry and Cameron, 1982 Gecarcinus lateralis gills 8 and 9 Henry and Cameron, 1982 Homarus gammarus Thuet et al., 1988 Na‘ channel 2 Carcinus maenas Uca tangeri CI channel Lucu and Siebers, 1987 in Grayzynsk and Bigalke, 1987 Callinectes sapidus Burnett and Carroll, 1989 SALT AND WATER BALANCE AMMONIA If the transport mechanisms of the gill are overwhelmed by the speed or amount of salinity change, the haemolymph concentration will change. To minimise the work that must be done to maintain volume in the face of water influx, intracellular osmotic concentration is lowered both by increasing inorganic ton excretion, and by exporting or metabolizing some of the free amino acids (FAA). Metabolism of the FAA releases ammonia, which is transported by the haemolymph, dissolved or incorparated into glu- lamate (Regnault, 1987), to the gill. There, am- monia is exchanged for Na’ (Towle and Holleland, 1987; Lucu er al., 1989), coupling ion uptake and nitrogen excretion, Enhanced rales of ammonia excretion during hypoiomic stress have been reported in the shore crab, Careinus maenas (Spaargaren, | 982; Harris and Andrews, 1985), the intertidal prawn, Palaemon elegans (Rathke) (Taylor ef al., 1987), the shrimp Cran- gon crangon L. (Regnault. 1984). Panaens japonicus Bate (Spaargaren er al, 1982) and several other species (Mantel and Farmer, 1983), Ammonia exerelion can respond rapidly to changes in salinity, ¢.g. in the intertidal prawn, Palaemon elegans (Rathke), which may be sub- jected to frequent, rapid fluxes in salinity, De- clines in FAA in the tail muscle, increases in ammonia excretion and adjustments in Na* con- centration all occur within the first two hours following a major salinity drop (Taylor er al., 1987). Similar rapid shifts in ammonia excretion follow transfer to low salinity in the bluc crab Callinecies sapidus (Rathbun) (Mangum ev a/,, 1976), whose habitat is marked by Jonger-term seasonal fluctuations in salinity, in addition to storm events, Organisms inhabiting estuaries with large tidal fluxes experience repetitive cy- cling of salinity. Crangon crangan in the Penze estuary, France, has enhanced rates of ammonia excretion during ebb tides, as riverine water bowers the salinity, and lowered rates of exere tion during flood tide, as high salinity waters return, The ammonia excretion rate is influenced by the velocity and direction of the salinity ing and by the range of salinities involved, and is greater in the winter. In the laboratory, shrimp exposed to simulated tidal cycles of salinity under winter conditions lose 1.75 times more ammonia than those in constant salinity (Regnault, 1984), In nature, burrowing (Bir- chard et al., 1982, Zanders and Martela, 1984) and circatidal activity rhythms {Al-Adhub and Naylor, 1975) may reduce exposure {o salinity changes and minimise the energetic cost of in- habiting a variable environment. GAS EXCHANGE In Callinectes sapidus, inorganic ions and H* jons compete for the same site un the haemocy- anin molecule, and raise or lower the oxygen affinity, respectively (Mangum, 1986), During hypoionic exposure, enhanced production of ammonia counteracts the lowering of ones affinity of haemoeyanin caused by reduced concentration (Weiland and Mangum, 1975), A permanent solution to reduced Ca** concentra- tion inthe haemolymph of blue crabs acclimated to low salinity is the synthesis of an alternate haemocyanin subunit. and changes in the pro- portions of another, such that oxygen affinity is re-established at a new, lower level (Mason e al., 1983; Mangum and Rainer, 1988), ACID» BASE BALANCE The pH of the cell depends on the strong jon difference (SID), as well as on the partial pres- sure of CO2 (Peu,) and the concentration af weak acids (Stewart, 1978). The major contro! of pH jn Walet-breathing animals is through adjust ments of the SID (the difference between the quantity of fully-dissociated strong base cations and strong acid anions) (Cameron, 1978: Stewart, 1978), As Cl and Na’ ate moved across transporting epithelia, possibly in exchange for HCOs- and H’, pH can change. Protein, amino acid, and ammonia concentrations change as cell volume regulation occurs. Thus, the same sys- tems that are involved in ion regulation affect acid-base balance as well (Cameron, 1978; Hoffman and Simonsen, 1989). Hypersaline ex- posure can cause acidosis, as metabolic acid production outstrips increases in bicarbonate concentration (Wheatly and McMahon, 1982), and hyposaline conditions may result in alkalosis due to excess base cations (Carcinus maenas L., Truchot 1973, 1981); Callinectes sapidus, Wei- land and Mangum, 1975). In marine aquatic crabs, the gill plays a major role in ion transport, gas exchange and ammonia excretion, with the role of the antennal gland largely that of water balance, since the urine produced is isosmotic to the blaod, Several freshwater crustaceans have evolved the capac- ily to produce a dilute urine, and the antennal gland in these forms functions remarkably like a vertebrate Kidney, playing an enhanced role in ion and acid-base balance and ammonia excre- tion (Wheatly and McMahon, 1982; Wheatly and ‘Toop, 1989). Even in these forms, the ma- jority of ton regulation occurs at the gill (Wheatly and Toop, 1989), The gut plays a role in fon regulation and water balance, too, (review, Mantel and Farmer, 1983), but (he contribution of the gills is paramount. How is ion regulation achieved in terres- trial crustaceans, given that the major ion- permeable surfaces, the gills, are no longer immersed in Jarge volumes of water? Are the ion-pumping, nitrogen excreting, acid-base balancing capabilities of the gills lost to the organism? Noy necessarily. Precisely be- cause the organisms are in air, voided urine is not lost to the environment, and cun be passed to the gill surfaces for ion techama- tion (Wolcott and Wolcott, 1985, 1991, and unpubl.), So far, several species huve been shown to reclaim ions from the urine during teprocessing al the gill (Table 2), The excre- tory product (“P*) that is eventually released by the animal can be very dilute, comparable in ion concentration to hypoosmotic urine produced by several freshwater crustaceans (Table 2). Reprocessing essentially permits the production of a dilute urine, thus circum- venting behaviourally the limited abilitics of the antennal gland. Urine represents the most saline Water avail- able to hyperosmoregulating terrestrial crustaceans, and as such, is a vital resource. The red land crab, Gecarcinus lateralis, inhab- its dry upland burrows, and its water sources are dilute, When ion concentrations in the haemolymph are experimentally depleted, they can be replenished with ions from the diet (Wolcort and Wolcotl, 1988), However, even feeding crabs show declines in haemolymph osmolality when the urine is prevented from reaching the gills (Wolcott, 1991). Avoidance of standing water, as in Gecarcoidea lalandu (Cameron, 1981) may be an adaptation to pre- vent accidental dilution of urine in the branchial chamber. lon reclamation is not the only function of the gill that is preserved by urine reprocessing. In both G. fateralis and the amphibious crab, Caerdisoma guakhumi, ammonia concentra- lions increase 14 and 10 fold, respectively, as urine is reprocessed into ‘P’ (Table 2) (Wol- cott. 1991). Not all species that recycle urine use *P* for nitrogen waste disposal, and nitro- Een excretion in species thal recycle urine js turning out to be highly variable (Greenaway, pers. comm., and this volume). MEMOIRS OF THE QUEENSLAND MUSEUM In air-exposed crabs, fluid in the branchial chamber, whether water from the environment or urine from the antennal glands, may provide a reservoir for acid-base adjustments in those crabs that can regulate ions (Burnett and McMahon, 1987; Burnett, 1988). Euryriuen albidigitum, an intertidal osmoconformer, ex- periences emersion-induced respiratory acido- sis, and is inactive when in air, In Pachygrapsus crassipes, an ion regulator. such respiratory acidosis is fully compensated, and crabs remain uctive in air. Unlike &. albid- igitum, fluid in the branchial chamber of P. crassipes tapidly increases in both carbon dioxide and in titratable alkalinity upon air exposure. Burnett (1958) suggests that alkalin- isation of the branchial chamber fluid main- tains a steeper gradient of Peo2 across the gill, favouring transport of bicarbonate from the haemolymph, and counteracting respiratory acidosis. Haemolymph ion regulation may have evolved in organisms whose variable habitat or vigorous exercise resulted in acid- hase imbalance, with concomitant disruption of metabolism and activity (Ballantyne ef al., 1987). lon regulation in turn supported utilisa- tion of brackish, freshwater and terrestrial hab- itats (Patts and Durning, 1980), Urine passed to the branchial chamber in the amphibious crab, Cardisoma guanhumi, has a high pH, and very high titratable alkalinity, about 20 times greater than sea water (D, Wolcott, unpubl. data, Table 2). This may also assist movement of CO2 across the gill, a process much slower in air than in water, reducing respi- ratory acidosis on emersion, und compensating for the hyper-capnic conditions inside the crabs’ burrows (Pinder and Smits, 1986). Adjustment of pH by altering the ratia of ca- tions and anions is more rapid than relying on metabolic removal of lactate after exercise or air exposure. Osmoconformers such as Eurylium albidigitum and Libinia emarginata apparently do not use ion exchange for pH regulation, and haemolymph acidosis is uncompensated (Bur- nett and MeMahon, 1987; Booth, 1986), From the complex interplay of ion and osmotic regulation in extracellular fluid and cells, invaly- ing ion transport, water fluxes, acid-base balance, oxygen transport, free amino acid pools, and nitrogen exerction, it is plain that the jong- and asmoregulatory abilities of the whole organism cannot be inferred from the abilities exhibited in isolated tissues, or measured under unnatural conditions. Often, abilities of organ- SALT AND WATER BALANCE 235 TABLE 2. Jon reclamation in hypoosmotic urine of Crustacea from fresh water habitats and reprocessed urine of crabs from terrestrial habitats. Haemolymph (mmol/L) FRESHWATER SPECIES Austropotamobius pallipes Corophium curvispinum Gammarus pulex Gammarus duebeni Goniopsis cruentata Macrobrachium australiense Procambarus clarkii Pacifastacus leniusculus TERRESTRIAL SPECIES Birgus latro Cardisoma guanhumi Gecarcinus lateralis Ocypode quadrata isms in the laboratory to maintain a constant ionic milieu in the face of salinity changes fall short of values determined in the field or under more natural conditions (Flemister, 1958; Rabalais and Cameron, 1985; D’Orazio and Holliday, 1985; Zanders and Martelo, 1984; Gross, 1964; Morritt, 1988; Spicer et al., 1987; Blasco and Forward, 1988). On the other hand, understanding the inte- grated response is not possible until the contributions of cellular and subcellular processes are appreciated. Integrated responses of many biochemical, neural, endocrinological and behavioural systems con- tribute to enantiostatic control of internal functions. Both the detailed, isolated mechanisms and the inte- grated systems must be studied before a clear picture of iono- and osmoregulation is achieved. (mmol/L) Urine References P (mmol/L) Reigel, 1968 Taylor and Harris, 1986 Lockwood, 1961 Lockwood, 1961 Zanders, 1978 Denne, 1968 Kamemoto et al., 1966 Pritchard and Kerley, 1970 Greenaway and Morris, 1989 Wolcott and Wolcott, unpubl. Wolcott and Wolcott, 1991 Wolcott and Wolcott, 1985 ACKNOWLEDGEMENTS I am indebted to the workers in the field of osmo- and iono-regulation, and apologise for citing such a small fraction of the crucial studies. This review was made possible by the support of grant DCB 8905019 from the National Science Foundation of the United States of America, and the sacrifices made by my husband, Tom, and children. LITERATURE CITED AL-ADHUB, A.H.Y. AND NAYLOR, E. 1975. Emergence rhythm and tidal migrations in the brown shrimp Crangon crangon (L.). 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AND CEC- CALODI, H.J. 1982 Excretion of nitrogenous pro- ducts by Penueus japonicus Bale in relalion \o environmental osmotic conditions. Comparative Biochemistry and Physiology 72A; 673-078. SPICER, J.L, MOORE, P.G. AND TAYLOR, A.C. 1987, The physiological ecology of land invasion by the Talitridae (Crustacea: Amphipoda), Pro- ceedings of the Royal Society of London B 232; 95-124. STEWART, P.A. 1978. Independent and dependent variables of acid-base control. Respiration Phys- inlogy 33: 9-26. TAYLOR, A.C,, SPICER, J. AND PRESTON, T. 1987, The relationship between osmoregulation and nitrogen metabolism in the intertidal prawn Palaemon elegans (Rathke), Comparative Bio- chemistry and Physiology 88A: 29)-298, TAYLOR, P.M. AND HARRIS, R.R, 1986. Osmoregu- lation in Corophium curvispinum (Crustacea: Am- phipoda), a recent coloniser of freshwater. [. Sodium ion regulation. Journal of Comparative Physiology 156B; 323-329, THOMPSON, W.E., MOLINARO, P.J., GRECO, 'T.M., TEDESCHI, J.B. AND HOLLIDAY, C.W. 1989. Regulation of haemolymph volume by uptake of sand capillary water in dessicated fiddler crabs, Uca pugilator and U'ca pugnax, Comparative Bio- chemistry and Physiology 944; 531-538. THUET, P., CHARMANTIER-DAURES, M. AND CHARMANTIER, G. 1988. Relation entre osmoregulation et activites d’ATPase Na-K" et d'anhydrase carbonique chez larves et postlarves de Homarus ganmarus (L,) (Crustacea; Decapoda), Journal of Experimental Marine Biology and Ecology 115; 249-261. TOWLE, D.W. 1984. Membrane-bound ATPases in arthropod ion-iransporting tissues. American Zool- ogist 24: 177-185. TOWLE, D.W, AND BAKSINSKT, A, 1989, Blectra- genicity of the crustacean Na"“/H* exchanger de- monstrated with a potential-sensitive dye. American Zovlogist 294); 1524. TOWLE, D.W, AND HOLLELAND, T. 1987. Am- monium lon substitutes for K* in ATP-dependent Ne" transport by basolateral membrane vesicles. SALT AND WATER BALANCE 239 American Journal of Physiology 252; R479— R489. TOWLE, D.W. AND KAYS, W.T. 1986. Basolateral localization of Na” + K*-ATPase in gill epithelium of two osmoregulating crabs, Cal- linectes sapidus and Carcinus maenas. Journal of Experimental Zoology 239: 311-318. TOWLE, D.W., PALMER, G.E. AND HARRIS, J.L. Ill 1976. Role of gill Na+ K* dependent ATPase in acclimation of blue crabs (Callinectes sapidus) to low salinity. Journal of Experimental Zoology 196: 315-322. TRUCHOT, J.-P. 1973. Fixation et transport de l’oxy- gene par le sang de Carcinus maenas: variations en rapport avec diverses conditions de tempera- ture et de salinite. Netherlands Journal of Sea Research 7: 482-495. 1981. The effect of water salinity and acid-base state on the blood acid-base balance in the eury- haline crab, Carcinus maenas (L,). Comparative Biochemistry and Physiology 68A: 555-561. WANSON, S.A., PEQUEUX, A.J.R. AND ROER, R.D. 1984. Na* regulation and (Na’ + K”)- ATPase activity in the euryhaline fiddler crab Uca minax (Le Conte), Comparative Biochem- istry and Physiology 79A; 673-678. WEILAND, A.L. AND MANGUM, C.P. 1975. The influence of environmental salinity on haemocy- anin function in the blue crab Callinectes sapidus. Journal of Experimental Zoology 193: 265-274, WHEATLY, M.G. AND MCMAHON, B,R, 1982, Responses to hypersaline exposure in the euryha- line crayfish Pacifastacus leniusculus J. The inter- action between ionic and acid-base regulation. Joumal of Experimental Biology 99; 425-445. WHEATLY,M.G. AND TOOP, T. 1989. Physiologi- cal responses of the crayfish Pacifastacus leni- asculus to environmental hyperoxia IT. Role of the antennal gland in acid-base and ion regulation. Joumal of Experimental Biology 143: 53-70. WOLCOTT, D.L. IN PRESS. Nitrogen excretion is enhanced during urine recycling in two species of terrestrial crab. Journal of Experimental Zoology. WOLCOTT, T.G. 1973. Physiological ecology and intertidal zonation in limpets (Acmaea): acritical look at ‘limiting factors’. Biological Bulletin 145; 389-422, WOLCOTT, T.G. AND WOLCOTT, D.L. 1985. Ex- trarenal modification of urine for ion conserva- tion in ghost crabs, Ocypode quadrata (Fabricius). Journal of Experimental Marine Bi- ology and Ecology 91: 93-107. 1988. Availability of salts is not a limiting factor for the land crab, Gecarcinus lateralis (Fremin- ville). Journal of Experimental Marine Biology and Ecology 120; 199-219. 1991. Ton conservation by reprocessing of urine in the land crab Geearcinus lateralis (Freminville). Physiological Zoology 64: 344-361. YANCEY, P.H., CLARK, M.E., HAND, 5.C., BOWLUS, R.D. AND SOMERO, G.N. 1982. Living with water stress: evolution of osmolyte systems. Science 217: 1214-1222, ZANDERS, |.P. AND MARTELO, M.-J. 1984. In- fluence of temperature on ionic regulation in the mangrove crab Goniopsis cruentata. Comparative Biochemistry and Physiology 78A(2): 249-254. ZANDERS, I.P. 1978, Ionic regulation in the man- grove crab Goniopsis cruentata, Comparative Biochemistry and Physiology 60: 293-302. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum THE BEHAVIOURAL BASIS CRUSTACEAN DISTRIBUTION TIDALLY MIXED ESTUARY Net flow in estuaries is seawards, exposing swimming animals to the risk of export to the sea. This has led to numeTous investigations of mechanisms facilitaung estuarine retention (Naylor. 1988), Generalisations are diffi- cult however, partly because of differences in estuarine cirey- lation patterns. Also, differentspecies may be moré abundant in different parts of an estuary, implying that various he- havioural mechanisms may be instrumental in mainiaining observed distributions. The area siudied was the Conwy Fstu- ary, the largest in North Wales, which is almost completely mixed, Here, retention strategies based on laminar flaw (Cronin and Forward, 1982) cannot operate. This work in- vestigates behavioural retention strategies of spevies from various habitats within the estuary. and explores {he relalion- ship berween behaviour, retemion and distribution. Probably the most significant behavioural strategy is thal of the planktonic copepod Eurytemora affinis, a curvhaline Species, most numerous in the low salinity zone. Drift-ner Sampling on rising spring tides showed copepod abundances in the waler column to be concentrated on flowd tides at downstream sites and on the ebb tide at the most upstream site, This suggests a preferred region in which the majority of animals are found. Sampling over each tidal evcle fortwo weeks at a mid-estuary site showed distinct semi-lunar var- iation of the tidal abundances of F. affinis. Greatest abun- dance over neap tides was on the ebb, but was on flood tides Over springs, Suggesting thal the population maximum moved upstream on springs and downstream on n¢aps. To test this, plankton samples were taken on three separate spring and neap tides, Each lime a distinct population maxi- mum was found, the position af which was further seaward on neap than on spring tides. Independent oceanographic studies on the Conwy estu- ary (Shiono and West, 1987) suggest no physical mecha- nism which could explain these observations on the basis thal E. affinis behaves as a passive particle. Extensive horizontal swimming by animals of this size seemed equally unlikely, but vertical migrations into the waler column at different times was an attractive working hy- pothesis, Endogenous locomotor activily was therefore tested for as a possible behavioural basis to these observations. Swim- Ming activity was measured under constant conditions in (he laboratory using an infra-red light beam actograph and a free-running activity rhythm in phase with the time of expected high tide was found. apparently the first in a copepod, This suggests that &. affiris moves into its pre- ferred salinity zone by swimming, under endogenous con- trol, on the slate of tide providing transport in the appropriate direction. The position of this zone varies with the semi-lunar cycle, and the swimming activity of the animals appears to change accordingly. OF IN A MEMOIRS OF THE QUEENSLAND MUSEUM Different retention strategies. are adapted by two species of amphipod. Garuneruy zaddachi and Corophium voluta- tor, Bowl swim periodically in the water column and so risk export from the estuary, C. volutator was found fairly con- sistently at the mid-estuary locations, bul G. zaddachi varied its position throughout the year with respect to salinity as also reported elsewhere by Girish er a/, (1975). Overwintering adults and developing juveniles occurred high up the estuary whereas reproducing adults were most common in mid-estu- ary, Thus the adult population, parncularly ovigerous females, move downstream while juveniles migrate up- stream Significantly na G. zaddachi were recorded at the mast Seuward site. Experimental studies demonstrated the presence of endo- genous swimming rhylhms in both amphipod species, but that each exhibited different kinetic swimming responses in a Qume tank, G.zaddachi showed increased swimming in higher current velocities, whereas C. velutator showed the Opposite response, Thus G. zaddachi appears to use a come hination of endogenously fimed swimming behaviour and responsiveness to water flow to vary its position along the estuary, while C. volutator appears {o avoid moving water and so limits displacement from its preferred habitat. In conclusion several strategies appear to have evolved by which estuarine crustacean species maintain their distribu- tions in an environment of net flow seawards. Moreover, the precise nature of the zonations found in each species suggest that inthe Conwy Estuary, behaviour is finely tuned toensure Telention in specific environments within the estuary and not simply within the estwary itself. Acknowledgements The authors wish to thank the Natural Environment Re- search Council (U.K.) for travel and studentship funding for ARH, Literature Cited Cronin, T.W. and Forward, R.B. Jr. 1982. Tidally timed behaviour; Effects on larval distributions in estuaries. In V.S. Kennedy (ed) ‘Estuarine comparisons’. (Academic Press: New York). Girish, H.B., Dieleman, J.C. Petersen, G.W. and Pinkster, S. 1974. The migration of wo sympatric gammarid species in a French estuary. Bijdragen tor de Dierkunde 44: 239-273, Naylor. 6, 1988, Rhy(hmic behaviour of decapad Crustacea. Symposium of the Zoological Society of London 59; 177-199, Shiono, K, and West, J.R. 1987. Turbulent perturbations of velocity in the Conwy Estuary, Estuarine, Coastal and Shelf Science 25; 533-553. Andrew R. Hough and Ernest Naylor, SchoolofOcean Sciences, University College of North Wales, Menai Bridge, Wales LL59, UK. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum RESPIRATORY GAS EXCHANGE AND TRANSPORT IN CRUSTACEANS: ECOLOGICAL DETERMINANTS STEPHEN MORRIS Morris, S. 1991 09 01: Respiratory gas exchange and transport in crustaceans: ecological determinants. Memoirs of the Queensland Museum 31: 241-261. Brisbane. ISSN 0079- 8835. Crustaceans have radiated into many different environments ranging from deep sea hydrothermal vents, through the intertidal zone and freshwater io terrestrial habitats. Adaptation lo these varied conditions has included marked and significant changes in both the gas exchange organs and blood pigment lunction. The funcuioning of haemocyasnin, the respiratory pigment of most crustaceans, is in many species under the complex control of biochemical feed back mechanisms. Modulation of haemucyanin funetion can occur due lo the accumulation of specific melaboliles or as a resull of specific compounds enlering the animal from the environment. For example hydrothermal vent fauna exhibit specific adaptations to high sulphide levels and mesopelagic species containing high levels of ammonia show different bul again specific adaptations. Metabolic modulation of blood pigment function occurs most extensively in the sub-littoral and intertidal species, Ter- restrial species show [he most marked morphological/biochemical changes in the structure and funetion of the gas exchange organs and appear (o have abandoned complex molecular modulation of blood gas transport. The ecalogical physiology of these adaptive trends ix considered using, examples, and directions for future investigation are discussed,L) Crustacean, oxygen, carbon dioxide, haemocyanin, respiratory, gas exchange. Stephen Morris, Department of Biological Sciences, University of Calgary, 2500 Univer- sity Dr. N.W., Calgary, Alberta T2N 1N4, Canada, Present address: School af Bialogical Setences, University of Sydney, Syddev, New South Wales 2006, Australia; 6 July 1990, The study of respiratory gas exchange and transport in crustaceans has proceeded largely on a comparative basis and for practical reasons has dealt primarily with decapod species. As a con- sequence, our knowledge is disproportionately based on a number of ‘large’ species from ‘inter- esting or challenging’ environments. which are then compared to ‘normal’ species. However, it is by examining adaptations to extremes that the plasticity and adaptability of the Crustacea be- comes apparent. There have been a number of recent teviews that have considered adaptation to specific en- vironments (Powers and Bliss, 1983; Vernberg and Vernberg, 1983; McMahon and Burggren, 1988; Burggren and McMahon, 1988), specific morphological adaptations (Greenaway and Far- relly, 1990) or have given general treatments (Mangum, 1983; Vernberg, 1983; Cameron and Mangum, 1983). The more general papers have not been restricted to respiratory gus exchange and transport. The present paper, while continuing the basic principle of examining adaptation to extremes atid by necessity with a bias towards the de- capads, will relate specific adaptations in the gas exchange organs and haemolymph function to the special demands of various habitats. These habitats range from abyssal hydrothermal vents, through the intertidal to fully terrestrial. Often adaptations not directly related to gas exchange and transport have forced compromise on the respiratory physiology. It is not within the scope of this paper to provide a complete description of all species from each habitat. Rather, ex- amples have been selected to demonstrate our current knowledge and to indicate those areas that warrant further study. DISCUSSION The two main respiratory gases, oxygen and carbon dioxide, move across the bady wall of crustaceans by diffusion. This is often facilitated by a respiratory pigment, most usually haemocy- anin, and there is goad evidence that CO? excre- tion is aided by carbonic anhydrase (Henry, 1987). Diffusion limited gas exchange can be KA sp E where M is the amount of diffused gas in mmol.min’, £ is the thickness of the barrier and A the area. K is Krogh's diffusion constant (mmol.min'atm') and ? is the partial pressure described by the Fick equation; M= 242 gradient across the barrier, The diffusion con- stant takes into account not only diffusion through the membrane but also the solubility coefficient of the extracorporeal medium. Since CO2 is c. 25 times more soluble than O2 in water, diffusion of O2 rather than COz is the limiting factor in aquatic species. Therefore, it is the maintenance of O2 supply that is the major mod- ifying factor in the evolution and control of respiratory systems (McMahon and Wilkens, 1983). In air the capacity for Oz and COz are essentially the same and the outward diffusion of COz2 therefore relatively slower; which has a major influence on the respiratory gas exchange and transport of air breathing species. Itis generally accepted that in non-malacostra- can crustaceans no specialised respiratory struc- tures are present but instead appendages, specialised parts of the integument or the body wall as a whole are employed (McLaughlin, 1983). The simplest form of malacostracan gill is a vascularised lamellar outgrowth of the thora- copod and occurs in multiple pairs in mysids and amphipods. In the isopods these structures are often elaborated (Edney, 1960). The gills of Eu- carida are more complex and with few excep- tions enclosed within the carapace in the paired branchial chambers through which water (or air) is moved. The most usual arrangement is for water to flow in through openings at the base of pereiopods (Milne Edwards openings) into the hypobranchial space, through the gills into the hyperbranchial space and then pumped out through exhalant openings on either side of the epistome (McMahon and Wilkens, 1983). Primi- tively, the gills existed as sets of four attached to each appendage but all modern decapods show a reduced number. The gills themselves fall into three categories depending on the complexity of branching: a) phylobranchiate the normal gill type for caridean shrimp and brachyuran crabs; b) trichobranchiate as found in most lobsters and crayfish; and c) dendrobranchiate as found only in penaeoids and sergistoids (McLaughlin, 1983). McMahon and Wilkens (1983) con- sidered that this increased branching of the gills might indicate the evolution of increased surface area for gas exchange. Perfusion of the gas exchange organs and the respiring tissues is equally important in deter- mining rates of gas exchange. The circulatory system of crustaceans has been termed ‘simple’ because of the open nature of large parts of the venous system. In the smaller crustaceans this may be true but in the larger decapod species the MEMOIRS OF THE QUEENSLAND MUSEUM open circulatory system is complex, highly effi- cient and tightly regulated (McMahon and Bur- nett, 1990). Haemolymph-flow through gills has been demonstrated to be organised and the direc- tion controlled (Burggren and McMahon, 1988; Taylor, 1990). Terrestrial species exhibit highly modified gas exchange structures and have made major alterations in perfusion, with respect to breathing air instead of water, or in the case of amphibious species breathing both (see below). AQUATIC vs TERRESTRIAL — A CONTINUUM The evolutionary and adaptive processes in- volved in moving from breathing water to breathing air have received some considerable study but it is only recently that we have begun to understand how the Crustacea have accom- plished this. The movement of crustaceans into terrestrial environments has occurred either via the freshwater or intertidal zone habitats (Hart- noll, 1988), although in some cases it is unclear which route was followed. Those of direct marine origin tend to have a marine pelagic larval stage whereas those from freshwater bene- fit from an abbreviated nonplanktonic larval development providing greater independence from water (Hartnoll, 1988). Within this con- tinuum there exist several discrete habitats, marine, estuarine, freshwater, intertidal, tidepool, amphibious, and semi- and fully ter- restrial, although any species may not be limited to one. ESTUARINE/FRESHWATER — SALINITY EFFECTS The major challenge for species moving into estuarine habitats and from there progressively to freshwater is the maintenance of salt balance. Increased osmoregulatory work could theoreti- cally lead to increased gas exchange but this has been difficult to demonstrate (Taylor, 1988). Moving into freshwater and more especially en- vironments of varying salinity does, however, have some demonstrable effects (Vernberg, 1983; Cameron and Mangum, 1983; Taylor, 1988). The green shore crab Carcinus maenas is atypical estuarine/intertidal species. The normal estuarine, intertidal and rock pool environments are subject to frequent and often abrupt changes in salinity. After exposure to low salinity the respiration rate of C. maenas is significantly elevated, peaking after 3-4 h but remains ele- vated for several days (Taylor, 1977). This re- sponse appears to be standard for those species so far investigated (Taylor, 1988). Quite clearly there is no rapid acclimation to reduced salinity. RESPIRATORY GAS EXCHANGE IN CRUSTACEANS The increased oxygen uptake is associated with a hyperventilatory response; with the increased oxygen demand possibly being met by a tachy- cardia and increased cardiac output (Taylor, 1977, 1988). The oxygen transporting properties of the haemocyanin from a number of estuarine and intertidal animals respond to salinity changes (Carcinus maenas, Truchot, 1973; Callinectes sapidus, Weiland and Mangum, 1975). These changes can occur as a result of the failure to completely regulate blood ions with respect to changing environmental salinity. In most aquatic crustaceans, such as Carcinus, increases in the concentrations of Ca and Mg especially, induce increased affinity for O2 by the haemocyanin and also increase the Bohr shift (Fig. 1). The rock pool species Palaemon elegans shows good ion regulation and consequently no effect on oxygen affinity when exposed to low salinity (Ramirez de Isla Hernandez and Taylor, 1985; Taylor et al., 1985). Callinectes sapidus although an osmoregulator also shows a decrease in the oxy- gen affinity of Hc when acclimated to low salin- ity and this led Mason et al. (1983) to suggest that some small dialysable factor may be re- sponsible. Recently it has be shown, however, that C. sapidus exhibits changes in haemocyanin phenotype, the expression of which is dependent on salinity (Mangum and Rainer, 1988), and the phenotypes have different functional charac- teristics. These changes with respect to acclimation salinity do not, however, always elicit the same effect in vivo due to concomitant changes in blood pH. Low salinity results in an increased blood pH and therefore an increase in oxygen affinity which compensates for the decreased affinity due to lowered blood ions (Fig. 1) (Tru- chot, 1973). There is also good evidence that some species show increased Hc levels in re- sponse to acclimation to low salinity (Sabourin, 1984; Taylor et al., 1985) but this occurs slowly over a number of days and is primarily an osmoregulatory response and not respiratory. SUBLITTORAL The most common demand on the respiratory system of sub-littoral species is to maintain aero- biosis during exercise. Exercise has been used as experimental treatment by a number of workers and extensive data exist for various Cancer spe- cies. In C. magister 20 min exercise causes an increase in ventilation and perfusion (McMahon et al., 1979). The increase in scaphognathite and 243 14 - Carcinus maenas Effect of [Mg] oo ia. oo ee, 12 |. Ll ™ +a pH 7.8 log xo * 7 —@- pH 7.2 torr 1.0 _— 0.9 ic a 0.8 —+—F TT T T T T ! 0 25 50 75 100 125 150 175 200 225 [Mg] mmol/L 1.0 Carcinus maenas Salinity Acclimation . | oe ; = a 08 — ‘ oy B 7 pane: 3 0.6 ~s / a / ~ 44.7 Yoo, pH 7.75 < 0.4 / ins a / / yp 36 Yoo, pH 7.75 0.2 fff 00 — —— —— 0 10 20 30 40 Po, torr FIG. 1. Upper, The effect of Mg on the oxygen affinity (log Psy) of haemocyanin from Carcinus maenas. The increase in affinity due to higher Mg concentration is more marked at high pH. The in- creased divergence of the plots at pH 7.2 and pH 7.8 is due to the increased pH sensitivity, ie. greater Bohr shift, induced by high Mg levels (after Tru- chot 1975);Lower, Salinity acclimation of O2 trans- port in C. maenas. The centre curve indicates the oxygen equilibrium of blood from Carcinus in full strength seawater and at the in vivo pH. Maintaining blood pH at 7.75 but reducing salinity would reduce affinity as shown by the right curve. Salinity accli- mation is normally accompanied by an increase in blood pH which compensates for the reduced affin- ity to actually produce a slight increase in affinity under in vivo conditions (left curve). Curves con- structed from the data of Truchot (1973). heart beat rates is accompanied by a marked increase in oxygen uptake which is reflected in a decrease of the blood oxygen content (Fig. 2). In a parallel study (McDonald et a/., 1979) it was noted that 20 min exercise resulted in significant L-lactate (end product of anaerobiosis) efflux into the blood, with a significant acidosis and a rise in the partial pressure of CO2, the latter despite the hyperventilation (Fig. 2). The anaero- bic component of this response, i.e. the elevated lactate levels and the acidosis, continued to in- crease for some 30 min post exercise and before 4.0 —| sw f Boia a3 ao -{ a 5 7 4 1 | 7} + oo — T T 2 2 o 19 4 ao 23 ac 16 | eo» thy e - = ic fs E J 7 6s I . zs 4 . Bos Wes = ad | “J 3 4 | i, z |! ————___ i ° r : 2 2 o 19 i+ as 22 as 6.0 ? | 73 4 i ee | 7-8 1) + a oe 7-7 | | a i} 7. | Ff 7 by rs m a¢ EE 2 2 3s 190 12 a8 22 26 MEMOIRS OF THE QUEENSLAND MUSEUM = OBO Sie Sat jit ee | o40 — @ Tt = 4 SBS o.ao @ Arterial i= mH Venous - o20 449 _* oe \ pe od —™ 0.10 D,00 {A =z se 1c 4 18 22 2a O07 > g o,06 — t go,05 + |\ ep 0.04 rs goo jg ra @ 0,02 7 —~s- 4 : Soo + = 4 6,00 T T TTY T 2 2 6 19 14 18 a2 26 oF Te on 5 t Ss 1 ' Bare =a b = oe = —_ os - red i rr est FS a3 z on iM - = + 2 2 « io 14 is 22 26 Time (h) FIG. 2, Changes.in respiratory blood-gas parameters, lactate and pH, oxygen uptake and ventilalion volume during 20 min exercise (filled vertical bars) und 24 h recovery in Cancer magister. Arterial and venous blood values are Supplied for O2 content (data abstracted from McDonald et al., 1979; MeMahon et al., 1979). returning to normal resting values. Complete recovery of all parameters required 24 h (Fig. 2). Obviously the exchange of respiratory gas and/or transport is insufficient to maintain aero- biosis in the working muscles. and supplemen- tary anaerobic energy production is used to meet the increased demand. Some species, normally sublittoral, contain in- dividuals that become air exposed and the success of these individuals in breathing air may determine their survival. Small Cancer produc- tus (<100g) are often found emersed in the low intertidal zone (DeFur and McMahon, 1984a). Air exposure of Cancer elicits a different re- sponse from exercise in that there is a decrease in oxygen uptake due to the failure of the gills as gas exchange organs but there is a similar in- crease in ventilation, in PCO2 and also CO2 content (Fig. 3) (DeFur and McMahon, 1984a,b). The response to this shortfall in owy- gen supply is again the initiation of anaerobiosis and the efflux of L-lactate into the haemolymph which exacerbates the haemolymph acidosis (Fig. 3). It is important to note that attempts to compensate for this acidosis appear to involve ihe mobilisation of CaCO3 from the carapace to produce HCOs- (Henry e¢ al, 1981; DeFur and McMahon, 19844; Innes et al., 1986). The con- comitant increase in circulating Ca will tend to have a potentiating effect on the affinity of the He tor oxygen (see above) partially compensat- ing for the decreased affinity due to the Bohr shift and thereby assisting oxygen loading at the gills. Again complete recovery of all parameters, especially L-lactate, required at least 24 h. Air exposure of aquatic species appears, therefore, not to be met with any special adaptive response. L-lactate may mitigate some of the effects of air exposure. Truchot (1980) reported that L-lactate increased the oxygen affinity of some crustacean haemocyanins, including Cancer. This effect has now been substantiated for a number of species (Bridges and Morris, 1985; Morris, 1990; dis- cussed below). The immediate benefit would seem tp be a partial compensation for the effect of a metabolic acidosis, which reduces the affin- ity of haemocyanin for Oz. Depending on cir- cumstances the effect can either improve loading of oxygen at the gills or increase the size of the venous reserve, that is the amount of oxygen RESPIRATORY GAS EXCHANGE IN CRUSTACEANS remaining bound to Hc after passing through the tissues (Morris, 1990). The latter would seem to be an adaptation to exercise and the former to breathing hypoxic water. LITTORAL AND POOL ENVIRONMENT Within the littoral zone exist a number of mi- crohabitats of which the rock pool environment is perhaps the best studied. While conditions in the pools may be similar to those of inshore seawater they can frequently and regularly be- come extreme, with wide fluctuations in oxygen availability (PO2 10 — 500 torr), temperature (-1.5 — 30°C), salinity, pH and carbon dioxide levels (Truchot and Duhamel-Jouve, 1980; Mor- tis and Taylor, 1983). Similar environmental changes have been described for habitats on boulder and sedimentary shores (Agnew and Taylor, 1986 and citations therein). With the exception of salinity similar environmental stresses occur in freshwater bodies. The rate of gas exchange and transport is de- termined by the metabolic demands of the ani- mal, which in crustaceans with no temperature homeostasis will tend to vary with environmen- tal temperature. The fluctuating temperatures experienced in smaller bodies of water might be expected to have significant effects on metabolic requirements. Long term (seasonal) temperature changes may be met by temperature acclimation (Newell, 1979). The pool dwelling prawn Palae- mon elegans, which shows temperature acclima- tion over a period of weeks, exhibits greater thermal tolerance (survives < 0°C) than the open water species P. serratus and P. adspersus which avoid temperature extremes (Taylor, 1988), In addition to greater tolerance such species often show some metabolic independence of tempera- ture (Qi0 < 2.0). Fluctuating temperatures are a feature of the littoral zone generally and are reflected in intertidal hermit crabs by low Qj0's of 1.4 and 1.6 (Burggren and McMahon, 1981). Similarly low Q10’s were recorded for P. elegans but these were size dependent (Morris and Tay- lor, 1985a). The increased O2 demand and CO2 production is met by increased ventilation and perfusion together with changes in the transport properties of the blood. Oxygen transport is af- fected by reduction in dissolved O2 at high temperature and by changes in the haemocyanin QO2 affinity, which arise from allosteric modula- tion and temperature dependent changes in pH (~ -0.016 pH.°C"'). Generally, the effect of in- creased temperature, at constant pH, is to decrease O2 affinity (Mangum, 1983). Acclima- 245 tion of He oxygen affinity also seems possible. In Carcinus moved to a higher temperature oxy- gen affinity first decreased but then slowly in- creased, which Truchot (1975) suggested was due to an increase of a dialysable factor. Moving Hemigrapsus nudus, an amphibious intertidal crab, from 15 to 30°C caused urate concentra- tions to increase from ().015 to 0.052 mmol.L! (Morris, Greenaway and McMahon, unpubl.). Urate has been identified as a modulator of He O2 affinity (below) and may explain the above temperature effects on Carcinus, the haemocy- anin of which is sensitive to urate (Lallier and Truchot, 1989a). This decreased O2 affinity at higher temperature may compromise oxygen up- take, although unloading at the tissues might be enhanced. In rock pool species this is mitigated by the fact that the highest temperatures occur during periods of hyperoxia (Morris and Taylor, 1983). Conversely, hypoxia is associated with the lowest diel temperatures and reduction in oxygen demand. Apart from allosteric modula- tion the haemocyanin of many intertidal species shows reduced temperature sensitivity at temperatures near the environmental mean. Crustacean He normally exhibits a 5H of -35 kJ.mol' or larger, 6H being the change in the heat of oxygenation of He with an increase in temperature. Forexample in P. elegans 6H =-1.7 kJ.mol’ (Morris e7 al., 1985) and the hermit crab Pagurus bernhardus 5H = 0 to -18 kJ.motl' (Jokumsen and Weber, 1982). Both of these species have He that is especially sensitive to pH (o << -1.0) which supports the suggestion that there is an inverse correlation between pH sen- sitivity and temperature sensitivity (Burnett et al., 1988), although this seems not to be true for all species, e.g. terrestrial and hydrothermal vent species (see below). It could also be argued that those species living under a relatively constant temperature regimen exhibit no special adapta- tion to temperatures never encountered, and that reduced sensitivity is a response to a eurythermal environment. During hypoxia many crustaceans can main- tain a near constant oxygen consumption down to very low levels of environmental oxygen and are termed regulators (Fig. 4). Below this ‘criti- cal’ PO2 anaerobiosis becomes increasingly im- portant. The critical PO2 (Pe) is highly variable between species but it now appears that the Pc is correlated with the extent and duration of hy- poxia experienced (Table 1). The maintenance of MQz is due to a response common to nearly all species investigated, a pronounced increase 246 sou oe OT 20 4 i 5 i = | = 2o0—~ \ | a\+————3 4.0 s 2 es 20 ™- oo 32a 26 20.0 —- few = | a 5 30.0 4 /| = [| 2 4 / I? s a i Oe * ear 2 2 4 to - ja ss ae s.°0 —— = 7. Ly I es a ee 728 \ - Ba! 2 ore - 7.7 7 -2 2 4 io La = 22 26 Time th) MEMOIRS OF THE QUEENSLAND MUSEUM : = Arterial %e C Venous 10, | mmol/L, 0 n a a ne MO, mol /kg.min 3so0co — 2000 | \ J isso Vy ml/kg.min -z a a 1o 14 is a a€ Time (h) FIG. 3. Changes in respiratory blood-gas parameters, lactate and pH, oxygen uptake and ventilation volume during 4h air exposure (filled vertical bars) and 24 recovery in Cancer productus. Arterial and venous blood values are supplied for O2 content (data abstracted from DeFur and McMahon, |984a,b). in the rate of scaphognathite beating (Taylor, 1988). The rate of beating increases steadily until the Pc is reached, e.g. P. elegans (Fig. 4), Al- though this increased ventilation helps maintain oxygen uptake the increased work itself repre- sents a metabolic demand and at the Pe it is considered that O2 uptake is sufficient only ta supply the pumping activity. Taylor (1988) compares rock pool and open water species and concludes that rock pool spe- cies often show higher He concentrations, which increases the amount of O2 transported, and ad- ditionally that these Hes show high affinity and pH sensitivity. The high affinity would en- courage oxygen uptake at the gills and the latter could assist in unloading at the tissues. While He concentration certainly is a factor it is now ap- parent that intertidal species, including rock pool animals have a series of mechanisms for ‘fine tuning’ He oxygen affinity (Morris, 1990). As a consequence the affinity will vary in dependence of physiological condition. The He of Palaemon elegans for example is extremely sensitive to L-lactate and affinity is markedly increased with only small changes in concentration (Table 2). The most apparent advantage of this effect is to aid the loading of oxygen at very low ambient oxygen and prevent the rapid onset of extensive anaerobiosis. In addition to L-lactate it has been found that urate (Morris et a/., 1985a,b) and more recently the catecholamine, dopamine (Morris and McMahon, 1989) have marked potentiating ef- fects on some crustacean Hes. In Carcinus and the prawn Penaeus japonicus, which encounters hypoxic conditions in lagoons, urate accumu- lates in the blood with hypoxia (Lallier and Tru- chot, 1989a,b). In addition, blood urate levels decrease progressively as the ambient POz is increased into the hyperoxic range (Lallier et al., 1987), Clearly urate concentration responds to environmental oxygen levels above the Pc whereas L-lactate formation is significant below the Pe, leading Lallier and Truchot (1989a) to conclude that under normal circumstances urate is most important in regulating blood oxygen affinity. Neurohormonal modulation of pigment oxygen affinity is most likely in situations of sudden stress. Intertidal, rock pool and near shore species appear to be provided with a suite RESPIRATORY GAS EXCHANGE IN CRUSTACEANS of complementary biochemical feedback sys- tems for regulating oxygen transport (Morris, 1990), The blue crab Callinectes sapidus 1s also oc- easionally found in the intertidal zone, although it copes poorly with breathing air, and contains Hc sensitive to L-lactate and urate. Prolonged hypoxia (50-55 torr) results in enhanced blood oxygenation but not as a result of signilicent increases in either lactate or urate but rather duc to increase in circulating Ca and by a change in the He phenotype (DeFur et al. 1990), The transport of CO2 will also be affected by the above modulators since the transport of CO2 and Oz are linked under most circumstances (Bridges and Morris, 1989). Hypoxia in rock pools is invariably accompanied by hypercapnia, with the inverse relationship during hyperoxia. a feature which has not been rigorously duplicated in laboratory simulation studies. Simultancous variation in CO? and Q3 levels in rock poals has markedly different consequences than varying Oz alone (Bridges and Morris. 1989). Using artificial tide pools Truchot (1986) demonstrated that the blood alkalosis. observed during labora- tory hypoxia, as result of the hyperventilatory response, is much less obvious when the CO2 level in the water concomitantly increases, Sim- ilarly the acidosis often observed as a result of hypoventilation during hyperoxia is consider- ably ameliorated. Thus rock pool animals face significantly different demands on the onygen transport system than do species inhabiting hy- poxic oceanic waters such as the oxygen min- imum layer (see below), When water PO? falls below the Pe many species show an important behavioral response, partial emersion. Although P. elegans exhibits exceptional oxyregulation, below 20 torr the prawns will partially emerse themselves at the air—-water interface and by a combination of hy- perventilation and pleopod beating aerate the surface film (Taylor and Spicer, 1988), Similar behaviour has been observed for freshwater crayfish, Orconectes rusticus (McMahon and Wilkes, 1983). This behaviour under conditions of hypoxia close to the Pe increases haemolymph oxygenation but also allows CO2 exchange with the water, which maintains blood pH (Taylor and Spicer, 1988). Similarly, small Cancer produc- fus when air exposed in situ where they are often partially buried take advantage of the interstitial water to reduce the degree of internal hyper- capnia and acidosis (Fig. 3). Under conditions of severe hypoxia (< Pe) many of these normally obligate waler breathers emerge completely from the water, e.g. P. elegans (Taylor and Spicer, 1988) and Echinogammarus pirloti (Agnew, 1985). This response, whereby under extreme conditions ij is more beneficial to breathe air than water, may represent selective pressure directing some species towards an am- phibious existence. AMPHIBIOUS — AIR AND WATER BREATHING The amphibious Crustacea, both those from the supratidal and those from treshwater bodies, show varying degrees of independence from water. This may be viewed as an evolutionary trend With species such as Carcinus maenas (Taylor and Butler, 1978) and the crayfish Aus- tropatamobius pallipes (Taylor and Wheatly, 1981) at the more aquatic end. A. pallipes is exemplary in that when the freshwater that it inhabits becomes very hypoxic it moves into air (Taylor and Wheatly, 1981), This initially pro- motes a response similar to that exhibited by C. productus (Fig. 3) but during a 24 h emersion period the initial increase in blood lactate and subsequently Ca appear to maintain oxygen up- 340 goo A250 By00 o Poo = sq || ofa S100 toe 60 yrteewe ° 2— > +--+ oo * - ‘ o — 7 f tao 200 300 ago 500 Po, torr 4 v1 ia. a ° . be ~~ 2 : rey i” vee Lad . 32 ‘ é Pa = 0 1 1 . _ iy 100 200 300 400 500 Po, torr FIG, 4. Showing the regulation of WOz (lower panel) by Palaemon elegans over a wide range of oxygen availability. Oxyregulation ceases at ca. 20 torr the critical POs for this species. The upper panel shows regulation of heart rate (Fh) by P. elegans and the scaphognathite rale (Fsc) during hypoxia. The hy- perventilatory response ceases near the critical PO2 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. Critical oxygen partial pressures (Pc) for the regulation of oxygen consumption in selection of crustaceans from various habitats. Species Cartcer pagurus 2H40 Curcinus maenas' 6U-R0 Pachygrapsus crassipes AU) Austropatamobins pallipes 40 Upogebia pugetlensis™ 5 45-50 Callianassa californiensis™ {0-20 Palaeman adspersus zi) Palaeman elegans" 10-15 Palaemon serratus 50-60) Palaemonetes varians WW-15 Echinogammarus pirlotl' 13-25 Echinogammarus obtusatus' 13-25 Hemigrapsus nudus' <10 Gnathophausia ingens! 6 Acanthephyra curtirostris 8 Euphausia pacifica® ¢ Is Bythograea thermydron” 19h Pe (torr) Source Bradford and Taylor. 198) Tavlor (1976), Jouve and Trughot (1978) Burke (1979) Wheatly und Taylor (1981) Thompson and Pritchard (1969) Thompson and Pritchard (1969) Hagerman and Weber (1981) Morris and Taylor (1985b) Taylor (1988) Hagerman and Uglow (1984) Agnew and Taylor (1985) Agnew and Taylor (1985) Morris et al. (In Preparation) Childress (1975) Childress (1975) Childress (1975) Mickel and Childress (1982b) 1 : £ ae a" @ z : a 3 ) bea - Intertidal/interstitial species, “Intertidal Qurrowing species, “Primarily rockpoal species, “Midwater species from the oxygen minimum layer, Hydrothermal vent crub “Measured at 825°C, “Measured at 2°C; Species nol numbered are normally aquatic/open water forms. take and transport, and stabilise blood pH and PCOz (Taylor and Wheatly, 1981; Morris et al., 1986b). The L-lactate produced in the initial period of hypoxia is slowly removed from the blood (Taylor and Wheatly, 1981). A. pallipes employs the same basic responses as fully aquatic species and this seems adequate for several days of air breathing. Compared to obli- gate aquatic species (Liocarcinus, Johnson and Uglow, 1985) Carcinus shows morphological adaptations in that the gills are more strongly chitinised and thus have a lesser tendency to collapse in air, allowing some gas exchange to occur across the gills. Hemigrapsus nudus, a more truly amphibious species, spends the greater part of the day breath- ing air but shows no specific modification to the gills, which collapse and adhere when the crab enters air, Instead this species shows increased vascularisation of the membrane lining the branchial chamber which takes on a lung fune- tion. For example in A. nudus breathing air for 4 hours the venous blood oxygen content was 0.20 mmol.L! and that of the arterial blood 0.26 mmol.L', while blood exiting the lung contained 0.30 mmol.L oxygen (~75% saturated; Morris, Greenaway and McMahon, unpubl.). Quite clearly oxygen rich blood from the pulmonary circuit was being diluted by oxygen poor blood from the branchial circuit. Interestingly, Hemi- grapsus He shows little sensitivity to lactate (Table 2) indicating a reduced dependence on modulation of respiratory pigment function, in- deed air breathing by Hemigrapsus causes no significant lactate production (Morris, Greena- way and McMahon, in prep). In the absence of biochemical modulation of haemocyanin func- tion Hemigrapsus maintains a constant arterial- venous oxygen content difference, a stable pH and a Stable, if elevated blood COz near 3.5 torr (Fig. 5), Amphibious species differ from aquatic species in that the blood gas and acid-base para- meters during air breathing are stabilised and respiration {8 not significantly supplemented by anaerobiosis. A number of amphibious species have devel- oped unusual accessories to breathing air, These include the evolution of gas exchange windows in the merus of each walking leg of Scopimera (Maitland, 1986) and the visceral ‘lung pump’ of Holthuisana (Greenaway and Taylor, 1976). Holthutsana, in reality a semi-terrestrial crab, while breathing air ceases scaphognathite activ- ity and jnstead moves the internal viscera from side to side alternately occluding and opening the branchial spaces and thereby causing a ven- \ilatory current over the gas exchange surfaces. It is of note that while species such as Hemigrap- RESPIRATORY GAS EXCHANGE IN CRUSTACEANS 249 TABLE 2. The oxygen affinity as Pso, its sensitivity to L-lactate and urate for some crustaceans selected with tespect to habitat and mode of existence. Values assessed at the species’ normal environmental temperature. 6 log Psi —— et dlog[Lac] _O log Psa } logiurate | Species Pso(pH7.8) (1mmol/1. lactate) -0.56 -0.46 -0.30 -0,27 -0.21 -0.21 Palaemon elegans' Apohyale pugetiensis' Traskorchestia traskiana® Bythograea thermydron® Cancer pagurus” Callinectes sapidus” 8.9 8.9 3.9 1.6 Carcinus maenas'? 10.9 3.9 24 15,1 Megalorchestia californiana®’ 14.7 2.8 (1.419 7A 5.2 2.5 5.6 17.6 4.9 16.6 15.1 12.0 7.9 7.2 -0.20 -0.19 -0.17 -0.13 -0.10 -U.19 -0.17 -0.16 -0.10 -0.08 -0,06 -0.06 -0.04 -0.03 -0.03 Uca pugilator® Cancer magister* Acanthephyra smith? Gnathophausia ingens* 4 . § Austropotamobius pallipes” 2 Hyas coarctatus” 7 Ocypode saratan Penaeus japonicus* Hemigrapsus nudus’ Acanthephyra acutifrons* Glyphocrangon vicaria* Oplophorus gracilirostris* Talitrus saltator’ Holthuisana transversa’ Geograpsus crinipes* Gecarcoidea natalis® Gecarcoidea lalandii® Birgus latro® Coenobita clypeatus® o Source Bridges and Morris (1985) Spicer and McMahon (1990) Spicer and McMahon (1990) Sanders and Childress (Pers Com.) Truchot (1980) Booth er al. (1982), Bridges and Morris (1985), deFur et al. (1990) Byrne, Morris, Spicer and McMahon (Unpub.) Morris and McMahon (1989) Sanders and Childress (1990a) Sanders and Childress (1990b) Truchot (1980), Lallier and Truchot (1989a) Morris et al. (1986a), Morris et al. (1985a) Morris and Bridges (1989) Bridges and Morris (1985) Spicer and McMahon (1990) Lallier and Truchot (1989b) Morris, Greenaway and McMahon (Unpub.) Sanders and Childress (1990a) Arp and Childress (1985) Sanders and Childress (1990a) Spicer, Taylor, McMahon (1990) Morris et al. (1988a) Morris, Greenaway, McMahon and Sanders (In Prep) Morris, Greenaway, McMahon and Sanders (In Prep), Morris, Greenaway, McMahon and Sanders (In Prep) Morris e: al. (1988b) Morris and Bridges (1986) #Values calculated using author's coefficients, “Lagoon species values for pH 7.6, "Extrapolated to pH 7.8 'Rockpool, *Sublittoral, “Intertidal, “Pelagic, “Freshwater. “Hydrothermal vent. 7Amphibious/Semi-terrestrial, *Terrestrial sus are good oxyregulators with a low Pc (Table 1). Holthuisana shows no obvious Pc and is an oxyconformer (Greenaway ef al., 1983b) and presumably elects to breathe air whenever the water becomes hypoxic. A further interesting adaptation to bimodal breathing by Holthuisana is the facultative switching of blood flow from the gills (water breathing) to the lungs (air breathing); the ratio being 1:6.6 in favour of lungs while in air and 1:4.1 in favour of gills in water (Taylor and Greenaway, 1984). This phe- nomenon almost certainly occurs in other spe- cies but it remains to be demonstrated. Other bimodally breathing species such as Cardisoma show well developed lungs and are equally facile at breathing air as water (McMahon and Burg- gren, 1988) but appear to be dependent on water for ion and osmoregulatory reasons (Greenaway, 1989). TERRESTRIAL — AIR BREATHING A number of adaptive features exhibited by the more accomplished air-breathing amphibious species are characteristic of and considerably more developed in terrestrial species. Further modification of the gills to aid in air-breathing occurs in a number of species, e.g. Ocypode (Greenaway and Farrelly, 1984). Most air- aay] breathing species however, show reduction in vill area and extensive elaboration of the branchiostegal lining for gas exchange (Fig. 6). In Birgus /atro the gills take no part in oxygen uptake (Greenaway ef a/., 1988), Although crustacean lungs have assumed varying forms data (rom several species indicate thal the lungs are very efficient in O2 uptake, in part due to the attenuation of the epithelial cells and chitin laver (MeMahon and Burggren, 1988; Greenaway and Farrelly, 1990). For example in 4 of 5 disparate species of air breathing crab Greenaway and Farrelly (1990) found that the pulmonary blood contained significantly more oxygen than the pericardial blood and the difference could be as much as 35% more, indicating thal lungs ure more important than gills. Indeed the most ter- restrial species haye become obligate air breathers and when immersed in waler become increasingly anaerobic due to the reduction in oxygen diffusion at the exchange surface, c.g. Gecarcinus lateralis (Taylor and Spencer-Da- vies, 1982). Similar observations have heen made for terrestrial amphipods (Spicer and Tay« lor, 1987). The evolution of lungs has also led to increased arterial PO2 in some cases signili- cantly greater than 100 torr (Pseudotlelphusa, Innes et al., 1986; Birgus, Greenaway et al. 1988), indicating that in resting animals the physically dissolved Oz supplies a significant part of the oxygen demand of the animal. One considerable advantage in breathing air is the relatively greater oxygen content (57mmoi.L'.torr') compared with water (1.8 — 2.2 mmol.L.torr') which together with a much reduced kinematic viscosity (~8%) cun make extracting oxygen from air considerably. less ex- pensive. As a consequence there is a tendency to make energetic savings by reducing the rate of ventilatory pumping, without reducing oxygen uptake (Table 3). Many amphibious species show markedly different rates in air and water (Table 3). Relatively elevated PCOd in the blood is the normal condition for air breathers and is a con- sequence of the parameters of the Fick equation (see above). For air breathing species the re- duced ventilation with respect to environmental oxygen availability will exacerbate problems of COz excretion. Movement of COz out of the animal into air requires a greater diffusion gradient and therefore higher internal PCO2 values. There is some evidence that ventilatory drive may become increasingly COa sensitive in terrestrial species (McMahon and Burggren, MEMOIRS OF THE QUEENSLAND MUSEUM en —__—_—_—_—_———— rs j se => actectal T io, ) — seman mite eT 4 { a0 + a + ey oe 7 | +> — pt n lead. ee ere reer se a 4 ae oF fa fe ee 20 2s te oe ee et ad = > —— ~~ r + 1 ’ Pew 3+ Ware) | AF = ‘ a a4 & AIR BRRATHINE =~ S03 4 © 410 Sw 18 tm 33 a2 8 ee ~- : es = ” t* i me - ‘? * t. | a ? ‘ 2 2 8 ete be re ee ew as ew ew oe ve = > 2 of ta . ue et ee . jbwecrarel * ! “ts — —8 aaah el. » * es I no $$ $$__—___—_ 22 @ b ® @ be 45 64 Os oe 363334 se bene Time (ny FIG, 5, Respiratory gas parameters, pH and [L-lac- tate | measured in the bload of Hemigrapsus nudus belore, during and for 6 hours after 24 h air breath- ing (indicated by horizontal bars). Arterial and venous QO2 content is given (Morris, McMahon and Greenaway, unpubl). 1979). The excretion of COz may occur across the lungs as well as the gills and appears to be facilitated by carbonic anhydrase (CA) which catalyses the COz <-> HCO3- reaction, thereby accelerating the diffusion of CO2 from the blood and into the epithelial cells of gas exchange organs. While the amphibious H. nudus has sig- nificant but low levels of CA in its lungs the lerrestrial Birgus has CA at >25% the specific activity of the gills which may explain the meas- urable CO32 loss from the blood passing through the lungs (Morris and Greenaway, 1990). The high CO; levels in terrestrial species does not resull ini noticeably lower blood pH cf. aquatic specics. his may be in part because of the usually h gher He concentrations (for values see MeMah- n and Burggren, 1988) which may exceed 00 mg.mL" in some land crabs. The high concentrations of Hc in the blood of most terrestrial species has been interpreted as increasing oxygen supply to the tissues (McMa- hon and Burggren, 1988) and while this is im- portant during any sustained exercise the efficacy of the lungs together with He O2 affinity RESPIRATORY GAS EXCHANGE IN CRUSTACEANS 25) (Table 2) ensures that dissolved O2 makes an important contribution. During exercise the He oxygen saturation in Birgus falls from 100% arterial and ~60% venous to only 80% and 25% by which time L-lactate concentrations have risen to over 22 mmol.L" (Greenaway ef al., 1988), indicating that the O2 limiting step is diffusion from the blood into the mitochondria. Tn more than 20 species of terrestrial decapod studied the haemocyanin shows no significant sensitivity to L-lactate or urate (Table 2). Indeed there appears to be a trend for increased air- breathing to be correlated with lower sensitivily. The result is that the allosteric modulation of He oxygen affinity used by aquatic organisms to optimise Oz delivery during exercise or en- vironmental hypoxia, or by proto-amphibious species to temporarily stabilise blood gas trans- > port during forays into air, is not utilised by well adapted air-breathing species. Instead the low kinematic viscosity and high O2 content of air appears to make compensation via changes in ventilatory and heart rates more economical. A further consideration is that urate is the prime nitrogenous waste in at least one species (Birgus latro) and accumulates as solid in the body of this and other terrestrial species (Greenaway and Morris, 1989; and citations therein). Urate solu- tions are saturated at low concentration and pre- sumably there is no advantage in selecting for an effector substance which is always at maximum concentration. The He of terrestrial species appears to be characterised by low pH sensitivity, the small Bohr shifts being approximately 50% the mag- nitude found for rock pool species (Table 2). The immediate consequence of this is that the effect of very large mixed acidosis (PCO2 and L-lac- tate increase) often < pH 7.0 e.g. Birgus latro (Greenaway er al., 1988) on He oxygen affinity is minimised. There have been several sugges- tions of a correlation between terrestrialily and He Oz affinity but a consideration of data col- lected at the species normal environmental temperature (and constant [lactate]) indicates no irend (Table 2). The problem is complicated by the modulator sensitivity of He in many aquatic species. The only modulating substance of note in terrestrial species would appear to be Ca Which may vary in response to drinking water quality, moult stage or during exercise induced acidosis. Values for lag 6P50/dlog [Ca] for water breathers range from -0.28 for Carcinus (Tru- chot, 1975) to -0.82 Callinectes (Mason et al, 1983). This coefficient varies from near 0) FIG. 6. Crustacean lungs. A, Corrosion cast of part of the vasculature of the lung of Ocypode cordi- manus. Note the single set of yessels (A), which interdigilates with the efferent vessels (E). Haemolymph returning from the lung is collected by a pulmonary vein (pv), which opens into the pericardial cavity. B, Diagrammatic illustration of the pattern of haemolymph flow through the lungs in terrestrial crabs of the families Gecarcinidae, Grapsidae and Sundathelphusidae. Afferent haemolymph passes to the respiratory membrane three times before reaching the pulmonary veins. AFF, Afferent vessel; GEL, gas exchange lacunae; RPV, respiratory poral vein; PV, pulmonary vein, C, Corrosion cast of the vasculature of one lung at the letrestrial crab Geograpsus grayi. Note the very large pulmonary. vein (pv), which collects efferent haemolymph and conveys il to [he pericatdial cav- ity. A large vessel on the inner dorsal margin of the lung distributes afferent haemolymph (arrows) (figures and legends reprinted with permission frani Greenaway and Farrelly, 1990). 252 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 3. Ventilatory frequency of some selected decapods from aquatic, amphibious and terrestrial habitats. Showing the tendency to decreased rate when breathing air. AQUATIC Cancer magister Cancer productus Cancer pagurus Callinectes sapidus AMPHIBIOUS Cardisoma guanhumi Gecarcoidea lateralis (AIR) (AiR) (WATER) (Air) (WaTER) Sudanonautes aubryi monodi TERRESTRIAL Birgus latro Coenobita clypeatus Holthuisana transversa Pseudothelphusa garmani McMahon et al., 1979 deFur and McMahon, 1984a Bradford and Taylor, 1982 Booth et al., 1982 Burggren et al., 1985 Taylor and Spencer-Davis, 1981 Cumberlidge, 1986 Smatresk and Cameron, 1981 McMahon and Burggren, 1979 Greenaway et al., 1983a Innes et al., 1987 *Employs a ‘lung pump’ *Some evidence for ‘lung pumping’ (Coenobita, Morris and Bridges, 1986; Holthui- sana, Morris et al., 1988a) to between -0.3 and -0.5 for several terrestrial species of Geograpsus and Gecarcoidea (Morris, Greenaway, McMa- hon and Sanders, unpubl.). Amongst the Amphi- poda, the semi-terrestrial Talitrus saltator (Spicer et al., 1990) and Orchestia gammarellus (Taylor and Spicer, 1986) produced coefficients of 0 and -0.33 respectively. Calcium sensitivity calculated from data for semi- and fully terres- trial isopods (Sevilla and Lagarrigue, 1979) in- dicate values ranging from -0.28 to +0.53. The significance of this Ca effect, while appreciated for amphibious/semi-terrestrial species (above), remains to be determined in terrestrial species. The temperature sensitivity of O2 transport warrants some consideration. In a number of semi-terrestrial/supratidal species the tempera- ture sensitivity is reduced near to the environ- mental mean (O. saratan 8H = -3 kJ.mol", C. clypeatus -14.8 kJ.mol'; Morris and Bridges, 1985, 1986) and may reflect the varying tem- peratures that occur in beach areas. In contrast the arid-zone crab H. transversa also potentially experiences fluctuating temperature but shows no special adaptation of the Hc (8H = -54kJ.mol') but instead may avoid temperature extremes during the aquatic and fossorial phases of its life cycle. The semi-terrestrial amphipod Talitrus saltator shows a marked temperature sensitivity and Spicer etal. (1990) also suggest that cryptic and fossorial phases enable this species to escape temperature extremes which have promoted low temperature sensitivity (-11 to -21 kJ.mol') in a range of supratidal amphipod Hcs (Taylor and Spicer, 1986). The majority of truly terrestrial species inhabit tropical/sub-tropical rainforests which are characterised by remarkably constant temperature and high humidity. Geograpsus crinipes, G. grayi, Gecarcoidea lalandii, G. natalis and Birgus latro all taken from the rainforest of Christmas Island all show high temperature sensitivity, at least up to 30°C (Morris et al., 1988b; Morris, Greenaway, McMahon and Sanders, unpub.), whereas Grap- sus tenuicrustatus and Geograpsus stormi taken from shore rocks, beach rubble and cliff faces show much lower sensitivities (-21 and -1.5 kJ.mol'). The tentative conclusion is that mini- mising the effect of temperature on blood O2 transport is as important to terrestrial species from eurythermal habitats as to inter- and suprat- idal species. In general the blood of air breathers has become increasingly independent of bio- chemical modulators and instead the animals appear to rely on morphological and mechanical compensation mechanisms. Dehydration could present a problem for air breathing species. Data from the high-shore Cy- RESPIRATORY GAS EXCHANGE IN CRUSTACEANS Oxygen Consumption Rates Midwater and Benthic Species as ad e 3 * 25 2 - Ranifie smotihg = al a H / 1 = . J a _ as oe — ———_ - . — “ * 5 = Soo 400 600 boa 4000 1200 4400 Depth m FIG. 7, Oxygen consumption rates trom 8 variety of non-migraling pelagic species indicating reduced O2 uptake in the deeper dwelling species. The Oz uptake rate of benthic Species appears io remain relatively constant and independent of depth (hori- zontal line), The rates for pelagic and benthic torms coincide near 1200 m (data from Childress, 1975; Mickel and Childress, 1982b; Childress and Mickel, 1985). clograpsus lavauxi suggest that under normal circumstances loss of body waler does nol alfect O» uptake (Innes er al., 1986). Severe dehydra- tion of Coenobita clypeatus appears to reduce O2 consumption, without significant effects on CO2 excretion, although the reasons for this are un- clear (McMahon and Burggren, 1988). Delydra- tion is likely to be important only under exceptional circumstances but requires further investigation. OCEANIC SPECIES Oceunic crustaceans can be divided on the hasis of habjiat, sublittoral, pelagic and benthic, Vertically migrating species experience very different temperatures, oxygen availability and pressures at different depths. Benthic specics and non-migratory pelagic species live at near con- stant temperatures and high pressure. The ben- thic species include the rather special case of the hydrothermal vent fauna which, in addition to high sulphide and metal levels in the water, voterate high and widely varying temperature as well as high pressure. There have been relatively few studies of the effect of temperature on oxygen uptake rates of oceanic species. Pelagic crustaceans living in midwater environments tend to show increased rates with temperature, with Qyy values of 1.5 to 3,0 (Teal, 1971; Childress. 1977), It is now well established that deep-living pelagic crustaceans have considerably lower O2 uptake rates than do 253 shallower-living pelagic species (Childress and Mickel, 1985), often by a factor of 20 but that this effect declines below 1500 m (Fig, 7). This decline is more than can be accounted for by temperature effects and cannot be explained by pressure (Mickel and Childress, 1982a). Childress and Mickel (1985) suggest that itis the relaxation of selection for strong swimming abilities at greater depth that allows fora reduced O2 demand. In migratory species the response to tempera- (ure is influenced by oxygen availability and hydrostatic pressure. The ecological signifi- cance of temperature-pressure interactions was shown by Childress (1977) Working on (he mi- graling copepod, Gaussia princeps. This species was most Sensitive fo pressure at shallow depths (100 — 300 m) during the night but that during the day, below 400 m within the oxygen min- imum layer temperature determined rates. A lowered rate of oxygen uptake while ina hypoxic environment would be of direct benefit. On the basis of such studies Vernberg (1983) supports the model of George (1979; Fig. &), This sug- gests that vertical migrators maintain a constant oxygen uptake as a result of the opposing effects of temperature and pressure changes, Deeper in the oxygen minimum layer cnvironmental PO2 may become very low (<2? lor) and oxygen potentially limiting. Midwater species appear to be adapted (o this situation, however, and most exhibit critical oxygen tension (Pc) below that normally encountered in the oxygen minimum layer (Childress, 1975; Table 1). This seems ta be achieved by maintaining a high flow of water over the gills, which have unusually high surface area and a high diffusion capacity (~10 fold greater normal) leading to a low 6PO2 across the gills (Belman and Childress, 1976). There are few deep-living brachyuran species and very few studies of benthic Crustacea. Ex- isting data indicate that there is no decrease in the O2 consumption of benthic species in de- pendence of habitat depth (Childress and Mickel, 1985), Interestingly, the O2 consump- tion rales of midwater and benthic species con- verge at about 1200 m (Fig. 7). Respiratory gas transport in oceanic crustaceans has been infrequently examined bul Arp and Childress (1985) examined the blood of a benthic (1800 m) shrimp, Glyphocrargon vicarid, The oxygen binding properlies of this species do not appear loo exceptional, with a modest Bohr shift ( = -0.37, 2°C), a relatively low affinity (Pso = 9.0 torr, pH 8.01, 2°C) and 254 MEMOIRS OF THE QUEENSLAND MUSEUM Metabolic Rate of Vertical Migrators MO, 1 28 25 15 11 Effect of Effect of 75; Pressure Ternperature | 5.0 Pressure Temperature (atm) 499 40 Cc 125 35 150 30 175 20 200: 2.0 Constant rate after George, 1979 FIG. 8. Demonstrating, using the model of George (1979), how the opposing effects of increasing pres- sure and decreasing temperature on the metabolic rate of vertically migrating crustaceans can operate to produce a constant rate throughout the water column. telatively low co-operativity (nso = 2.6 — 3.2). An unusual aspect of the haemolymph from ben- thic species is the marked increase in the Bohr factor (pH sensitivity) at higher temperatures, which has also been observed in the brachyuran Hyas coarctatus (Morris and Bridges, 1989). The oxygen affinity of haemocyanin from these species is remarkably insensitive to temperature, for G. vicaria 8H = -10.3 kJ. mol’! (calculated from Arp and Childress, 1985) and -6.4 kJ.mol'! for H. coarctatus (Morris and Bridges, 1989). The normal sensitivity would be nearer to -35 kJ.mol' (Bridges, 1986, table 3). It is possible that considering these animals usually occur in cold, stenothermal environments that these changes with increased temperature do not have any physiological significance. In terms of modulator sensitivity there seems to be no special adaptation to life in the deep ocean, for example G. vicaria has little sensitiv- ity to L-lactate ( dlog Pso/ dlog [lac] = -0.04) while H. coarctatus, which does extend in shal- lower water shows a greater sensitivity (-0.17). In recent investigations Sanders and Childress (1990a) have examined the oxygen transport function of Hc from a group of pelagic species, some vertical migrators. The migratory species had lower oxygen affinities but higher in vivo lactate levels than the non-migratory species. These shrimp Hes exhibited, however, very little sensitivity to L-lactate and temperature seems much more important. The non-migratory spe- cies had low temperature sensitivity (6H = 0 to -5.6kJ.mol"', cf. G. vicaria above) whereas there were very large temperature sensitivities in the migrators ( 6H = -135 to -140 kJ.mol’). Sanders and Childress (1990a) suggest that low tempera- ture sensitivity is not a feature of benthic crustaceans alone but rather of deep living forms, in stenothermal environments. They also con- clude that increased O2 affinity at lower temperatures is adaptive, by maintaining O2 up- take, for migrating species as they move down into the relatively cold and hypoxic oxygen min- imum layer. In the warmer surface waters, where 0 = A. smithi f -200 -| Night >20°C fd -400 — a Depth (m) we z -600 , A. | acutifrons . & s A. smithi -800 — Day 3 - 6°C " -1000 rs r . 1 0 50 100 150 200 Po, (torr) 10 ~— ® gf ieee | 0.8 s go * g | — = ‘ and anaerobic lactic acid production, that a PH insensitive pigment is advantageous. Hydrothermal vent crustaceans while difficult and costly to study are of special interest due to the unique nature of their island habitats, The vent brachyuran, Bythograea thermydron, shows oxygen consumption rates in the normal range for shallow water brachyurans and does not show unusual teniperature sensitivity of O2 uptake (Mickel and Childress, ]Y82b), Oxygen binding by the haemocyanin of B. thermydray is, however, distinctly unusual (Sanders er al, 1988), In Bythograea an increase from 2 to 10°C causes an affinity increase ( OH = +23 kJ.mol') but from 10 to 20°C behaves normally (OH =-60) kJ.mot'), This was in contrast to the blood of the vent caridean Alvinocaris lusca which exhibited a reverse temperature effect over the entire temperature range, so that affinity was lower al luw temperature ( 6H = #13 kJ.mol'; Sanders e¢ al., 1988). The Bohr shift inA. /usca is twice that of B. thermydren (the Bohr shif\ is dependent on the hydrothermal vent site; Sanders, pers. com.) sug- gesting that in A. /usca significantly decreased affinity via. a low pH will enhance O2 delivery to the tissues. B. thermydron, with a law pl sensi- tivity, experiences decreased QO? affinity at low and high temperature. Al low temperatures the Qyo effect will reduce oxygen demand. As. temperatures increase nearer to the vent waler PO: decreases and Bythograew responds with 235 -. ————_ - Lz - ib - / | (torr) * e | % - oe ae O.6 Pe 9,4 log Pso 0.3 CO, Bani shirt . ® INK > 50 mmol/L a.0 i t 72 74 Te 7.8 pH FIG, 10, The oxygen affinity (log Ps) of haemoey+ arin from the mesopelugic shrimp Notostomus gih- basus is shown to behave normally with respect to pH but the aftinity and pH sensitivity are signifi- cantly modified by the presence of high concentra~ tions of NHa+ and NH3. Under jn vive conditions of high ammonia und trimethylamine the Oxygen affinity is both much lower and insensitive to pH (Sanders, Morris, Childress and MeMahon, un- publ), pronounced hyperventilation (Sanders e/ al., 1988) which is the normal response of shallow water brachyurans to hypoxic stress and results in an exceptionally low Pe (Mickel and Childress, 1982b); which should be compared with rock pool species (Table 1), This species also has pronounced anaerobic metabolic capac- ity for short hypoxie forays (ef. intertidal spe- cies) and interestingly L-lactate has a potentialing effect on the haemocyanin of this species, which is again reminiscent of shallow water forms. What is unusual is that thiosul- phate, the detoxified product of vent sulphide, in Bythograea also increased He oxygen affinity (Sanders and Childress. in prep.). 8. thermydron shows some specific adaptations to the variable temperature of its habitat but shows no unusual adaptations to pressure and retains. the aquatic brachyuran response to hypoxia, To conclude, the Crustacea show a range of sophistication of respiratory gas exchange and transport, Adaptations oceur at the cellular and enzyme level with respect to temperature sénsi- tivity in order to regulate O2 demand and CO production, and are exhibited by species from various habitats, Environmental hypoxia is met either by a lowering of the Pe, by improving oxygen uptake efficiency and regulating: de- mand, or by a behavioural response, air breathe ing. The emergence response may represent the first sleps towards terrestrialism. Aquatic and proto-amphibious species take advantage of a 256 tange of metabolites to regulate haemocyanin oxygen affinity and this appears to have evolved from an exercise response. Some freshwater, intertidal, vertically migrating pelagic and vent species which experience varying temperature show adaptation of hacmocyanin function. Spe- cies from more stable temperature regimen, both aquatic and terrestrial, show fewer adaptations in respect of temperature, Fully terrestrial spe- cies show marked changes in the morphology of the gills and especially the branchiostegal mem- brane. The evolution of a lung has allowed the Crustacea to lake advantage of the relatively greater concentration of O2 in air but in the most adapted species has made them obligate air breathers. Terrestrialism is correlated with a decreased utilisation of biochemical modulation of blood gas transport and an increased impor- tance of morphological and mechanical compen- sation mechanisms. 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MORRIS. S.. GREENAWAY, P. AND MCMAHON, B.R. 1988a, Oxygen and carbon dioxide transport by the haemocyanin of an amphibious crab, Holthuisana transversa. Journal of Comparative Physiology 157: 873- 882. 1988b. Adaptations to a terrestrial existence by the robber crab Birgus latro |. An in vitre investigation of blood gas transport. Journal of Experimental Biology 140: 477-491. MORRIS, 8S. AND MCMAHON, B.R. 1989, Poten- tiation of hemocyanin oxygen affinity by cate- cholamines in the crab Cancer magister: a specific effect of dopamine, Physiological Zoology 62: 654-667. MORRIS, S, AND TAYLOR, A.C. 1983. Diurnal and seasonal variation in physico-chemical condi- lions within intertidal rock pools. Estuarine coastal and Shelf Science 17; 151-167, 1985a, Oxygen consumption by Palaemon elegans (Rathke) in response to temperature change: a determinant of distribution. Experimental Bi- ology 44; 255-268. 1985b. The respiratory response of the intertidal prawn Palaemon elegans (Rathke) to hypoxia and hyperoxia, Comparative Biochemisiry Physiology BLA: 633-639. MORRIS, S., TAYLOR, A.C,, BRIDGES, C,R AND GRIESHABER, M,K. 1985, Respira- tory properties of the haemolymph of the in- tertidal prawn Palaemon elegans (Rathke) Journal of Experimental Zoology 233: |75- 186. 254 MORRIS. S,., TYLER-IONES, R. AND TAY- LOR, E.W. 196a. The regulation of haemocyanin oxygen affinity during emer sion of the crayfish Austropotameblus pal- fipes. 1. An in vitro investigation of the interactive effects of calcium and L-laciate on oxygen affinity. Journal of Experimental Biology 121: 315-326. MORRIS, S., TYLER-JONES, R.. BRIDGES, C.R. AND TAYLOR, E,W. 1986b, The reg~ ulation of haemocyanin oxygen affinity during emersion of the eraylish Austropola- mobins pallipes. IL. An investigation of in vive changes in oxygen aftinity, Journal of Experimental Biology 121; 327-337, NEWELL, R.C, 1979. ‘The biolagy of intertidal animals’. (Marine Ecological Surveys Ltd; Faversham, U.K). POWERS, L.W. AND BLISS, D.E. 1983. Terrestrial adaptations. 271-333. In F.J. Vernberg and W.B. Vernberg (eds.) ‘The biology of the Crustacea, Vol 8, Environmental adaptations’. (Academic Press; New York), RAMIREZ DE ISLA NERNANDEZ, S. AND TAYLOR, A.C. 1985. The effect of tempera - {ure on the osmotic and ionic regulation in the prawn, Palacmon elegans (Rathke), Ophelia 24: 1-15. SABOURIN, T.D, 1984. The relationship between Muctuating salinily and oxygen delivery in adult blue crabs. Comparative Biochemistry Physiology 78A; 109-118. SANDERS, N.K,, ARP. A.J. AND CHILDRESS, JJ. 1988. Oxygen binding characteristics of the hemocyanins of two deep-sea hydrothermal vent crustaceans, Respiration Physiology 71; 37-68, SANDERS, N.K. AND CHILDRESS, J.J. 1988- Ton replacement a5 4 buoyancy mechanism in a pelagic deep-sea crustacean, Journal of Ex- perimental Biology 138: 333-343, 1990a. A comparison of the respiratory function of the haemocyanins of vertically migrating. and non-migtating oplophorid shrimps. Jour- nal of Experimental Biology 152: 167-187. L990b, Adaptations lo [he deep sea oxyyen min- imum layer: Oxygen binding by the hemocy- nain of the bathypelagic mysid, Gnathophansia ingens Dohrn. Biological Bul- letin 178: 286-294. SEVILLA, C. AND LAGARRIGUE, J.-G. 1979. Oxygen binding characteristics of oniscaidea hemocyanins (Crustacea; terrestrial iosopods). Comparative Blochemistry Physiology 64A; 531- 536. SMATRESK, NJ. AND CAMERON, J.N.. 1981. 240 Post-exercise acid-base balance and ventilstory control in Birgus lairo, (he coconul crab, Journal of Experimental Zoology 218: 75-82. SPICER, J.l. AND MCMAHON, B.R, 1990. Haemocyanin oxygen binding und the physi- ological ecology of 4 range vl talitroidean amphipods (Crustacea) |, pH, temperature and L-lactate sensitivity, Journal of Compurative Physiology 160: 195-200. SPICER, J.J. AND TAYLOR, A.C. 1987. Respira- tion in air and water of some semi- and fully terrestrial talitrids (Crustacea: Amphipoda: Talitridue). Journal of Experimentsl Marine Biology and Ecology 106; 265-277, SPICER, J.J, TAYLOR, A.C, AND MCMAHON, B.R, 1990, O2-binding properties of huemocy- anin from the sandhopper Talifrus saltator (Montagu, 1808) (Crustacea. Amphipoda), Journal of Experimental Murine Biology and Ecology 135; 213-228. TAYLOR, A.C. 1976, The respiratory responses of Carcinus maeias to declining oxygen tension, Journal of Experimental Biology 65: 309- 322. 1977, The respiratory response of Carcinus maenas (L.) to changes in environmental salinity. Journal of Experimental Marine Bi- ology and Ecology 29; 197-210). 1988. The ecophysiology of decapods in the rock pool environment, Symposium Zoological Saciety of London 59: 227-261. TAYLOR, A.C., MORRIS, 5. AND BRIDGES, C.R. 1985. Modulation of haemocyanin oxy- gen affinity in the prawn, Palaemon elegans (Rathke) under environmental salinity stress. Journal Experimental Marine Biology and Ecology 94; 167-180, TAYLOR, A.C. AND SPENCER-DAVIES, P 1981. Respiration in the land crab, Gecarcinus lateralis, Journal of Experimental Biology 93: 197-208, 1982. Aquatic respiration in the land crab, (ie- carcihus lateralis (Fréminville). Comparative Biochemistry and Physiology 7ZA: 683-658. TAYLOR, A.C, AND SPICER, J\I, 1986, Oxygen- transporting properties of the blood of two semi-terrestrial amphipods, Orchestia game marellus (Pallas) and QO. mediterranea (Costa). Journal of Experimental Marine Bi- ology and Ecology 97; 135-150. 1988. Functional significance of a partial-emer- sion response in the intertidal prawn Palue- mon elegans (Crustacea: Palaemonidae) during environmental hypoxia. Marine Ecology (Progress Series) 44: 141-147. MEMOIRS OF THE QUEENSLAND MUSEUM TAYLOR, E.W. AND BUTLER, P.J. 1978. Aquatic and aerial respiration in the crab Car- cinus maenas (L.) acclimated to 15°C. Journal of Comparative Physiology 127: 315-323. TAYLOR, E.W. AND WHEATLY, M.G, 1981. The effect of Jong-term aerial exposure on heart rate, ventilation, respiratory gus ex- change and acid-base status in the crayfish Austrepotamobius pallipes. Journal of Ex peri- mental Biology 92: 109-124. TAYLOR, H.H. 1990). Pressure-flow characteristics of crab gills: implications for regulation of hemolymph pressure, Physiological Zoology 63; 72-89, TAYLOR, H.H. AND GREENAWAY, P. 1984. The role of the gills and branchiostegites in a bimodally breathing crab, Halthutsana trans- versa’ Evidence fora facultative change in the distribution of the respiratory circulation. Journal of Experimental Biolagy 111; 103- Pal THOMPSON, R.K. AND PRITCHARD, A.W. 1969, Respiratory adaptations of two burrow- ing crustaceans Callianassa californiensis and Upogebia pugettensis, Biological Bul- letin 136; 274-287, TRUCHOT, J.-P. 1973. Fixation et transport de Voxygéne par le sang de Carcinus maenas: Variations en rapport avec diverses conditions de température et de sulinilé, Netherlands Journal of Sea Research 7: 482-495. 1975, Factors controlling the iy vitro and in vive oxygen affinity of the hemocyanin in the crab Carcinus maenas (L.). Respiration Physi- ology 24; 173-189. \980, Lactate increases the oxygen affinity of crab hemocyanin. Journal of Experimental Zoology 214: 205-208. 1986, Changes in the hemolymph acid-base state of the shore crab, Carcinus maenas, exposed to stmulated tidepool conditions, Biological Bulletin 170. 506-518. ‘TRUCHOT, J-P. AND DUHAMEL-JOUVE, A. 1Y80. Oxygen and carbon dioxide in the marine intertidal environment: Diurnal and tidal changes in rockpools. Respiration Physiology 39: 241-254, TEAL. I.M. 1971. Pressure effects on the respira- (ion of vertically migrating decapod crustacea. American Zoologist 11; 571-576, VERNBERG, F,J. 1983. Respiralory adaptations, 1-42. In F.J. Vernberg and W.B. Vernberg (eds) ‘The biology of the Crustacea, Vol 8, Environmental adaptations’, (Academic Press: New York)- RESPIRATORY GAS EXCHANGE IN CRUSTACEANS 261 VERNBERG, W.B. AND VERNBERG, F.J. 1983. sapidus. Journal Experimental Zoology 193: Freshwater adaptations. 335-363. In F.J. 265-274. Vernberg and W.B. Vernberg (eds) ‘The bic WHEATLY, M.G. AND TAYLOR, E.W. 1981. ology of the Crustacea, Vol 8, Environmental The effect of progressive hypoxia on heart adaptations’. (Academic Press: New York). rate, ventilation, respiratory gas exchange and WEILAND, A.L. AND MANGUM, C.P. 1975. The acid -base status in the crayfish Austropota- influence of environmental salinity on hemocy- mobius pallipes. Journal of Experimental Bi- anin function in the blue crab Callinectes ology 92: 125-142. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum OSMOREGULATION IN THE FRESHWATER SHRIMP, MACROBRACHIUM CARCINUS (LINNAEUS) River shrimps of the genus Macrobrachium are de- capods of great economic importance and are widely dis- tribuled throughout Mexico, principally M. carcinus, M, acanthurus, M- heterochirus and M. olfersit in the Gulf of Mexico, and M, americanum and M-. tenellum on the Pacific coast. Some of these shrimp require brackish water to complete (heir larval development and have different physiological responses to salinity. However, before culti- valion of these species many investigations of their physi- ological requirements are necessary, Osmoregulajion in decapods has been the subject of many investigations but data for the genus Macrobrachium are relatively few and most information available in this respect concerns M, rosenbergii. Moreira et a], (1983, 1987) have venfied the effect of salinity in the metabolic rate of the first zocul stages of M, avanthurus, M. amazonicum, M_ carcinus, M, heterochirus, M. holthuist and M, olfersii from Brazil, and McNamara (1987) studied osmoregulation in M. olfersti. The present paper reports the results of an investigation on the osmotic regulation in M. carcinus in relation to fast and slow salinity changes. Materials and Methods The osmoregulatory capacity in Macrobrachium care cinus was. estimated by comparing haemolymph osmotic concentration with that of the external medium. Juveniles and adults (10.67-13 em and 70-125 g, length and weight respectively) were collected in the River ‘La Antigua’, Ver., Mexico. The animals were acclimated in 70 Ltanks in the laboratory at 20°C and 0 ppt salinity for 45 hours, After that, groups of 10 to 20 animals were placed in individual tanks lo carry oul (he experimen|al protocol; this included twoslow osmolarity treatments (0-7 ppt and 0-14 ppt) and two fast treatments (0-28 ppt and {}-35 ppt). One group was kept al 0 ppt throughout the experiment and served as a control. Osmolarity of the media Was adjusted using a hand refractometer, reading the equivalent salinity in ppt. The osmotic pressure of 30 wh samples of haemo- lymph and external medium was determined in triplicate with a micro-osmometer ‘j-Osmette' (Precision Systems Inc.) every 6 hours to complete 168 hours of total observa-~ tion. Haemolymph was obtained by puncture of the peri- cardjc cavity with a capillary pipette, after the organisms had been dried with an absorbent tissue: samples were then centrifuged at 3000 rpm for 10 seconds, Concurrently pleopod selae were examined to determine moull stage, MEMOIRS OF THE QUEENSLAND MUSEUM Results and Discussion Osmotic préssure méasurements indicate that the organisms were hyperosmotic in freshwater and low salinities, maintain- ing their HOC (haemolymph osmotic concentrations) between 400 and 500 mOsm/kg at 0 to 15 ppt, similar to M. olfersit and M. potiuna (Moreira ef ai, 1983). On the other hand, the isosmoltic point was achieved near 490 mOsm/kg (17 ppt) compared to the value of 492 mOsm/kg given for postlarvae of M. carcinus (Moreira et al., 1987), The species remain isosmotic at high salinities (above SUU mOsm/kg) increasing their HOC with the external concentration, especially al salini- ties between 17 and 25 ppt. Finally, the specimens in premoult Stage had a greater HOC than organisms in postmoult stages, with values of 327 and 421 mOsm/kg respectively; the smallest values occurred in individuals just moulted (408 mOsm/kg). On the other hand, the species was isosmotic in the intermoult stage, similar ta M, rosenbergii (Stern et al., 1986). Acknowledgements The author wishes to express his gratitude to J.A, Viccon and A, Esquivel for reviewing the manuscrip! and ta Biology Investigations Center of Xalapa of University of Veracruz. This research was partially supported by CONACYT (National Council of Science and Technology) and Univer- sidad Autonoma Metropolitana. Literature Cited McNamara, J.C. 1987. The time course of osmotic regulation in the Freshwater shrimp Macrobrachiwmolfersil (Wieg- mann) (Decapoda, Palaémonidae), Journal of Experi- mental Marine Biology and Ecology 107; 245-251, Moreira, G.S., McNamara, J.C., Shumway, S.E. and Moreira, P.S, 1983. Osmoregulation and respiratory me- tabolism in Brazilian Macrobrachium (Decapoda, Palae- monidae). Comparative Biochemical Physivlogy 74A(1): 57-62. Moreira, G.S.. Ngan, P.V. and Shumway, S.E. 1987. The effect of salinity on the osmo-ionic regulation of Macrobrachium carcinus. (Linnaeus). Bulletin of Marine Science 41(1): 639p, Stern, S. Barut, A. and Cohen, D, 1986. Osmotic and ionic regulation of the prawn Macrobrachium rasenbergti (De Man) adapted to varying salinities and ion concentrations. Comparative Biochemical Physiology. 86A(2); 373-379, B,G. Signoret Universidad Autonoma Metropolitana Xochimilco. Depto. El Hombre y su Ambiente. Calz, Hueso 1100. Col. Villa Quierud. C.P 04960, México, DF. México. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum BEHAVIOUR OF CRUSTACEA: ECOLOGICAL AND SOCIAL PERSPECTIVES SANDRA L. GILCHRIST Gllehrist, $.L. 1991 09 01, Behaviour of Crustacea: ecological and social perspectives. Memoirs of the Queensland Museum 31. 263-275. Brisbane. ISSN 0079-8835. Visual, chemical, acoustical, and tactile information can vary crustacean responses to social and ecological conditions. The relative importance of the types of cues received can vary in marine, semi-terrestrial, and terrestrial enviranments. Some species experience only one ol these types of habitats throughout their lifetimes while other species encounter all three habitats during particular life stages, Variations of ecological parameters within habitat Jend specitic context 10 actions and reactions exhihited by decapods. Population dynamics and social behaviour of decapod crustaceans are reveiwed with reference lo how age structure and ecological conditions influence perception of environmental and social signals. Of particular interest are cues which relate to development of space use, home Tange, territoriality and food gathering relative to potentially limiting abtotic and bivtic resources, As model systems, specific case analyses will be made for hermit crabs and tree crabs. [] Crustacea, behaviour, age, structure. Sandra L. Gilehrist, Division of Natural Sciences, New College of USF, Sarasota, FL USA; 6 July, 1990. Successful invasion of terrestrial habitats by crustaceans is limited to relatively few species scattered among a small number of taxa. Only one semiterrestrial shrimp Merguia has been described (Abele, 1970; Bliss, 1968; Gilchrist ef al., 1983); however, little is known of its be- haviour or physiology. Many land crabs spend a large amount of time in terrestrial habitats, al- though most still require an aquatic medium for reproduction (see Burggren and McMahon, 1988 for a discussion of terrestrialisation), Ter- restrial species have some obvious external var- jations which differ from aquatic counterparts in respiratory apparatuses and in appendages (espe- cially appendages used in arboreal movement), Behavioural modifications are much more com- mon in crabs existing in terrestrial environments than in aquatic environments, especiully relative to locomotion, cammunication, feeding, mating, gas exchange and osmoregulation, Development of offspring also tends to be more abbreviated as crustaceans become more terrestrialised (Mer- guia; Abele, 1970; Burggren and McMahon, 1988), Age structure of the various populations alsa differs. For example, in terrestrial species ju- veniles rarely are encountered among adults; while in aquatic species, there may be a wide size range of individuals occupying a single habitat. Cannibalism has been noted commonly among some land crabs and may maximise distribution of food materials acquired during larval stages while reducing reproductive cost of consuming one's own offspring broadcast into an aquatic environment through supplying materials to sib- ling survivors (Wolcott, 1985; Helfman, 1979). While potential cannibalism may explain some age class distribution patterns, ecological factors such as environmental stress and predation by non-conspecifics are also important. There are differences in behaviour between aquatic and terrestrial juveniles as well as striking variations between juvenile and adult conspecifics as- sociated with physiological constraints and pre- dation. However, differences between behaviours of the aquatic and terrestrial species seem to appear after cmergence onto land. An exhaustive review of behavioural varia- tions inter- and intraspecifically for aquatic ana terrestrial crabs is beyond the scope of this analy- sis. Rebach and Dunham (1983) edited an excel- lent series of papers dealing with various aspects of behaviour. In this study, ! willexpand on some of the topics discussed in their series relative to age structure and ecological context. To illustrate behavioural alterations relative to age structure and ecological conditions, 1 will limit this discussion to selected representatives of the Anomura (Birgus, Calcinus, Clibanarius, Coenobita, and Pagurus) and Grapsidae (Ara- jus), These genera show varying degrees of so- ciality as well as a range of terrestrialisation. AGE STRUCTURE The literajure Is replete with examples of com- 264 mon occurrences of adult and juvenile crabs in aquatic habitats. Groups may gather for many reasons, for ex- ample exploitation of a common resource such as observed at areas where gastropod shells are released by predators (Gilchrist, 1982; McLean, 1974; Rittschof, 1980) and feeding sites (Scully, 1983) or aggregation to relieve environmental stress (such as shading or trickle cooling). Aquatic hermit crabs gathering in areas where gastropods are consumed (termed predation sites) are of a wide size range even at a single site (Gilchrist, 1982; Rittschof, 1980). Typically, crabs form in a semicircular pattern downstream of the predation site with larger, interactive crabs near the front of the group and smaller crabs near the rear. Shell exchanges are common and rapid at natural sites (Gilchrist, 1982; Rittschof, 1980), some mating occurs, and in less than 1% of observations cannibalism on a smaller crab takes place. Active physical interactions are common as the crabs establish a dominance hierarchy at such sites. In shell exchange experiments con- ducted in the field and the laboratory, rarely is mortality among opponents recorded (major works record no mortality: Abrams, 1981; Haz- lett, 1989; Imafuku, 1989). For the terrestrial hermit crab Coenobita compressus, newly meta- morphosed juveniles seeking shells do respond to simulated predation sites (crushed gastropods; Table 1) in association with more aquatic spe- cies. Preliminary light microscope observations suggest that as the land hermits animals molt and emerge onto land, setation patterns on the ap- pendages alter, becoming less dense and appear- ing shorter. Ghiradella et al. (1968) indicated that aesthetascs of Coenobita resemble chemore- ceptors of terrestrial insects. Adult Coenobita compressus do not appear differentially attracted to crushed gastropods in greater numbers than to other carrion. Rittschof and Sutherland (1986) noted that chemical cues stimulated feeding be- haviour of Coenobita rugosus, but did not seem important in eliciting shell seeking behaviour. Electron micrographic analyses of the setae and teceptors may reveal differences in morphology and function of these structures ontogenetically with the transition from aquatic to terrestrial habitats. It is interesting to note, however, that some intertidal hermit crabs observed in the trop- ics do not appear to respond to predation sites (Table 2) as frequently as more temperate coun- terparts. Clearly, they can respond to certain gastropod fleshes, however, it is not obvious whether nonresponse to other fleshes is control- MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 1. Responses of newly metamporphosed Coenobita compressus to simulated predation sites using G statistic with 1 df after correction for con- tinuity. Respondents control* | treatment Flesh type Acanthina brevidentata Thais melones Nerita scabricosta Cerithium stercusmuscarum Anachis varia Anachis fluctuata Anachis rugosa Nassarius exilis Mitra tristis Cantharus elegans Turbonilla panamensis Siphonaria gigas Siphonaria maura Conus brunneus Littorina aspera * Cage w/shell alone led behaviourally or at the receptor level. The mean size (hard carapace length) of crabs attend- ing flesh sites was 7.02 mm 1.65, indicating that for these experiments only medium to large crabs were attracted to gastropod fleshes. After a period of time (6-8 hours) hermit crabs in the experiment came to the flesh sites and consumed the gastropods. These crabs, like aquatic coun- terparts (Lepore and Gilchrist, 1988) may be attracted by degradation products such as putrecine and cadaverine. As terrestrialisation increases, physiological and physical constraints tend to separate activi- ties of different age groups both temporally and spatially. Herreid and Full (1986) observed that large Coenobita compressus travel faster than smaller crabs, doubling speed as leg length doubles. They also observed that smaller crabs expend more energy walking and climbing rela- tive to balancing the shell. Thus, it would be expected that smaller crabs which may be more subject to predation and dessication would move smaller distances from refugia. Adult crabs tagged in Panama moved several hundred metres a day while smaller crabs tended to make short forays from the jungle edge to the wrack line for feeding. When climbing, large crabs fell less frequently than small ones. Adult Birgus are large and somewhat solitary. Aggregations may be observed around a food source (Grubb, 1971) although burrows and rock CouUHKH WKH Cr SK SWI Kah BEHAVIOUR OF CRUSTACEA 265 TABLE 2, Relative attraction to gastropod flesh by Calcinus obscurus in intertidal and subtidal areas of Panama. Gastropods were crushed and placed beneath cages while controls were cages alone and a cage plus a shell (controls were not significantly different, thus were pooled in the analysis). Null hypothesis that responses were independent of flesh was tested using G Statistic with | df after correction for continuity. Intertidal Gastropod flesh Culebra Flamenco Caniharus ringens Cerithium stercusmuscarum Planaxis planicostata Anachis fluctuata Nerita funiculata Thais melones shelters (resting sites) are typically occupied singly. Very small individuals are not recorded co-occurring with adults (Gilbson-Hill, 1947). Much of the work with physiological parameters of Birgus has been done with smaller specimens (350,000 added to site in three years), populations of three species seemed to decrease while one species (P. pollicaris) increased only after two full years of shell addition (Fig. 3), added shells were assimi- lated into the populations, From these data alone, conclusions relating to shell use and recruitment over a long period of time seem uncertain. How- ever, factors independent of shell use or shell 7O 60 * Ppotiicoris @ Pompressus » Plongicarpus 50 4 shells ¥ added 30 | MEAN NO CRABS/m* SANDFLAT — hatch rate % surviving through glaucathoe [weighing [| n _|_— counting _| maclaughlinae v * weighing counting ee availability may be used to explain the observed patterns. In 1985 and 1986 a series of strong storms occurred in the sampling area during the primary breeding season for the crabs. Few gravid females were collected, suggesting that recruitment might be low during the next 6 months. In 1987, P. pollicaris was collected. in relatively high numbers during April and May but then decreased to near normal levels in June and July. During June and July stingrays moved into the area. Rays were observed harvesting the small hermit crabs in sandflat areas. Aggressive behaviour of female hermit crabs = Pmocloughlinoe complex bd spp a , ~ 1983 (984 1985 MONTH N NDJFMAMJJASONDJIFMAMJJASONOJUFMAMJIJASONODJIJFMAMI JY ASON OD 1986 1987 FIG. 3. Long term shell addition experiment to observe effects of available shells on recruitment. Shell additions did not significantly alter long term population patierns. BEHAVIOUR OF CRUSTACEA 269) TABLE 6. Water retention of shells and hermil crab desiccation relative to shell condition for Coenobita compressus in Pacific Panama. Shell type shell condition crab size Nerita scabricosta | with algae without algae hole in apex with algae without algae hole in apex Turbo saxosus with algae” without algae hole in apex with algae without algae hole in apex Thais melanes with alpae without algae hole in apex with algae without algae hole in apex X+sdtime to crab extension from shell (min) x + sd amount of waler retained (cc) after 1 hour full exposure How HH bs ie — 50 fi oo uo [s) HHA | aE t ia ” it was observed that prior to death crabs éxténded from shells and did not retract upon stimulation of abdomen; érabs Teaching this point were quickly rehydrated, ee shell had only sparse amounts of algae observable from aperture, does appear to alter during brooding. Neil and Elwood (1985) observed that gravid crabs (P. bernhardus) have decreased levels of attack and increased levels of defensive behaviour. They also note that shell exchange is infrequent. Gil- christ (1982) found that for Clibanarius vittatus, P. pollicaris, and P. maclaughlinae gravid females were more likely to have greater num- bers of shell co-inhabitants than males. Hazlett (1970) suggest a chemotactile discriminatory cue while Imafuku (1986) postulated that recep- tive females may emit a water-borne chemical which facilitates discrimination between the sexes. It is not unreasonable to speculate thal other organisms might use such chemicals to orient to a female as well. Further, these shell occupants were observed eating eggs as well as abdomenal appendages of the crabs. Gilchrist (1982) and Bertness (1981) observed that gravid crabs changed shells more often than nongravid ones, contradicting the observations made by Neil and Elwood. Perhaps this difference may be explained by variations in shell co-inhabitants in the various study areas. Current observations of P. longicarpus, P. maclaughlinae and P. polli- caris in Sarasota Bay (unpubl. data) indicate that gravid females of these species change shells often, move into less saline waters for extended periods, and tend to be somewhat restricted in overall movement patterns. Despite some evidence to the contrary (Gil- christ, 1982; Gilchrist and Abele, 1984; Wilber and Herrnkind, 1982), it is commonly assumed that hermit crab populations are limited by sup- plies of empty shells (Hazlett, 1981; Kellogg, 1976; Vance, 1972). Thus, many studies of in- teractions have focused on competition for this limiting resource. Consumption rate and com- bined effects of different sorts of variability (Chesson, 1985) are important in determining coexistence in specific natural systems. Super- imposed on variation in consumption rate is the age structure pattern of the populations in that differences in shell use occur with crab age (Abrams, 1980). Correlations have been noted between shell selection and level of environmental stress (Bert- ness, 1981c; Taylor, 1981, 1982; Young, 1980) as well as predation (Bertness, 1981c; Borjesson and Szelistowski, 1989). Mortality of all life stages can result from predation (including parasitism). The type and condition of shells may afford some advantages \o crabs with certain predators, however, crab 270 behaviour may be of equal or greater importance in circumventing predation, Crypsis, burrowing behaviour, or use of refugia such as seagrass beds may decrease predation by vertebrates. Birds, including especially gulis(Oldham, 1930) and fish, are effective predators on these crabs (Pagurus; Fig. 5). Use of weathered or fouled shells may provice camouflage for crabs in par- ticular habitats (Blackstenc, 1984; Conover, 197f; Jensen, 1970; Partridge, 1980), Fouling of shells by algae (Smyth, 1989) and hydroids (Jen- sen, 1970: Stachowitsch, 1980) may prevent boring organisms from weakening shells through bicerasion or may deter predators from handling shells, Abrams (1978) found strong selection against unused shells by Coenobtia compressus, noting thal crabs of this species modified the aperture as well as internal shell structures. Coenobita compressus in used shells chirped more often and for a longer period of time than crabs in newly liberated shells (Gil- christ, unpubl. data). Abrams also observed that a green alga coated the interior of the shell. In shell experiments with this crab species, aquatic juveniles with algae in the shell had greater numbers of shell cohabitants while adults with algae in the shells tended to have greater Water retention and longer times to desiccation (Table 6). ‘Agonistic encounters relating to the shell re- source are recorded commenty for aquatic her- mit crabs. Hazlett (1966) gives a detailed description of many components to shell fighting (or shell exchange). Abrams (1982) studied shell exchange between many different species pairs \n tropical and temperate zones and noted that crabs jn adequate or high quality shells typically retained their shells. Further, he suggested that exploitative competition for new shells might be morte important in understanding shell distribu- tion among species than shell fighting. Tmafuku (1989) summarised 2 important fea- tures of shell fights: exchange of resource and vanation in value of resource for individuals. Shell fights may include a variety of agonistic interactions, These typically include both visual and tactile components (Hazlett. 1966 inmer alte), Field et ab (1987) explored jhe use of sound production by Trizopagurus as a defen- sive hehaviour, It also aids in Species tecoyni- tion. In additino, they noted that the shell has only asmall role in modifying the sound. Coene- bite clypeatus and C. compressus sound produc- tion (chipping) may occur alune with vesual displays and tactile behaviour, Chirping MEMOIRS OF THE QUEENSLAND MUSEUM frequency may increase significantly when new crabs are introduced into an area (pers. obs,)- Birgus may also use sound in such contexts (Grubb, 1971), Male Araius observed on Tidy Island in Florida may rap chelae and the fourth pereciopods On horizontal trunks when threatened by a can- specific. In tagging experiments with large male Aratus (carapace width >14mm), these animals exhibited a patrolling behaviour, This consisted of moving vertically on the trunk for about a half metre (either up or dawn), raising the chelae while tilting the front of the body outward and then zigzagging over the trunk. The same males were found on specific trees a greater amount of time than would be expected by chance alone, suggesting further studies are necessary on the potential territorial behaviour of this crab. Several similarly sized crabs occupy a tree at one time. Rarely were overt agonistic encounters observed although numerous crabs were ob- served with missing chelae or ambulatory ap- pendages. These missing appendages may be explained in part by successful avoidance of predation (Table 3). In 7 cases of aggressive encounters noted in 50 hours of observation, all were on the root area of the mangrove. In each case, one crab approached (he other from above. Each crab extended and raised ihe chelue while moving back and forth in a semicircle. The ab- domen was close to the surface While the anterior of the crab was elevated. The cyestalks were lowered to about a 45" angle with the carapace. In two cases, the crabs were ‘bubbling’ from the oral opening. Typically, afier about 90 seconds of such posturing one crab would sidestep and move away from the encounter. In 3 instances a brief shoving match followed the semicircular movements, The match ended when one crab was pushed off the surface entirely or when the first three pereiopods of one crab were lifted off ihe surface. The lifted crab backed away and maved around the root away from the opponent. The crab that was knocked from the surface was missing part of the left 4th pereiopod, Only male crabs were involved in 3 encounters, only females in 2 encounters, and male-female pairs were found in 2encounters. The only other social encounters observed for these crabs were 3 prob- able copulatory events, The male approached a female from above and from an angle, In each case, the male then moved over the top of the fernale while completely surrounding her body with (he perejapods. The male then lifted his body above the female while holding the chelae BEHAVIOUR OF CRUSTACEA down and clasping the female with the second pereiopods, The female then gathered her ap- pendages close to her body, and rose from the surface. After that point, copulation proceeded much the same as observed by Warner (1967). Females were hard shelled in each case. Other forms of social encounters for Aratus were observed during feeding bouts around root areas of black and red mangroves. Feeding be- haviour and social interactions were noted for crabs during low tide only when roots were exposed, Activity was especially noted during crepuscular low tides. Stall animals (carapace width 25) formed around freshwater, Crabs were observed dipping the chelae into the water and moving them to the mouthparts, As larger crabs approached, smaller crabs scattered and moved back into the jungle, Large crabs etlher drank in the same manner as described for the smaller crabs or immersed the entire shell into the water. Feeding and drinking behaviours of these crabs are noted elsewhere (Newton and Gilchnst, (989). Larger crabs typi- cally maintained a relatively large distance be- tween each other at freshwater sources. However, clicking and chirping frequency in- creased as mew crabs approached the waler anurcy, Most crabs appeared to scavenge or browse for food, However, predalion on both plants and alimals occurred. Immature insects (grubs, caterpillars. and maggots) were readily eaten as were young leaves near the jungle flaor, A wide variety of items were detected by crabs including chocolate, honey, dog food, taw eggs, and cat food. Much like their terrestrial counterparts, marine hermit crabs may feed in aggregations of mixed sizes. li is not clear, however, whether social facilitation or chemical attraction leads to in- creases in aggregation size. Schembri (1982) described the feeding behaviour of fifteen spe- cies of hermit crabs from southeastern New Zca- land. He found a wide range of feeding mechanisms among the group including deposit feeding, browsing, suspension feeding, preda- tian, and scavenging, He indicated that a variery of secondary mechanisms- During aggregate feeding, observed for marine species in Sarasota Bay, not only are conspecif- ics found at such siles bu also other species may be attracted. Pagurus longicarpus was found in every mixed group. As a group forms, several types of interactions may occur. If the food item is small enough, a crab may altempt to flee with it. Typically, a tugging match ensues with each contender holding on with the major chela and plucking from the food item with the minor chela. As more crabs join, larger crabs typically displace small ones. Smaller crabs climb onto the shells of these larger crabs, collecting food from the water column above the feeding crabs, Larger crabs flick other crabs with. the major chelae while holding onto the food item, If the item is too large to guard in this manner, a number of larger crabs will begin feeding on the item. Smaller crabs which try to move beneath larger crabs are typically flicked away, I have observed neither shell exchanges nor malting be- haviour during such feeding bouts. Hermit crab predators are also attracted to food sources, hus shell exchanges and copulation may not be pro- ductive at feeding sites, Aggregates in marine habitats may also allow crabs to avoid predators. Callinecies typically approaches the aggrega- thons from downstream, rushing the group as it nears. Fishes and birds lend to move over the groups slowly, making several quick darts before the group disband. Such predator attacks on ter- restrial species have not been recorded, SUMMARY Clearly, terrestrialisation has led to be- havioural modifications in crustaceans. Physia- logical differences in smaller crabs on land may serve to separate them ecologically from their adult counterparts. Physiological differences in sizé do not seem as important in aquatic species- Chemical, visual, and tactile inputs are impor- tant components of modulating motivation anda action of terrestrial and aquatic species, How- ever, the relative importance of the types of cues may differ in the two media. The full extent of how chemical and acoustical information may modify behaviours is still under investigation, Further study of both the receptors and responses are necessary. In addition, careful ontogenetic studies of the morphology of receptors and de- velopment of behaviours should be completed, MEMDIRS OF THE QUEENSLAND MUSEUM ACKNOWLEDGEMENTS A portion of this work was conducted at the Smithsonian Tropical Research Institute in Panama, Assistance and cooperation at the Naos Laboratory and from the people on the island of Taboga is greatly appreciated. The New College Faculty Development Fund supported a part of this work in Florida. M.A.G. Burton, J, Collins, A, Ferris and N. Newton supplied valuable field work for this project. Thanks also to C, Saeman and J.B, Morrill for editing early copies of the work. LITERATURE CITED ABELE,L.G. 1970. Semi-terrestrial shrimp (Merguia rhizophorae). Nature 226; 661-662 ABRAMS, PA. 1978, Shell selection and ulilizetion ina terrestrial hermit crab Coenohita compres- sus (M. Milne Edwards). Oecologia 34) 259— 253. 1980. Resource segregation and interspecific cam- petition in a tropical hermit crabs community. Oecatogia 46: 365-379. 1981, Sheil fighting and competition between wo hermil crab species in Panama. Oecologia 51- 84-90. L982, Frequencies of interspecific shell exchanges between hermit crabs. Journal of Experimental Marine Biology and Ecology #1; 99-109, BEEVER,J.W.,SIMBERLOFP, D, AND KING,L.L. 1979. Herbivory and predation by the mangrove iree crab Aratus pisonii. Oecologia 43: 317- 328, BERTNESS, M.D. 1981, The influence of shell type on hermit crab growth rate and clutch size (De- capoda, Anomura). Crustaceana 40: 197-205. BLACKSTONE, N. 1984. The effects of history on the shell preference of the hermit eral Pagurus longicarpus (Say). Journal Experimental Marine Biology Ecology #1: 225-234. BLISS, D.E. 1968, Transition from water to land jn decapod crustaceans.. American Zoologist 8: 355-392. BURGGREN, W.W. AND MCMAHON, B.R. 1988. “Biology of land crabs’, (Cambridge University Press; Cambridge). 479p. BURTON. M. 1990. ‘Levels of herbivory on black and white mangroves’. Senior thesis, New Col- lege of USF, Sarasota, 47p. CHESSON, P,L, 1985. Coexistence of competitors in spartially and temporally varying environments: A look at the combined eftects of different sorts of variability. Theoretical Population Biology 28(3): 263-287. BEHAVIOUR OF CRUSTACEA 27 CONOVER, M.R. 1976. The influence of some sym- bionts Of the shell selection behaviour of the hermit crabs, Pagurus pollicaris and Pagurus longicarpus. Animal Behaviour 24: 191-194. DE WILDE, P.A.W.J. 1973. On the ecology of Coenobita clypeatus in Curacao with reference to reproduction, water economy and osmoregu- lation in terrestrial hermil crabs. Studies of the Fauna of Curacao 44: 1-138. DOWDS, B.M. AND ELWOOD, R,W, 1983. Shel) wars; Assessment strategies and the timing of decisions in hermit crab shell fights. Behaviour 85: 1-24. 1985, Sheil wars II: The influence of relative size on decisions made during hermit crab shell fights. Animal Behaviour 33: 649-656. FERRIS, A. 1988. ‘A biomechanical analysis of loco- motion in the mangrove tee crab Aratus pi- sonii’. Senior thesis, New College of USF. Sarasota. 47p, FIELD, L.H., EVANS, A. AND MCAMILLAN, D.L. 1987. Sound production and sttidulatory struc- tures in hermit crabs of the genus Trizopagurus. Journal of the Marine Biological Association of the United Kingdom 67: 89-110. FOTHERINGHAM, N. 1980. Effect of shell utiliza: tion on reproductive patlerns in tropical hermit crabs. Marine Biology 55: 287-293 GERITZ, S.A.H., METZ, J.AJ., KLINKHAMER, P.G.L., AND DEJONG, T.J. 1988, Competition in safe-siles. Theoretical Populavion Biology 33(2): 161-180. GHERARDI, F. AND VANNINI, M. 1989. Field observations on activity and clustering in two intertidal hermit crabs, Clibanarius virescens and Caleinus laevimanus (Decapoda, Anomura). Marine Behaviour and Physiology 14; 145-159. GHIRADELLA, H.T., CASE, J.F. AND CRAN- SHAW, J. 1968. Structure of aesthetases io selected marine and terrestrial decapods: chemoreceptor morphology and environment. American Zoologist 8: 603-621. GIBSON-HILL, C.A, 1947, Field notes on terrestrial crabs, Bulletin of Raffles Museum 18: 43-52. GILCHRIST, S. 1982. ‘A critical view of hermit crab shell use’, PhD Dissertation. Florida State Uni- versily, Tallahassee, Florida, USA. 137p. GILCHRIST, S,, SCOTTO, L. AND GORE, R.H. 1983. Early zoeal stages of the semiterrestrial shrimp Merguia rhizophorae (Rathbun, 1900) cultured under laboratory conditions (Decapoda, Natantia, Hippolytidae) with a discussion of characters in the larval genus Eremmoacaris. Crustaceana 45(3); 238-259. o GILCHRIST, 8, AND ABELE, L.G. 1984, Effects wf sumpling method on the estimation of popula- tion parameters in hermit crabs. Journal of Crustacean Binlugy 4: 645-654. GRUBB, P. 197|, Ecology of terrestrial decapod crustaceans on Aldabra. Philosophical Transac~ tion of the Royal Society of London, Series B 260: 411-416. HAZLETT, B.A. 1966. Social behaviour of the Paguridae and Diogenidae of Curacao. Studies of the Fauna of Curacao and other Caribbean Islands 23: 1-143. 1968, Stimuli involved in feeding behaviour of the hermit crab Clibanarius viltatus. Zeitschrift fir Tierpsychologie 25: 608-614, 1970. Tactile stimuli in the social behaviour of Pagurus bernhardus (Decapoda, Paguridae). Behaviour 3@: 20-40. 1972. Ritualization in marine crustacea. 97-125, In HE. Winn and B.L. Olla (eds) ‘Behaviour of marine animals, vol, 1, Invertebrates’. (Plenum Press, New York). 1978, Shell exchanges in hermit crabs: aggression, negotiation, or both. Animal Behaviour 26: 1278-1279. 1981. Influence of rearing conditions on initial shell entering behaviour of a hermit crab (Decapoda, Paguridae). Crustaceana 20(2); 167-170. (983. Interspecific negotiation: mutual gain in ex- changes of a limiting resource, Animal Be- haviour 31: 160-163, 1989, Mating success of male hermit crabs in shell generalist and shell specialist species. Bebar~ joural Ecology and Sociobiology 25; 119-128. HAZLETT, B.A, AND BARON, L.C. 1989, In- fluence of shells on mating behaviour in the hermit crab Calcinus tibicen. Behavioural Ecology and Sociobiology 24: 369-376. HAZLETT, B.A, AND ESTABROOK, G. 1974, Ex- amination of agonistic behaviour by character analysis. U! Hermit crabs. Behaviour 49: 88-110), HELFMAN, GS, 1979. Coconut crabs and cannibal- ism, Natural History 88; 76-83. HERREID fl, C.F. AND FULL, RJ, 1986. Lacomo- tion of hermit crabs (Coenobita compressus) on beach and treadmill, Journal of Experimental Biology 120: 283-296. IMAFURU, M. 1986. Sexual discrimination in the hermit crab Pagurus geminus, Journal of Ethology 4; 3947. 1989, Shell fights in the hermit crab Pagurus geminus: Effect of cheliped use and shell rap- ping. Journal of Ethology 7: 35-39. IMAFUKU, M, AND IKEDA, H. 1990, Sound pro- duction in the land hermit crab Coerobita pur- pureus Stimpson, 1958 (Decapoda, Coeno- bitidae). Crustaceana 58(2); 168-174. JENSEN, K. 1970. The interaction belween Pagurus bernhardus (L.) and Hydrectinia echinata (Fleming). Ophelia 8: 135-144. KELLOGG, C.W. 1976. Gastropod shells: A poten- tially limiting resource for hermit crabs, Journal of Experimental Marine Biology and Ecology 22: 101-111. KINOSITA, H. AND OKAJIMA, A. 1948, Analysis of shell searching behaviour of the land hermit crab Coenobita rugosus H, Milne Edwards. Journal Faculty Science Tokyo £1: 293-358, KURTA, A. 1982. Social facilitation of foraging be- haviour by the hermit crab, Coenobita compres- sus, in Casta Rica. Biotropica 14; 132-130. LEPORE, M. AND GILCHRIST, S. 1988. Hermil crab atlraction to gastropod predation sites. American Zoologist 28(4): 72A. MCLEAN, R.B. 1974, Direct shell acquisition by hermit crabs from gastropods, Experientia 30; 206-208. MCMAHON, B.R. AND BURGGREN, W.W. 1981. Acid-base balance following temperature accli- mation in land crabs. Journal of Experimental Zoology 218: 45-52. MORRIS, S,, GREENAWAY, P,, AND MCMA- HON, B.R. 1988, Adaptations tu a terestrial existence by the robber crab Birgus tatro: [. An in vitro investigation of blood gas transport. Journal of Experimental Biology 140: 477-491. NEIL, S.J, AND ELWOOD, R.W, 1985, Behavioural modifications during egg-brooding in the hermit crab, Pagurus bernhardus L. Journal of Experi- mental Marine Biology and Ecology 94: 99- 114. NEWTON, N. AND GILCHRIST, S. 1989. Feeding and shell preferences of terrestrial hermil crabs. American Zoologist 29(4): 37A, OLDHAM, C. 1930. The shell smashing habits of gulls, Ibis 6; 239-244, PARTRIDGE, B.L. 1980, Background camouflage: An additional parameter in hermit crab shell selection and subsequent behaviour. Bulletin of Marine Science 30(4):; 914-916, PAGE, H.M. AND WILLASON, S.W, 1982. Dis- iribution patterns of terrestrial hermit crabs at Enewetak Atoll, Marshall Islands. Pacific Science 31): 107-117. REBACH, 8. AND DUNHAM, D. 1983. ‘Studies in adaptation: The behaviour of higher Crustacea’ (John Wiley and Sons Inc.: New York). 2452p. REESE, E.S. 1963. The behavioural mechanisms un- derlying shell selection by hermit crabs. Be- haviour 21: 78-126. MEMOIRS OF THE QUEENSLAND MUSEUM RITTSCHOF, D. 1980. Chemical attraction of hermit crabs and other altendants to simulated gastropod predalion sites. Journal of Chemical Ecology 6; 103-118. RITTSCHOF, D. AND SUTHERLAND, J.P. 1986. Field studies on chemically mediated behaviour in land hermit crabs; Volatile and nonvolatile ordors. Journal of Chemical Ecology 12(6): 1273-1284. SCULLY, E.P. 1983, The behavioural ecology of competition and resource utilization among her- mit crabs.23-55. 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Availability and use of shells by intertidal hermit crabs. Biological Bulletin of the Marine Biology Laboratory, Woods Hole LS2; 120-133. STACHOWITSCH, M, 1980. The epibiotic and en- dolithic species associated with gastropod shells inhabited by hermit crabs Paguristes oculatus and Pagurus cuanensis, Marine Ecology 1: 73- 101, TAYLOR, P. 1981. Hermit crab fitness: The effect of shell condition and behavioural adaptations on environmental resistance. Journal Marine Bi- ology Ecalogy 52: 205-218. TAYLOR, P.D., SCHEMBRI, P.J. AND COOK, P.L. 1989. Symbiotic associations between hermit crabs and bryozoans from the Otago region, southeastern New Zealand, Journal of Natural History 23: 1059-1085. TAYLOR, R.C. 1967a. The anatomy and adequate stimulation of a chordotonal organ in the BEHAVIOUR OF CRUSTACEA antennae of a hermit crab. Comparative Bio- chemistry and Physiology 20: 709-717. 1967b. Functional properties of the chordotonal organ in the antennal flagellum of a hermit crab. Comparative Biochemistry and Physiology 20: 719-729. VANCE, R.R. 1972. Competition and mechanism of coexistence in three sympatric species of inter- tidal hermit crabs. Ecology 53: 1063-1074. WARNER, G.F. 1967. The life history of the man- grove tree crab, Aratus pisonii. Journal of Zoology (London) 153: 321-335. 275 WILBER, JR., T.P. AND HERRNKIND, W.F. 1982. Rate of new shell acquisition by hermit crabs in a salt marsh habitat. Journal of Crustacean Bi- ology 2: 588-592. WILSON, K.A. 1985. ‘Physical and biological inter- actions that influence habitat use of mangrove crabs’. PhD dissertation, University of Pennsyl- vania. 167p. WOLCOTT, T. 1988. Ecology. 55-96. In W.W. Burg- gren and B.R. McMahon (eds) ‘Biology of the land crabs’. (Cambridge University Press: Cam- bridge). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 276 INDUCED OVARIAN MATURATION OF PENAEUS VANNAMEI BY IMPLANTATION OF LOBSTER BRAIN In many decapod crustaceans, contro! of ovarian matura- tion is a major problem in developing commercial aquacul- ture programs. Induction of ovarian maturation in Penaeus vannamei, by implantation of brain prepared from female lobster, Homarus americanus, with developing ovaries was investigated under tank culture conditions. Three of five females with brain implants were maturing while none of 10 females of the control groups with abdominal ganglion or no implant matured (Table 1), Two ripe stage V were found 17 days after implantation of lobster brain. This indicates that ovarian maturation of P. vannamei in tanks can be induced and accelerated by implantation of brain prepared from ma- MEMOIRS OF THE QUEENSLAND MUSEUM turing females of another species. Ovarian maturation may be induced by a brain hormone (BH), secreted by the brain of maturing females. This brain hormone is not specics specific in activity in the shrimp and lobster, | have demon- strated that ovarian maturation 1s induced by a ganad-stimu- lating hormone (GSH), secreted by the thoracic ganglion of maturing females in penaeid shrimp. This GSH may be triggered by BH, which probably is working as a gonad- stimulating hormone-releasing hormone (GSH-RA) in regu- lating ovarian maturation in shrimp and lobster. Tsao Yano, National Research Institute of Aquaculture, Nakatsuhama, Nanseicho, Mie, Japan. TABLE L_ Effects of implantation of brain prepared from maturing female lobster, Homarus americanus, on induction of ovarian maturation of Penaeus vannamei 17 days after trealment. * Size: 30-35g in body weight. Brain implantation Abdominal ganglion implantation No implantation THE EFFECT OF ARTIFICIALLY LIGHTED TRAWLS ON CATCHES OF CRUSTACEANS A series of 32 micronektonic samples were taken with a rectangular midwater trawl (8) in open oceanic water off N.W. Africa (20°30'N, 19°40"W), at a depth of 800+25m, below the effective penetration of surface daylight. The net, fitted with a sea-light and battery pack, was fished fora series of two hour tows, half with lights on and half with lights off, throughout the day and night. Catches of crustaceans, comprising mainly of mysids and decapods, were relatively consistent in biomass (wet dis- placement volume), species composition, and size irrespec- tive of the artificial lighting. Mysids were represented mainly by one species of Eucapia, total numbers and biomass of which were similar in most samples. Decapoda were identified to species and the carapace length measured. The size varied from 4.5mm CL to a maximum of 35mm CL but most specimens were in the range 4.5mm-15mm CL, A total of thirty species were identified, of which four were numerically dominant and a further ten occurred in moderate numbers, There was no indication that artificial lighting had an affect on species composition. Numerically dominant decapod taxa included two species of Gemnadas, oné of Acanthephyra and one of Sergia many specimens of which were juveniles or young adults. % of maturing Preliminary statistical analyses including an analyses of yariance based on the ten most abundam decapod species indicated that there was no significant difference between catches irrespective of the artificial lighting. This confirms previous work (Hargreaves, unpubl.) that catches of many decapod and mysid species found at depths of 800m off Madeira were hardly affected by lighted traw!s, Initial results on crustacean biomass from paired hauls (Clarke and Pascoe, 1985) indicated that at 800m depth in the Bay of Biscay and off Madeira catches of Decapoda may be diminished with the use of lighted trawls. These indications are not supported by the present.data, However differences in species sampled or in their maturity stages may be responsible for the apparent variations, Literature Cited Clarke, M.R, and Pascoe, PJ. 1985. The Influence of an electric light on the capture of deep-sea animals by a midwater trawl. Journal of the Marine Biological Asso- ciation of the United Kingdom 65; 373-393, P.M. Hargreaves, Institute of Oceanographic Sciences, Deacon Laboratory, Wormley, Surrey, GU8 543 UR, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM THE RED CUTICLE ON THE CLAW OF MALE CHERAX QUADRICARINATUS (DECAPODA;: PARASTACIDAE} The freshwaler crayfish Cherax quedricarinates (von Martens) isa member of the Australian tamily Parastacidac. {t occurs in northern Australia from Cape York through the Northern Territory (Riek, 1951). In recemt years, C, quadricarinatus has become the major freshwater crustacean cultured in Queensland, Features which make this species ideal for aquaculture include (i) little aggression When held at high densities (ii) good survival at high temperatures (ifi) serial spawning. A striking feature of this crayfish is the soft red cuticle that develops on the outer edge of the propodus in mature males, (Growth of the red patch in relation to orbital carapace length is positively allometric. The red patch does not develop in juveniles, and typically occurs in those individuals whose ardilal carapace length exceeds 23mm. Intersexes (those crayfish with both male and female genital openings and which comprised 19 in a sample of 456 individuals) develop the red patch, Occasionally, the red patch is developed by females (3 Individuals in a sample of 279 females), The possible function of this sexually dimorphic feature is in- triguing. A role in defence or allack is unlikely — soft cuticle makes an unsuitable weapon. A role as a visual, sexual signal iS also unlikely — the crayfish are mainly active at night, and mosi crustaceans examined so far are red blind (Shaw and Stowe, 1982), Anecdotal reports indicate thal the red patch af the male claws makes contact With the female when the male makes a series of short, sharp jabs at her during court- ship. Major differences between red patch culicle and ordinary cuticle are: (i) itis soft, Nlexible and yields easily ta touch. The flexibility of red patch cuticle is not achieved in the same way a5 gecurs at hinges between body or leg segments. Hinge cuticle has no coninuous famellse rynaing parallel to the epicuticle. (li) it is uncalclfied (sections through red patch cuticle showed no black colouration when stained using von ULTRASTRUCTURE AND FUNCTION OF THE STOMACH OF PERACARIDA' AND EUPHAUSIACEA Ulirastructurally the stomach is by far the most complicated part of the alimentary canal in Peracarida and Eucarida (for Teferences see Felgenhauer and Abele, 1985; Starch and Strus, 1989), All parts are demonstrated in scanning and transmission electron micrographs. They consist mainly of masticatory par and filters, The most complicated region of the stomach is the ventral suttace with primary filters, secondary filters, anc! mferotater- alia (Storch, 1989; Storch and Strus, 1989; Storch, in prep.; Ullrich et al., in prep.). The mesh sizes of primary and secondary filters vary considerably. Secondary filters of lerrestrial Tsopoda seem lo be the most efficient filters in the enimal kingdom, They are good for microfiliration and come very close to ultrafiltration. They are Compared to the respec+ live structures in Mysidacea, Tanaidacea, Amphipodu, and Euphausiacea. Filters of these delicate dimensions have tn be constantly cleaned to be kept functional. Spines of the medias! face of (he Inferolateralia are probably suitable for (his purpose Additionally, washing occurs when the secretian of the 277 Kossa‘s technique for calerum (Culling, 1974) while control sections through chick embryo were positive). (iii) exa- and endocuticle are nor differentiated, In ordinary cuticle, epi-, exo- and endocutlcle layers are clearly defined, At the tran- sijion zone between cuticle types ihe epicuticle continues withoul change bul (he width of the endocuticls decreases, In red patch cuticle no obvious distinction can be made between exocuticle and endocuticle, giving it a two-layered appearance rather than a three-layered one. (jv) the lamellae are narrow, The width of lamellae in red patch cuticle is just over one third the width of lamellae in the endociiticle of ordinary cuticle (12.5um vy 32.5j1m). Sensilla density on red patch cuticle is similar to thai on hard cuticle of the claw, [tis also similar lo the density on the claws of females in the region Where the red patch would occur, if they had one. Two types of sensilla, simple anc plumose, occur on the ordinury culicle adjacent {p the red patch, whereas anly simple sersillve appear to occur on the red patch cuticle. Whether the red patch gives the male different sensitivily lo tactile or other stirmulation from that of the female awalrs further investigation. Literature Cited Culling, CFA. 1974, ‘Handbook of histopathological and histochemical techniques’, 3rd ed (Butterworths). 470 472 Riek, EF, 1951, The freshwater crayfish (Family Parn- stacidae) of Queensland. Records of the Australian Museum 22/4): 368-388. Shaw, §.R. and Stowe, §. 1982. *Photoreception’. 291—367- In BLL. Atwauu and 0.C. Sandeman (eds) 'The biology of Crustacea’, Vol, 3. (Academic Press: New York) MJ Thorne aiid DR, Fielder, Department of Zoology, Tre University of Queensiand, St Lwela, Queensland 4072, Australia. midgut wands move /hrough the same opening as the filtrate hut in the opposite direction, Literature Cited Felgenhaver, B,E,, and Abele, L.G, 1985, Feeding structures of two alyid shrimps, wilh comments on curidean phylo~ geny. Joumal of Crustacean Biology 5(3); 397-419. Storeh, V. 1989, Scanning and wansmissivn electron micru- scopic observaljons on the stornach of three mysid species (Crustacea), Jounal of Morphology 200; 17-22 In Prep, Scanning and transmission clectron mictoscopic observalions on the stomach of Orehestia cavimana aml Arcitalitras sylvaticus (Amphipoda). Storch V. and Sus, 1.17989. Microseopic anatomy and ultrasiruc- ture of the alimentary canal in terrestrial isopods. Monitore Zoolagien Italiano Monographie 4; 105-126 Ullrich, B, Storch, V,,and Marschall, H. P. fn Prep, Microscupic anatomy and ltrastructure of the stomach of Euphaiesia superbe Dana (Crustacea, Euphdusiacea). V. Storch, Departnent ef Zaviagy, University af Heidelhers, D A900 Hetdetbers. Germany. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 278 BIOCHEMISTRY AND FUNCTION OF CRUSTACEAN NEUROHORMONES Triggered by various. environmental stimuli, the nervous yystem produces and releases several peplices which enable an organism to handle specific simations. The regulatory polencies of the peptides so fur postululed include cardiay control, luco- motion, feeding behaviour, migration of chromatophores and retinal pigment, moult suppression/acceleration, the develop- ment of (estis, voeyles and vitellogenin, limb regeneration, blood glucose adjustment, endogenous rhythmicity, lipid, car- bohydrale and protein metabolism, osmo- and hydrominers] and respiratory regulation, RNA/DNA synthesis, mito- chondrial respiration and carotingid metabolism: almpst overy aspect of crustacean life. The number of postulated factors is large (Kleinholz, 1985; Webster and Keller, 1988), the number of fsolatect neurohormonal peptides, however, is small and our knowledge of their physiological fanctions is still Hmited, Several factors are based on inadequate evidence or are still under discussion ¢.g. the neurodepressing hormone (Cooke and Sullivan, 1982). In terms of the amino acid composition, the moult-inhibiting hormone (MTH) from Cereinus ataenus, the crustacean hyperglycemic hormones (CHH) trom Grconectes limosus, Porcellio dilatatus and Procambarus bouvier! and the neurodepressing hormone trom various species have heen char~ acterized. The primary sequence is reported for two FMRF-like peplides (FL), a member of the pigment concentrating hore mone family, from two pigment dispersing hormones, front ¢ardioactive peptides and from the CHH of Carewms maenac (Kegel e¢ af, (989). For this 8524 Da neuropeptide the complete coding sequence for the pre-pra CHH has been obtained recently from a DNA-library (Weidernann er al, 1989), MTH and the gonad (vitellogenin) inhibiing hormone (GIH/VIH) apparently belong to the CHH neuropeptide family, judging by the comparison of amino acid sequences, which have been analysed ta wpproximarely 80%, Recenr observations are consistent with the hypothesis thal the spec- trum of functions of these identitied neurohormones might be broader than their names suggest. The red pigment concentrat- ing hormone (RPCH), for example, affects not only the erythro- phores hut also the pyloric rhythmy by alternating the membrane potential in the lateral pyloric and pyloric dilator motor neurons, Therefore, RPCH (ora very similar molecule) is thought tO release 4 modulator tram the somatogastne gan- glion. A-similar modulation of proctolin on the pyloric network has been reported, In addition to glocuse CHH aflects irehalose and maltose blood concentrarions and releases amylase from the midgut gland in crayfish, The distribution of the crustucean- cardivactive peptide (CCAP) in the central nervous system suggests that CCAP might be a novel neurotransminer with multiple functions, ¢.g. modulation of the matility of isolated hindguts, In addition to these neuropeptides, which are derived trom) neutohemal sources such as the sinus gland or pericardial organ, numerous, mainly vertebrate-type peptides, have been Jescribed in Crusticean neuronal tissue using immurineyto- chemical methods. The stained epitope does not necessanly prove the identity of the onginal antigen, either functionally or biochemically. Some of these X-like peptides with limited or no relation to vertebrate hormones, such as cholecys- tokinln/gastrin-ilke or calcitonin-lke peptides have been ko- luted or sequenced. The physiological functions of these peplides are mostly unknown or the subject of speculation MEMOIRS OF THE QUEENSLAND MUSEUM Opioid- and FMRFamide-like peptides have been deman- strated by HPLC, RLA and immunoeytochemistry Indecapod crustaceans (Jaros, 199(1). The FMRFamide-like peptides (FLI3,4), isolated from Homarus, seem to be invalved in the modulation of cardiac neuromuscular junctions (Trimmer ev al., 1987). The CHH release-inhibiting effect of leu-enkephalin, blocked by naloxone, was shown by Jaros er ai, (1985), Mer- enkephalin has been shown to stimulate the release of chroma- {ophorovopic hormones and other evidence exists for the involvement of an opipid regulation of locomotor activity in Geearcinus lateralis. These different results demonsirate the broad spectrum of opioid effects on crustacean physiology, An exciing future field of study for the endocrinologis! is the growing body of information regarding a possible neurshor- monal-immunological axis even in invertebrates. Pilot siudies reveal un impiicalion of apioids on hemocyle aggregation. Acknowledgement The work is supported by the Deutsche Forschungsp- meinschall (1a 3972-4), Lileramure Cited Cooke, 1M, and Sullivan, R.E. 1982, Hormones and Neu- rosecretion, 205-291), In H.L. Atwood and D.C Sand- eman (cds) “The biology of Crustaceu’, Vol. 3. (Academic Press: New York), laros PLP, Diteksen, H. and Keller, R. 1985, Occurrence Of immunoreactive enkephaling in a teurohaemal organ and other neregus structures in the eyestalk of the share erah, Curcinus maenas L. (Crustacea, Decapody). Cell and Tissue Research 24%: LLL-117, Jaros. P,P. 1990, Enkephalins, biologically active neuropep- tides in inwertehrates, with special references (0 crustaceans 471/482. In K. Wiese, W.D. Krenz, J. Taui2, H. Reichert and B. Mulloncy (eds) “Frontiers in crustacean neurobiology’. (Birkhauser: Basel). Keacl, G., Reichweln, B., Weese, S,, Gaus, (,, Peter-Katalinic, J. and Keller, R. 1989, Amino ucid sequence of the crustacean hyperglycemic hormone (CHH) from the shore crab, Carcinus maenas, FEBS Letters 255; 1-14. Kleinholz, LH. 1985, Biochemistry of Crustaeean Hormones. Pp. 463-522. In D.E. Bliss and L.H. Mantel (eds) "The binlogy of Crustaceans’, Vol, Y, (Academic Press; New York), Trimmer, B.A., Kobietski, L.A. and Kravitz, B.A, 1987, Purification and charactenzation of PMRFamide-like immunoreactive substances fram the lobster nervous system: isolation and sequence ynalysis of two closely elated peptides, Journal of Comparative Neurology Rote 1O-26, Webster. $.G, and Keller, R, 198%, Physiology anu biochem- wiry of crustacean neurohonmonal peptides. 173-196. In M.C. Thorndyke and G.J. Goldsworthy (eds) *Néu+ copeplides in invertebrates’, (Cambridge University Press; Cambridge), Wedemaan, W,, Gromoll, J. anu Keller, R. 1989. Cloning and sequence analysis of CDNA for precursar af 2 cristacéan hyperglycemic hormone. FEBS Letters 257: 31-34, Peter P. Jaros, University of Oldenburg, Deparment of Animal Physiology, Germany. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM PHOTORECEPTOR MEMBRANES AND VISUAL PIGMENTS IN THE APPOSITION EYES OF THE TERRESTRIAL CRAB, OCYPODE RYDERI (OCYPODIDAE), DURING THE DAILY LIGHT CYCLE The ghost crab, Ocypode ryderi, is very common on the equatorial sandy beaches of the east African coast. The activity periods of these animals are ruled by the tides, and therefore they feed at the water-line of low, rising tides during both day and night. Their very large compound eyes are of the apposition type, which adapt to strongly different light intensities by changing the size of the rhabdoms in each ommatidium. These changes are controlled internally (without the need for an external zeitgeber) according to the diurnal cycle. Morphometric studies on the form of the rhabdom and the size of its microvilli gave the following results. The rhabdom volume changes — while its length remains constant by a factor of 8. The total surface of the microvillar membranes, however, changes only by a factor of 6, because the diameter of each microvillus is slightly larger during night than day, The visual pigment molecules are closely packed in the membranes, as can be seen in electron micrographs of freeze fracture preparations, where each particle represents a group of four molecules, The thabdom, which consists of the rhabdomeres of eight visual cells, has a characteristic variation of its form during the daily cycle, The most distal part, which is built exclusively by the distal receptor cell, named no. 8, exhibits the greatest volume change. Its variation in diameter is paralleled by the proximal surface of the crystalline cone. The rhabdomeres of the otherseven receptor cells together all arrange to forma long, thin conus, The change in its diameter is much more pro- nounced in the distal than in the proximal part. The visual pigment content — as measured spectrometri- cally in extracts — parallels the change in microvillar surface: during the night there is 6.5 times the amount as during the day. In contrast, the protein moiety, opsin, changes significantly less — only by a factor of 4 — which means that a considerable part of it is stored in the cell during the day. It is unknown where this lipophilic material is situated, The visual pigment, rhodopsin, consists of the protein moiety opsin and ils chromophoric group, which was deter- mined by HPLC as retinal), The characterization of the spéctfal properties of the pigment system in the eyes of Ocypade was carried out by successive itradiation of digi- tonin-extracts from isolated rhabdom-membranes with mon- ochromatic lights, Short-time illumination (< 1 min) with long wavelengths (590 nm) transforms the blue sensitive visual pigment (P4790) into its metarhodopsin (M520). Longer lasting illuminations lead to the decay of metarhodopsin into opsin and free retinal; (Amax 380 nm) or, in the presence of hydroxylamine, retinal-oxime ( Amax 368 nm). Further illuminations with light ot a shorier wavelength (471 nm) lead to a decrease in absorbance around 430 nm and to an increase around 510 nm. Illuminations were carried oul until no changes in the difference-spectra after illumination could be observed. Computations from the difference-specira obtained, using nomograms from EBREY & HONIG (1977, Vision Res 17, 147), resulted in a visual pigment with a Amax of 424 nm and a metarhodopsin with a Amax of 518 nm. Light of 530 nm reconverts the metarhodopsin into rhodopsin. Additional illumination with UV-light (348 nm) leads to a decrease of the absorbance around 350 nm and to an increase around 510 nm. The photoproduct of this conversion is thermostable af 8°C and can be reconverted into rhodopsin by illumination with 517 nm, Computations of these spectra gave a UV-visual pigment with a Amax of 355 nm anda metarhodopsin with a Amax of 510 nm. These pigments, which are expected to occur in different receptor cells. together build a three-component-colour vi- sion system, which is demonstrated here for the first time in a decapod crustacean. H. Langer, .M. Pieper and U. Henning, Tierphysiologie, Fakultét fiir Biolagie, Ruhr-Universitat Bochum, 4630 Bochum 1, Germany. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 280 VENTILATION ACTIVITY AND GUT FULLNESS OF THE BURROWING GHOST SHRIMP, CALLIANASSA AUSTRALIENSIS DANA (DECAPODA: CALLIANASSIDAE), DURING LOW TIDE Invertebrates thal live in deep burrows in the inlertidal zone are thought to gain an advantage by being insulated trom environmental changes al low Jide. Stress causes many intertidal invertebrates to cease feeding at some time of the tidal cycle (Newell, 1979). The shrimp, Callianassa austral- iensis teeds in burrows but may passibly change its feeding activity at low tide. This study aimed to detect and quantify changes in behaviour that may help explain the role of the ude in the feeding energetics of this species. Methods and Materials The study site was located on One Mile Beach on North Stradbroke Island, (27°29'S, 153°24'E), The oxygen tension of burrow water samples was determined using a portable oxygen meter and magnetic stirrer. Animals were collected by using a ‘yabby pump’ al different times after the tide had uncovered their burrow apertures. General physiological and morphological data collected included, sex, wel weight, carapace length, moult state, and ‘empty’ or ‘not-empty’ state of (he gut of each shrimp was recorded. In one group of animals (T = Oh n = 43, T = 2h n = 38) the fresh and dry weight of the foregut and ‘intestine’ was obtained after dissection. The temperature of mud (30cm depth) and surface puddles were recorded in conjunction with each sample of shrimps. Results and Discussion The shrimps ceased ventilating and purging sediment from their burrows 2—3h after low tide. The oxygen tension of water samples taken from the burrows fell significantly at low tide, from 19.98 1,25 kPa at Oh (N = 8) to 12.04=3.01 kPa, (N = 10, P<0.05) after 1h, bur there was no. further change after 3h (13,584.72 kPa, N = 10, P>0.20), Large amounts of oxygen were therefore available for respiration by these shrimps at Jow lide. Warming of the sediment during daylight low tides was less marked (at about 30cm depth, in the order of 1-2°C) than the rapid warming found in puddles on the surface of the mudflat (7-8"C). Ai least some shrimps pump this warm surface water through their burrows al low tide, No significant change in wet or dry foregut weight could be detected, however, the mass of the intestines of shrimps MEMOIRS OF THE QUEENSLAND MUSEUM collected after 2h of low tide was lower than thal of shtimps collected at the beginning of low tide, (Mann Whitney test applied to wet weights, Z = -3.937, N1 = 43, N2 = 38). The mean percentage (prior to arcsine transformation) of the population with ‘empty’ intestines increased at low tide (data from 7 tides), from 5.36+6.19% to 47.51+20.44% within the first hour (using aresine transformed data, t= -4.9058, DF = 12, P<0.0005), before levelling off (t = 2h 61.87+20,04%, t = 3h 64,.00+16.835). This change was reflected also in shrimps captured in the act of burrow ventilation/sediment purging during several low tides (pooled data, T = 0, N = 78 empty 0%: T = 1-Zh, N = 65, empty 50.8%), indicating that sediment purging (with associaled thermal stress) was not confined ta shrimps containing faecal pellets. The decline in sediment purging behaviour at low tide occurred in parallel with, and cannot therefore be explained by, changes in gut fullness, i.e. ‘feeding’ activity. Knowing the relationship of ‘empty’ intestine weight (log (W) = 3.736 log (L) - 3.145, N = 28, 7 =0.55, F = 329.8 P<<0,001) and “not-empty” intestine weight (log (W) = 2.424 log (L) - 1.084, N = 53, 1° = 0.67, F = 105.0, P<<0,001) ta carapace length (L) allows mean faecal pellet egestion rates to be calculated. Roughly half of the population empties their intestines in the first hour of low tide, requiring those shrimps to egest faeces at 11.08 and 26,Slmg wet faeces hr! for shrimps with a carapace length of 8 and 12mm respectively. This result compares well with the data obtained by Frankenberg er al. (1967) from faecal pellets discarded by Ci allichurus major a\ low tide, (50.6mg wet faeces burrow ~ h). A large partion of the shrimp population clears faeces from their intestines during low tide and may very well cease feeding al this time, Further work is required to establish why some shrimps fail to empty their gut and to explain the variation in response between tides, Literature Cited Frankenberg, D., Coles, $.L. and Johannes, R.E. 1967. The potential trophic significance af Callianassa major fecal pellets, Limnology and Oceanography 12; 113-120. Newell, R.C. 1979. ‘Biology of intertidal animals’. 3rd Ed. (Marine Ecological Surveys Ltd: Faversham, U.K.).781p. Brian D. Paterson, Queensland Food Research Laboratories, Queensland Department of Primary Industries, Hamilton, Queensland 4007, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM THE INFLUENCE OF SIZE DIFFERENTIAL ON AGONISTIC ENCOUNTERS BETWEEN INTERMOULT FRESHWATER CRAYFISH IN CHERAX CUSPIDATUS RIEK, 1969 (DECAPODA; PARASTACIDAE) The resource holding potential (RHP, Parker 1974) of an animal is a measure of that individual’s absolute fighting ability, and consists of a combination of its morphological and physiological traits such as body size, age. size of weapons, armour and energy reserves (Caldwell, 1987). RHP is one of several concepts generated from the application of game theory 10. animal contests (Maynard Smith and Parker, 1976; Parker and Rubenstein. 1981). Such concepts have enabled the formulation of testable predictions relating to the agonistic behaviour of animals under various conlest condi- hons. The research outlined in this paper (esled Iwo predictions of simple game theoretic models. These were: 1, arasymmetry in RHP between opponents will decide contest oulcome; and 2. RHP differences between opponents will determine strategies used in contests, with escalated interactions likely to occur between opponents with similar RHP. Methods Sexually immature, intermoult, young of freshwater cray- fish Cherax cuspidatus were used in experiments. Total carapace length (T.C.L.) was the RHP index employed. Crayfish were paired at five size ratios : 171, 1)0,9, 1:0.8, 1:0.7 and 1:0.6 and allowed to inleract for 180 minules in containers (9 x 9.5 x 9.Scm high) with no shelter present. Crayfish were released into the containers simultaneously to eliminate any passible ownership effect. Replication level was 16. The initiator, winner, duration and type (whether fight, attack. strike or threat) of each agonistic interaction was recorded. The dominant individual for each pait was defined as the one which won at least 60% of all interactions. The size of each dominant (whether the larger or smaller member of the pair) was also recorded. Results and Discussion The larger animal was always. dominant once the size difference. was 2()% or more. The larger individual was dominant significantly more often than expected by chance at the 1:0.9 (p<{).01) and 1:1 (p<0.05) size ratios, Two pairs at the 1:1 ratio had equal T.C,L. values. The remainder was separated by differences between 0.85 and 4.05%. indicating thal size discrepancies of less than 5% can influence outcome of agonistic intoractions. The measurements taken for the four pairings at !:1 and three al 1:0.9 in which the individual with smaller T.C,L.was dominant, teVvealed that in cach case the ‘smaller’ animal. was superior in at least one of the other potential RHP values 281 (weight, chelae length, age). This result suggests thata single RHP index has limited utility for pairs when both members ar€ Superior in one or more morphological measurements. Such a silwation is especially relevant to organisms with indeterminate growth. e.g. Crustacea. Size discrepancy between opponents had a significant inverse rélationship with total agonistic time, fight time, maximum and average bout length (p<0.001), fight frequency and frequency of all interactions (p<0.01), and strike frequency and time of threat, strike and attack com- bined (p<0.05), Attack frequency, threat frequency and at- tack response latency did not vary significantly between size Tatios, Size discrepancy had an inverse relationship with the proportion of interactions initiated by the smaller animal in each replicate (p<0.05), but formed no significant relation- ship with proportion of interactions won by the smaller individual (p>0.05). The larger animal in each pair mitiated (p<0.01) and won (p<0.000)) the first agonistic interaction significanily more oflen than expected by chance. The smalier animal initiated a proportion of the first interactions, irrespective of size ratio. Assessment of RHP among pairs of C.cuspidarus always involved agonistic interaction, possibly as a means to probe for recently moulted crayfish. Differences in RHP between opponents determined the oulcome of inleractions, Contests in which opponents could accurately assess the asymmetry in RHP, ic. 1:0.6 and 1:0.7 size ratios, were settled without escalation. Those in which role assessment could not be accurately made by conventional behaviour, te. 1:1, 1:09, 1:0,8, resulted in escalation, The results of this work ate in agreement with the predictions generaicd by simple game theoretic models. Acknowledgements The assistance provided by Anita Smyth and Tam Gor- ringe is gratefully acknowledged. Literature Cited Caldwell, RL, 1987. Assessment strategies in slomalopods, Bulletin of Marine Science 4f; 135-150. Maynard Smith, J. and Parker, G.A. 1976. The logic of asymmetric contests. Anima! Behaviour 24: 159-175. Parker, G.A, 1974, Assessment strategy and the evolution of fighting behaviour, Journal of Theorelical Biology 47: 223-243. Parker. G.A. and Rubenstein, D.L 1981. Role assessment, reserve strategy, and acquisition of information in asym- metric animal conflicts. Animal Behaviour 29:221—240, Chris R, Pavey and Don R. Fielder, Zoology Department, University of Queensland, Queensland 4072, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum IONIC PERMEABILITY OF THE CUTICLE AND TONOREGULATION IN DECAPOD CRUSTACEANS The janic permeabilities of the isolated gill cuticle have been deduced from diffusional transculicular potential and conductance meusurements. in several species of decapod crustaceans. I) is established that the Gulicle permeability depends upon the species considered and its ionoregulation capability, upon the localisation of the gill (nthe gill chamber Or even upon the topographic region in a single gill and upon the nature of the ionic species. In each case the cuticle must always be considered as a diffusion harrier for the main osmotic effectors, Na’ and C} , However, the efficiency of this barrier is low in (he case of the sienohaling osmoconformers, Humurus, Nephraps, Maia. In hyperregulators such as Astacus, Eriached and Carcinus, the efficiency of the cuticular barrier ts much higher, The cuticle permeability of the crayfish gill lamina is Jow tor all jonie species but CY. In the crayfish vill filaments and in crab gills, permeubility to cations is high. but perme- ability to Cl is low, In hyperreguiators, the cuticle exhibils important differ- ences in its electrical characteristics between the vanaus pairs of pills or even between different topographic regions of the same gill. Wtshows in addition a tunctional asymmetry Which favours jonic influxés. This asymmetry is almost nonexistent in osmoconforming species. The physiological significance of the cuticle is discussed in relation to the jonoregulation capability of the species and more particularly to the subcuticulur spaces described in al! gill epithelia of hyperregulatory Crustacea facing reduced salinity, It is propounded thal the will cuticle contributes to MEMOIRS OF THE QLIEENSLAND MUSEUM ‘ NEPHROPS CANGER ASTACUS HOMARUS: MAIA CARCINUS (up te tL) 5 -2 1 i " ] “* > 8 -s } e | 474 a ao -5 7 7 ia 5 +8 4 4 j * of] “7 oO Xn @ not FIG, |, Comparison of the permeability of the gill cuticle from six crustaceans to the main osmotic effectors Na’ and Cl, The permeabiliry (P) is plotted on a logarithmic scale, Notice the difference between regulators and osmocon- formers etiher within the macrura or within the brachyura (L = gill lamina; F = gill filaments). Taking into account the electroneutrality condition, the following salt permea- bility sequence-as related to the species would be : Ho- marus, Nephraps > Mata > Cancer > Carcinus > Astacns. of ions across specific channels af the sites where active uplike lakes place. A. Péqueux, University af Liége, Laboratary of Animal Physiology, B-4020 Liége, Belgium. JM. Lignon, LERP, CNRS, 23, rue Becquerel, F reduce ionic leaks in repulatars and yel allows forthe entry 67087 Strasbourg, France. NEUROENDOCRINE CONTROL OF THE OVARY AND HEPATOPANCREAS IN SIBERIAN PRAWN, EXOPALAEMON MODESTUS In many decapod crustaceans, the eyestalks have an X- otpan-stnus gland complex (XSC) as a neuroendocrine organ controlling various physiological phenomena such as colour change, moult, reproduction ete: Among the hormones syathe- sived in the XSC, gona inhibiting hormone (GIH} is involved. in the regulation of gonad maturation, Despite studies of eye- stalk ablation in many species, the source of nutrients required for precocious gonad maturation, and the primary action site of GITH are not yet clear, The present study examined the effects of eyestalk factors, especially GIH, on ovarian maturation and hepalopancreatic metabolism when the eyestalks were ublated to block the GIH source. Animals were collected from freshwater reservoirs, around the Scosun area on the west side of Korea, during the hibernat- ing season. The prawns were transported to the laboratory and placed in w crustacean rearing chamber, The prawns were maintained in glass tanks equipped with sub-sand filters. The temperature was maintained at 25+1°C and pholo-period was adjusted to 12hr light : 12ht dark. Animals were fed with chopped mussel and fish ad libitum. Eyestalks were ablated bilaterally by using small scissors and then cauterised. The ovaries and hepatopancreases were dissceted out aficr two weeks for histological observation and biochemical determi- nation (UV spectrophotometry). Gonad index was increased more than 2% in ablated prawns compared with 0% forthe controls. Mean oocyte diameter was also increased from 128 um to 850 jum in oyestulk ablated prawns, The number of yolk granules in oocytes was markedly preaterin eyestalkless than in intact prawns. The pyknotic index of hepatopancreas cells of ablated prawns was about 3 times greater than that of the controls, At the same me, & looser arrangement of hepatopancreas cells was observed after the operations than thaliseen in the lissue of the controls. The contenty of total proteins, lipids and carbohydrates in the ovary of the destalked animals were significantly increased (P<0.05) although those in hepatopancreas were decreased coinciden- tally. However, the content of rihonucleic acid was not signil- ivantly different between two organs, Based upon these results, the differences in biochemical con- stituents and the histological changes, demonstrate that organic reserves from the hepalopancreas might be mobilised into the ovary during ovarian maturation induced precociously hy cyestalk ablation. The present results show that metabolic changes within the ovary and the hepatopancreas might be closely related and controlled by neuroendocrine factors. Yong-Dal Yoon, tong Min Kim and Eun Byun Chun, Department of Biology, College of Natural Sciences, Hanyang University, Seoul 133-791, Korea. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 283 PATTERN AND PERSISTENCE IN THE BURROWS OF TWO SPECIES OF THE FRESHWATER CRAYFISH, PARASTACOIDES (DECAPODA: PARASTACIDAE}), IN SOUTHWEST TASMANIA Parastacoides spp. burrow extensively in the acid, peaty soil of weslern Tasmania and two or more species can commonly be found in close sympatry. The habitat is often partitioned zonally on the basis of soil conditions, especially drainage, on slopes (Richardson and Swain, 1980). This paper describes a mosaic of habilat partition benween Iwo undescribed species, Methods The field site, i southwest Tasmania, consists of an area of gently-sloping heathland (annual rainfall c. 2000 mm; mean maximum daily remperatures: 22.8°C; Watson, 1978), On a grid of 108 contiguous 4m” quadrits, [he positions of all burrow entrances of each species were recorded fourtimes fram 1980 to 1990. Parastaceides sp.1 constructs burrows with several entrances grouped in and around a water-filled depression, while P. sp.2 burrows have only one or two entrances which are ofien ronfed over with excavated soil, Seven environmental parameters were measured in each quadrat: buttongrass area, soil depth, soi! compressibility, water contlen!, root depth (proportion of the sojl profile occupied by roots; this horizon was clearly demarcated fram inorganic soil below), mean water table depth, and water table variability. Results and Discussion About 160 P. sp.1 and 150 P. sp.2 entrances were present, the species sometimes within 2m of each other. The general pattem of burrow distribution varied very litle over 10 years with no major burrow systems (these mostly belong to P. $p.1) appearing or disappearing. There has been some turn- aver in the overall number of entrances in both species, highest in P. sp.2, and an overall decline in the number of FP, sp.2 entrances. In these peaty, sedgeland habitats at least, Parastacaides burrows persist much longer than their inhabitants because the soils are very coherent and because the occupants do yt have to burrow extensively to obtain food (Growns and Richardson, 1988). Since the burrow systems are occupied by only a single adult, and burrow occupancy is preaier than 9U%, (he stability of the burrows over the 10 year period argues thal the craylish populations ate stable, or in the case of P. sp.2, declining, Since uncolonised habitat appears ta be available to both species, what factors control population numbers? Dry conditions in southern Tasmania over the last 10 years may be responsible for the decline in P. sp.2. This species occupies a drier part of the habitat and, although it can lolerate a few weeks without free wajer in its burrow (Fradd, 1979), itis probably more vulnerable to drought than P. sp.1. For P. sp. |, food seems unlikely to be limiting (Growns and Richardson, 1988), physical space is available and pre- dation of adults by birds and marsupials only occurs rarely. But there ts heavy juvenile mortality during the year, or more, which they spend in the parental burrow, and there mus} also be heavy mortality when the sub-adalts.¢stablish new bur- rows. Only one new system was observed in the course of this Study, so Sub-adults apparently take over vacant burrows. The quadrats were ordinated an ihe basis of the 7 en- Vironmental variables, appropriately transformed, using principal components analysis. The first two axes accoumed for 77.5% of the overall variation, The quadrats grouped on the basis ot the identity of burrows which were within 0.5 m of the centre of the quadrat (where the environmental varia- bles were measured): the groups were clearly separated. P. 5p: 1 burrows were associated with deeper, wetter. spongicr soils. Unburrowed quadrats were not separaled from bur- rowed ones, suggesting that the habitat is noi saturated. Other Purastacoides spp, (Richardson and Swain, 1980; Richardson and Horwitz, 1988) occur parapatrically where better drained soils on slopes rise Out of deeper muck peals on valley floors; this pattern has been observed between the twa species studied here at a neighbouring site. But where slopes are shallow, the change in soils is indistinct and the resulling mosaic of conditions allows fine scale coexistence as described here. Acknowledgements Thanks to those who helped in the field, Stephanis Kalish for laboratory assistance and the Tasmanian Deparmmen) of Parks Wildlife and Heritage for permission to work in the Southwest National Park. Literature Cited Fradd, P.J, 1979. ‘Aspects of the ecophysiology of the fresh- waler crayfish Parastacerdes tasmanicus (Clark 1936)". Unpublished Ph.D. thesis, Department of Zoology, Uni- versity of Tasmania. Growns, 1,0. and Richardson, A.M.M. 1988. The diet and burrowing habits of the freshwaler crayfish Parasta- coides tasmanicus tasmanicus Clark (Decapoda: Pura- stacidae). Australian Journal of Marine and Freshwater Research 49: 525-534. Richardson, A.M.M. and Horwitz. P,H.J, 1988, Habitat par- titioning in parastacid crayfish. Freshwater Crayfish 7: 91-97, Richardson, 4.M.M. and Swain, R. 1980. Habitat require- ments and geographical distribution of three subspecies ol Peraslucoides tasmanicus and Engaeus cisiernuriuy (Crustacea, Decapoda: Parastacidac), burrowing cray- fish from south west Tasmunia. Australian Journal of Marine and Freshwater Research 31; 475484. Watson, B, 1978, ‘Climate, Lower Gordon River Scientific Survey’. (Hydro-Electric Commission! Hobart). Sip. Alastair M.M. Richardson and Roy Swain, Department of Zoology, University of Tasmania, Bax 252¢, GPO Hobart, Tasmania 7001, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ig GREGARIOUS BEHAVIOUR CRUSTACEAN MICRONEKTON: ECOLOGICAL PERSPECTIVE Aguregalions of aquatic crustaceans are customarily re- garded as transient phenomena; groupings that have arisen through the agency of hydrological or meteorological factors, of through intermittent intrinsic factors, e.g. need lo feed, mate or avoid predators, Small size or low taxonomic level is usually associated with planktonic rather than micto- nektonic existence. However there is abundant evidence that euphausiids, mysids, decapods and even copepods can exert some considerable influence over their posilion in the water column and have Underrated powers of swimming. We present evidence to show that many of these organisms are naturally gregarious and that 4 range of selective forces hive favoured gregurious behaviour because of the advan- lages such associations offer over solitary existence. The principal selective forces are believed Lo be the same as those invoked to explain fish schooling. 1, Protuction from predators, By analogy with fish schools, advantages could accrue from a) early detection; b) allack dbatemont; ¢) predatot evasion, d) predator confusion (Pitcher, 1986), tn addition, if predators are uctually deterred from allacking schools or if carly detection results in avoidance of the predator before the need for strenuous excupe reactions, then there may be a cansiderable energy saving. There is strong evidence in support of a-d in escape responses of euphausiids and mysids, Ageregations have bven shown to modify their antipredator response according to the degree of threat and aggregative stale. The fact that school structure is only disrupted when the threaLto individu- als hecomes extreme, is strong evidence for the survival yalue uf grouping. 2. Improved feeding. Again by analogy with fish schools, the advantages should accrue from: a) finding food faster; b) more time tor feeding; c) sampling food more effectively, Gd) information transfer; €) opportunity for copying (Piicher. 1986). Little diréct evidence exists in supportof these advan- IN AN MEMOIRS OF THE QUEENSLAND MUSEUM lages for gregarious crustaceans. In fact there is some con- flicting evidence to suggest thal higher foraging and teeding rales in lower density aggregations have 10 be (raded off againstsafety in large groups, However, these hypotheses ate difficult to test because of the problem of creating schools and presenting patchy food distributions in the water colunin in laboratory experiments. 3, Reproductive facilitation. There are many documented cases of crustaceans apparently aggregated tor the purposes of more efficient fertilisation, However, the effect of group size on feeundiry and reproductive success has not been tested. 4, Energy conservation. Neo data are available to test the possibility of hydrodynamie advantage by swimming in schools as has been suggested for fish. The swimming actions of crustaceans are fundamentally different from those of fish. This might be expected to result in differences in nearest neighbour distributions in schools of the two groups if ani- mals were exploiting vortices shed from swimming uppend- ages. No such differences have yet been described, Crustacean schools are strikingly similar to fish schools in internal structure and escape responses. A reluctance 10 dccept that many crustacean species ate naturally gregarious, and technical difficulties concerned with maintenance and recording of school behaviour In the laboratory, has delayed rigorous testing of the benefits of schooling as proposed above, Literature Cited Pitcher, T.J. 1986. Functions of shoaling behaviour in tele- ost. 294-336, In TJ. Pitcher (ed.) ‘The hehaveour of (eleast fishes’. (Johns Hopkins University Press: Bal- more}. A. Ritz and DP. O'Brien, Department of Zoology. University of Tasmania, Hobart, Tasmania 7002, Australia. EFFECTS OF HYDROSTATIC PRESSURE ON THE TIDAL VERTICAL MOVEMENT OF ACETES SIROGAE HANSEN (CRUSTACEA: DECAPODA) Acetes sibogae, collected at the mouth of Brisbane River (27°30'S, 183°12"B) and held in the laboratory for a min- imum of 10 days, wis Subjected to three levels (10, 16 and 26kPa) of constant pressure and three (friangular, quadratic and sinusoidal) circatidal pressure regimes with different propetiies in the rate, relative rate, and acceleration of change, to test two hypotheses; (1) hydrostatic pressure of circatidal frequency und amplitude affects the tidal vertical movement of A. sibogae directly and/or through entraining endogenous tidal rhythms, and (2) this shrimp responds tu amplitude, rate, relative rate and acceleration of hydrostatic pressure change. At constant pressures, test animals moved up and down through the water colunin in the test tank with short, noncir- catidal period, If contrast, A. sibogae responded to all the three cireatidal pressure regimes (triangular, quadratic and sinusoidal) both directly, by vertical adjustment in the water eolunin, and indirectly, by phasing endogenous rhythms in uphasic animals, Both mechanisms allow A, sthogae to react both predictively and immediately (0 pressure changes, The amplitude ‘of circatidal hydrostatic pressure waves was shown to be implicaied in initiating the tidal vertical move- mentof this shrimp, in contrast with the insignificant role of the rate, telative tate, or certain accelerations. This is not surprising since response to the amplitude of pressure change alone is an adequate action as there is greal regularity of changes in hydrostatic pressure associated with tides. Such actlons allow a predictable response, without the need to monitor changes inthe rare, relative rate und acceleration. Y. Xiao andi, G._ Greenwood, Department af Zoalagy, University of Queensland, Queensland 4072, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 285 SENESCENCE, FLUORESCENCE AND CRUSTACEAN AGE DETERMINATION Assessment of the age of individuals is currently a signif- scant problem in studies of crustacean population dynamics, specifically the management of commercially important crustacean stocks, which are coming under increasing threat of over exploitation, Several methods have been tried for assessing age in crustaceans, butall are severely restricted. The most widely used method, that involving prediction of age trom body size, based on growth rates determined from modal analysis, tag recapture programs or laboratory rearing, suffers a fun- damental problem’ — variability of growth raie between individuals, Individuals of the sume chronological age, Brow- ing in the same environmental regime, may sometimes differ in their size by an order of magnitude. This phenomenon clearly limits the usefulness of body size as an indicator of age. The wide application of this method of age prediction reflects the need for, but lack of, a suitable alternative. Thus, new approaches to crustacean age determination are essen- lial. Ettershank (1983) attempted to use the inlensily of extracted chloroform-soluble fluorescence to age field-cap- tured Antarctic krill, Euphausia superba. Similar extractable fluorescence had been shown to accumulate linearly with age in insects and was thought to be derived from the universally occurring lipotuscin age-pizment. Subsequently however, work by the presen! author and athers (Nicol, 1987; Sheehy and Ettershank, 1989; Sheehy and Roberts, in press),.some of which was on crustaceans of known age, revealed some serious flaws in the methods used by Ettershank and previous workers, Most importantly, ‘lipo- fuscin-like’ extractable Muorescence did not appear to bo derived from lipofuscin und ils inlensily bure little relation- ship to age. Recently, prominent workers in the broader field of gerontology have been voicing serious doubts about the hiochemical extraction method for lipofuscin determination (Sohal, 1987). Clearly, the polential of lipofuscin as am index of age in crustaceans required reassessment. Methods and Results Flvorescent morphologies! lipofuscin was identified in histological sections from a wide range of crustaceans, in- cluding several of economic imporlance (Sheehy, 1989, 1990a). Alternative quantification techniques were developed, Using fluorescence microscopy and new image analysis methods (Sheehy, 1989, 1990b). conclusive evi- dence of the physiological age dependence of lipofuscin accumulation in the Crustacea was obiained for the first time. in laboratory reared freshwater crayfish, Cherax quadricari- natus, of precisely known chronological age, lipofuscin quantities in the base of the olfactory lobe cell mass of the brain were superior predictors of chronological age (r= 0,96) to morphometric parameters, such as carapace length, nor- mally used for this purpose. While carapace length was able to place only 51% of the experimental individuals into their correct age class, lipofuscin volume fraction correctly placed 93% of the same. individuals. Lipofuscin volume fractions were similar in the olfactory lobes of crayfish of similar chronological age despite a wide disparity in bady size and weight, Discussion The present results suggest that lipofuscin has significant potential as an index of crustacean age. Although lipofuscin accumulates with physiological age, rather than strict chronological age, and its accumulation is affected by en- vironmental paramoters such as temperature (Sheehy, 1990b), growth is also influenced by environmental factors. At this slage, there is no reason to believe thal lipotuscin would nol be a superior predictor of age 10 body size under variable field conditions. Early results suggest that it may be possible to predict absolute chronological age of field ani- mals. using relatively simple luboratory established models incorporating ambien! lemperature (Sheehy, 1990b), Literature Cited Eltershank, G. 1983, Age structure and cyclical annual size change in the Antarctic krill, Euphausja superbu Dana. Polir Biology 2: 189-193. Nicol, 8, }987, Some limitations on the use of the lipofuscin upoing technique. Marine Biology 93: 609-614. Sheehy, M.R.J. 1989. Crustacean brain lipofuscin: an exami- nation of the morphological pigment in the freshwater crayfish Cherax cuspidarus (Crustacea: Parastacidae), Joumal of Crustacean Biology 9(3): 387-391, 1990a, The widespread occurrence of fluorescent morpho- logical lipofuscin im the crustacean brain, Journal of Crustacean Biology 14): 615-622. 1990b. Individual variation in. and the effect of rearing temperature and body size on, the concentration of fluorescent morphological lipofuscin in the brains of freshwater crayfish, Cherax cuspicatus (Crustacea; Par- astacidae). Comparative Biochemistry and Physiology 9M A): 281-286. Shechy, M,R.J, and Bttershank, G. 1989. Solventextractable, age pigmentlike autofluorescence and its relationship to growth and age in the waterflea Daphnia carinata King. Australian Journal of Zoology 36; 611-625, Shechy, M,R.J, and Roberis, B. tn Press, An alternative explanation for discrepancies in lipofuscin fluorescence data from insects, crustaceans and other aquatic species. Experimental Gerontology. ‘Sohal, R.S, 1987. Quantification of lipofuscin: a critique of the current methodology. Advances in the Biusciences 64. SS—9L. MRS. Sheehy, Zoology Department, University of Ouweensland, St Lucia, Queensland 4072, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 286 BRANCHIAL MODIFICATION OF URINE AND OSMOREGULATION IN THE LAND CRAB, BIRGUS LATRO (ANOMURA: COENOBITIDAE) The regulatory capacity of the excretory system of Birgus latra was examined in relation to osmoregulation in the terrestrial environment. On land the availability of salts and water in the diet and drinking water, and evaporalive waler loss, may yary widely. Successful land animals, e.g. insects, mammals, generally exhibit versatile control of urinary fluid output and salt concentration. Previous measurements on Biregus (Gross, 1955) indicated thal the urine, like that of other anomuran and brachyuran crabs, was isosmotic to the haemolymph. Harris and Kor- manick (1981) infetred that urine filtration continued even during desiccation. These observations suggested that Birgus may have a poor capacily for excretory regulation, the urine representing a potentially large drain on body water and ions. Gross (1955) postulated that Birgus osmoregulates be- haviourally by choosing between drinking water sources of different salinities. However, on Christmas Island, Indian Ocean, &. latra range up to several kilometres from the coast, and sea water is clearly unavailable to most individuals as a source of ions and water. In rain forest, crabs drink from temporary rainwater puddles. Crabs were maintained on fresh water and on saline (300, 600,1000 mosmol/kg sea water) drinking regimens. The final urine, released from the antennal organs, was confirmed to be isosmotic with haemolymph, However, Birgus exhibits branchial reprocessing of the urine, as postulated for some brachyuran terrestrial crabs (Wolcott and Wolcott, 1985, 1988). The final excretory product (‘P', Wolcott and Wolcott, 1988) differs greatly in composition and flow rate from the filtered primary urine and the Final urine, The urinary apertures are directed posteriorly and open undemeath the branchiostegites. Hydrophilic hairs on the sca- phognathites, branchiostegites and mouthparts convey urine Lo the gills and to the mouth. The volume of the urine is reduced by reingestion and its composition is modified by branchial ion transport processes. Switching between fresh water and saline regimens caused rapid compensatory adjustments to drinking tate, primary urine formation (51Cr-EDTA clearance), branchial ion reabsorption and P production. The volume and MEMOIRS OF THE QUEENSLAND MUSEUM concentration of the released P could be varied widely, e.g. {Na] and [Cl] <10 to >600 mmol/L. The combination of reingestion and branchial ion transport provides Birgus with a versalile, ion and waler conserving, excretory system, well-suited to its terrestrial habitat. Animals drinking fresh- water effectively reabsorbed more than 90% of the filtered water, and more than 99% of the filtered sodium and chloride. In animals drinking sea water, reabsorption of each of these components decreased to about 70%. This regulatory role for the gills is supported by strong uptake of Na and Cl from experimentally recirculated salines and by the demonstration of high activities of Na + K activated ATPases in gill extracts. Literature Cited Gross, W,J. 1955. Aspects of osmotic regulation in crabs showing (he terrestrial habit. American Naturalist 89: 205-222. Harris, R-R, and Kormanik, G.A. 1981, Salt and water balance and antennal gland function in three Pacific species of terrestrial crab (Geearcoidea lalandii, Cardi- soma carnifex, Birgus latro), \| The effects of desicca- tion. Journal of Experimental Zoology 218; 107-116, Wolcott, T.G. and Wolcott, D.L. 1985, Extrarenal modifica- tion of urine for ion conservation in ghost crabs, Ocy- pode quadrata Fabricius. Journal of Experimental Marine Biology and Ecology 91: 93-107. 1988. Availability of salts is not a limiting factor for the land crab, Gecarcinus lateralis (Preminville). Journal of Ex- perimental Marine Biology and Ecology 120; 199-219. HH. Taylor, (address for correspondence) Department of Zoology, University of Canterbury, Private Bag, Christchurch, New Zealand. P. Greenaway, School of Biological science, University of New South Wales, P.O, Box 1, Kensington, New South Wales 2033, Australia. §. Morris, Department af Zoology, University of Sydney, New South Wales 2006, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM A STUDY ON FEASIBILITY OF CHROMOSOME SET MANIPULATIONS IN THE MARINE SHRIMP, SICYONIA INGENTIS The feasibility of manipulation of chromosome sets was studied in the ridgeback prawn, Sicyonia ingentis, to develop new techniques for chromosome karyotype study in shrimps, to elucidate the effects of hot and cold shock or chemical induction on chromosome set manipulation, and to present a cytological analysis of haploidy, diploid Ch ig a ae un a Ra Bd SK AR AN ES ga ne | {8 a6 ae aa C068 6a 88 ba As at § FIG. 1. Karyotype of the marine shrimp Sicyonia ingentis (2n = 50M + 14SM). FIG. 2. Haploid chromosome of Sicyonia ingentis, from nauplius. 287 FIG. 3. Polyploid chromosome of Sicyonia ingentis, from egg under fluorescence microscopy. triploidy and other polyploidy. Artificially induced spawned eggs of this shrimp were fertilized by UV-ir- radiated sperm from the seminal receptacles of the females to induce haploidy. Normally fertilized eggs were subjected to hot, cold or chemical (colchicine or cytochlasin D) shock to induce polyploidy. This study showed that S. ingentis has 64 chromosomes (50M + 14SM) using newly developed techniques with embryos and nauplii. Chromosomes were detected success- fully by fluorescence microscopy and/or air-dried method. Haploidy was induced by UV-irradiating sperms and higher haploid rate was observed in eggs than in nauplii. Triploidy and/or tetraploidy were obtained in the polyploid inducing experiments. The efficiency of induction depended heavily on the time between spawning and treatment, temperature, and duration of treatment. Because the eggs were too fragile to be handled before the formation of hatching envelopes, the second polar body could be retained more easily than the first one. However, an optimal procedure for treatment needs to be developed. J.H. Xiang, Institute of Oceanology, Academia Sinica, Qingdao, People’s Republic of China. W.H. Clark, F. Griffin and P. Hertzler, Bodega Marine Laboratory, California, U.S.A. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 288 GENETIC IDENTIFICATION OF TEN SPECIES OF PENAEID PRAWN POSTLARVAE A study of the ecology, recruitment and dynamics of the early life-history siages of pengeid prawns is being under- taken in the Gulf of Carpentaria, northern Australia. It is essential in this study to identify to species level the in- dividual pengeid postlarvae. Wentfication of specimens to species group is possible using morphological characters, however it has proved very difficult to identify all species in this way. Some of the complicating factors in this have been: the small size of individuals (down to 1mm carapace length). developmental changes, benthic collection often resulting in broken or damaged bodies, and the large numbers requiring identification. Allozyme electrophoresis was thus employed as a tool which could solve these problems. Two primary criteria were set for the choice of appropriate genetic enzyme markers. Firstly, the enzyme loci must ex- hibit a reliable and consistent difference between species Which must have a true genetic basis. Secondly, the enzymes must be sufficiently strong, hardy and casy to detect. to allow the simple and rapid identification of large numbers of in- dividuals. After examining the developmental expression of 39 enzyme loci, 2 loci, Gpi (Glucose-6-phosphale isomerase) and Pep (Peptidase, leucyl-glycine as substrate) were found which together could unambiguously identify ten species of prawn postlarvae withm the genera Penaeus und Meta- penaeus. These species were: the tiger prawns Penaeus mon- odon, P, esculentus and P. semisulcatus, the banana prawn P, merguiensis, the king prawns P. latisulcatus and P. lon- pistylus, the endeavour prawns Metapenaecus endeaveuri and M. ensis, the york prawn M, eboracersiy and the greasyback prawn M. moyebi. The techniques used (Lavery and Staples, 1990) were designed to maximise the efficiency of the identification procedure and are summarised as follows: |) Frozen in- dividual postlarvae plus 5 microlitres of buffer were placed in the wells of a perspex grinding chamber which had 24 wells in one line, 2) All 24 specimens were homogenised thoroughly at the same time using a 24-pin plate. 3) A sloued applicator was used to pick up a small quantity of liquid extract from all 24 specimens al one time and apply them to a cellulose acetate plate. 4) Electrophoresis was carried out for 90 to 150 minutes, followed by staining for a specific enzyme, either Gpi or Pep. Using the two loci together, and referencing the observed banding patterns with known controls, all ten species could be identified (Fig. 1), Fewer than 5% of individuals could not be accurately identified because of low activity or smearing of bands. The technique has proved to be very efficient, with MEMOIRS OF THE QUEENSLAND MUSEUM Speces Mand Mens Mimoy Mebo Pisc Psem mon Pict lang Pmerg ~- @@ e® e RELATIVE MOBILITY FIG. 1. Diagrammatic representation of banding patterns of len penaeid species for the joci Gpi and Pep, the whole procedure being carried out in less than three hours, thus making il possible for one technician with minimal equipment to identify 300 individual prawn postlarvae per day. Over 20,000 penaeid postlarvae have already been iden- tified using this technique in the continuing programme of research on penaeid prawns in the Gulf of Carpentaria. Acknowledgements Considerable thanks musi go to all the CSIRO staff who collected the specimens used in this study. Literature Cited Lavery, S. and Staples, D. 1990, Use of allozyme electro- phoresis for identifying two species of penaeid prawn postlarvae, Australian Journal of Marine and Freshwater Research 41: 259-266. Shane Lavery, Zaology Department, University of Queensland 4072, Australia. Michael Cosgrove, CSIRO Marine Laboratories, P.O, Box 120, Cleveland, Queensland 4163, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum DEVELOPMENTAL CHANGES IN THE BIQENERGETICS OF DECAPOD LARVAE K. ANGER Anger, K. 1991 09 01: Developmental changes in the bioenergetics of decapod larvae. Memoirs of the Queensland Museum 31: 289-308. Brisbane, ISSN 0079-8835, Developmental changes in binenergetic traits of larval Decapoda are reviewed, comparing subsequent stages of a moult cycle. larval instars, or different taxa thal are considered to represent a phylogenetic sequence. Recent dala suggest that some developmental trends in energy partitioning might be similar on all these levels of comparison. These tendencies imply: decreasing instantaneous growth rules, increasing melabolic loss, decreasing, net growth efficiency, and an increasing dependence an energy reserves accumulated in earlier stages of development. They are interpreted as signs of an increasing degree of lecithotra- phy in late stages of a moull cycle, Jute instars of larval development. or in evolutionary advanced taxa within a phylogenetic sequence, respectively, Biochemical changes suggest a developmental shift in predominant growth mechanisms, from hypertrophy (enlargement of average cell size during development, accumulation of lipid reserves) toward hyperplasy (increase in cel) number, protein accumulation). Within a moult eyele, the latter phase hecomes in principle independentof external energy supply, when a critical point (the ‘ point of reserve saturation’, or ‘Dq threshold’), has been passed. Such a binenergetic transition, from 4 phase of energy accumulation to one of epidermal reconstruction, can uccur also between successive instars of development: in hermit crab develapment, the megalopa reaches metamorphosis exclusively with energy accumulated by preceding instars. This mode of development, termed secondary lecithotrophy, is interpreted as an adaptation to extremely specialised habital requirements (here; amolluse shell). In the sequence Caridea— Astacidea—Anomura—Brachyura. there isan increusing trend in the average carbon/nitrogen talio of larvae, This suggests an evolutionary tendency in the larval development of the Decapoda toward an increasing lipid conlent and possibly, increasing degrees of secondary lecithutrophy and habitat specialisation, It corresponds with decreasing trends in the qumber and variability (the latter both in relation to number and morphology) of larval instars, and an increasing degree of morphological change during development. [j Crus- iacea, Decapoda, larval development, moult cycle, bioenergetics, growth mechanisms, K, Anger, Bialogische Anstalt Helzoland, Meeresstation, D-2792 Helgaland, Germany; 6 July, 1990. The bioenergetics of an organism can be defined through the construction of an energy budget that quantifies the fate of nutritional energy (Ivlev, 1945; Warren and Davis, 1967, Welch, 1968). The partitioning among the major energy flows (tissue and exuvia produc- tion, respiratory and exeretory losses) in crustaceans is illustrated in a schematic dia- gram that treats these flows as black boxes (Fig. 1). While bioenergetic aspects have been studied in great detail in adult Crustacea, those of their larval stages are much less known. In the present review, | summarise recent ad- vances in our efforts to open in larval decapod crustaceans those black boxes, and so under- stand in more detail how they function inter- nally, how they are connected among each other, and how such bioenergetic traits may change during development. Only two decades ago, virtually nothing was known about uptake and partitioning of nutri- tional energy in decapod larvae reared under controlled conditions in the laboratory. First quantitative data on feeding and growth were published by Reeve (1969) and Regnault (1969), who studied caridean shrimp larvae. Respiration rates had already been measured by Zeuthen (1947) in an unidentified zoea larva, and later by an increasing number of authorsin various larval decapod species (Schatzlein and Costlow, 1978), Mootz and Epifanio (1974) presented the first fairly complete energy budget fora larval decapod, the crab Menippe mercenaria. This study was followed by an increasing number of others that provided more or less complete information on energy partitioning in larval prawns, lobsters, anomurans, and brachyurans (Table |). Most of these budgets have in com- mon that they account for only grass changes during larval development, presenting ‘aver- age’ flow values for subsequent instars. Haw- ever, each larval instar undergoes during its 290 moult cycle a number of anatomical, physiologi- cal and biochemical changes that are controlled by hormonal processes (Christiansen, 1988). Hence, a much higher temporal resolution in sampling and measuring protocols, and consequently, consider- ably increased experimental and analytical efforts are necessary to study changes in energy partition- ing of decapod and other crustacean larvae in rela- tion to developmental processes. The first study that explicitly related bioenergetic changes in a larval decapod to the moult cycle was published only one decade ago (McNamara et al., 1980). The moult cycle can be devided into stages and substages, for which a classification system was introduced already half a century ago by Drach (1939). However, the first detailed description of anatomical changes occurring during individual moult cycles in a larval decapod appeared only recently (Anger, 1983). This description allows the identification of the major stages of Drach’s classi- fication system, and their use as a meaningful reference basis for the analysis of physiological and biochemical changes that may be observed during the course of larval development. The following synopsis will deal exclusively with changes in bioenergetic traits as results of developmental events, and it will be based mainly on information from a few intensively studied “model species’ such as the brachyuran crabs Hyas araneus and Carcinus maenas, and the hermit crab Pagurus bernhardus. In these instances, sufficient experimental data obtained under constant condi- tions have become available to allow some gener- alisations and modelling. Effects caused by external factors such as temperature, salinity, and food availability must be excluded here from this Teview. THE MAJOR ENERGY FLOWS The parameters of the energy budget (Fig. 1) are linked by the following equations, from which conversion or growth efficiencies can be derived (Ivlev, 1945; Warren and Davis, 1967; Welch, 1968): G=Gr+Ge=F-L-R-U [eq. 1] A=G+R+U=F-L [eq. 2] Ki = G/F [eq. 3] K2=G/A [eq. 4] where: A = assimilation of energy from food MEMOIRS OF THE QUEENSLAND MUSEUM Partitioning of energy Feeding (F) energy of food materials Assimilation (A) energy of assimilated materials Loss (L) energy of faeces, leached materials Excretion (U) energy of nitrogenous waste (mainly ammonia) Energy of metabolizable materials (physiological fuel value) Respiration Growth (G) (R) energy of accumulated materials standard metabolism, activity, SDA, moulting Exuvial loss Tissue growth (G, ) (G, ) energy of cast production of living exoskeleton biomass FIG. 1. Schematic diagram of energy partitioning in decapod larvae (after Ivlev, 1945; Warren and Davis, 1967; Welch, 1968). F = food uptake G = total body growth (briefly referred to as ‘ growth’) GT = tissue growth (production of living biomass) Gr = exuvia growth (production of cuticle materials) K = gross growth efficiency K2 = net growth efficiency L = sum of losses by defaecation and leaching (loss of small particles and liquid from food, due to ineffi- cient feeding mechanisms) R = respiration (measured as oxygen consumption) U = excretion of nitrogenous waste products (measured as ammonia production) In the above form, all parameters of the budget refer to gains or losses of energy that were inte- grated over some period of developmental time, for instance the duration of a given moult cycle (= instar) or of complete larval development ina given species; they are expressed in energy units (Joules) per individual. Instantaneous rates of BIOENERGETICS OF DECAPOD LARVAE 291 TABLE 1. Studies on energy partitioning in larval decapod crustaceans. Taxonomical position according to Bowman and Abele (1982). Infraorder Penaeidae Nephropidae Penaeioidea Astacidea Anomura Brachyura Paguridae Xanthidae Cancridae Portunidae Majidae Species References Remarks Penaeus monodon Homarus americanus Homarus americanus Pagurus bernhardus Menippe mercenaria Rhithropanopeus harrisii Cancer irroratus Carcinus maenas Hyas coarctatus Hvas araneus Libinia ferreirae Remarks: 1, only cumulative budgets (average flow rates) of successive instars; 2, excretion ignored, or added to faecal losses; 3, faecal losses calculated from difference between ingestion and assimilation, or ignored; 4, energy content of larvae estimated from dry weight or ash-free dry weight (assuming a constant energy content); 5, exuvia production not considered, or data taken from literature (from other species); 6, no energy budget given, but measurements from which a partial budget may be calculated; 7, ingestion rate not measured, i.e., partitioning only of assimilated matter considered; 8, excretion data taken from literature (from other species); 9, energy content of larvae and exuviae calculated from carbon values (Salonen et al., 1976). References: A, Kurmaly et al. (1989); B, Logan and Epifanio (1978); C, Capuzzo and Lancaster (1979); D, Sasaki et al. (1986); E, Anger, 1989; F, Anger et al. (1990); G, Mootz and Epifanio (1974); H, Levine and Sulkin (1979); I, Johns (1982); J, Dawirs (1983); K, Jacobi and Anger (1985); L, Anger and Harms (1989); M, Anger et al. (1989a). energy flow, e.g. growth rate; G, will be indicated by a point above the symbol; their dimension is: Joules per individual per unit of time (h!, or d’!). FOOD UPTAKE (F) AND Loss (L) The nutrition of decapod larvae under natu- tal conditions has been studied by few investi- gators (Lebour, 1922; Stickney and Perkins, 1981; Youngbluth, 1982; Harding ef al., 1983; Paul et al., 1990), so that we know very little about their actual food sources in the planktonic environment. These few field data as well as the overwhelming amount of labora- tory observations (Harms et al., 1991) suggest that most decapod larvae are omnivorous, with a general preference for zooplankton as a food source. In larval decapods, in particular in anomuran and caridean shrimp larvae, we observed fre- quently a very inefficient feeding behaviour: much prey is killed but then eaten only par- tially. This phenomenon (‘sloppy feeding’) was found also in some insect larvae (Johnson et al., 1975) and in carnivorous copepods (Ikeda, 1977), where it was termed ‘wasteful killing’ or ‘over-hunting’, respectively. Incomplete in- gestion of prey, together with leaching of liq- uid and small particulate materials from food during the feeding process (Dagg, 1974; Pe- chenik, 1979) leads to practically uncon- trollable losses and thus hampers the precise measurement of actual ingestion rates in de- capod larvae. The significance of this effect will probably vary with species and stage of larval development, and with the amount, size, and quality of food. The stage of the moult cycle has a significant influence on ingestion rates. Anger and Dietrich (1984) and Dawirs and Dietrich (1986) showed in crab larvae great daily vari- ability of feeding activity, mostly with high values in early stages (postmoult, intermoult), and strongly decreasing figures during the pre- moult phase of the same instar. Repeated ex- 292 0.55 0.50 0.40 0.35 Ingestion rate (J/d) = 123 4 5 67 8 9 101112 Megalopa Ingestion rate (J/d) Development (d) MEMOIRS OF THE QUEENSLAND MUSEUM 12 Zoea II 1.0 +- 0.8 0.6 0.4 Ingestion rate (J/d) 0.2 = va d — Peas eS 123 4 5 67 8 9 10111213 | Hyas araneus I OB pre geese seen pseeseencnennnennenennnnsnraceennnnnannnnnnnnnnsnnnnansnnnnnnnnnnnneneen 0.5 0.4 0.2 Megalopa Specific ingestion rate 0 10 20 30 40 50 Development (d) FIG. 2. Hyas araneus. Changes in individual and energy-specific ingestion rates during larval development (units: Joules: individual -d-'; and fraction -d ', respectively) (data from Anger et al., 1989b.) periments with Hyas araneus larvae con- firmed these findings, with maximum inges- tion rates occurring progressively earlier in subsequent larval instars (Fig. 2). Similar pat- terns in F were found when phytoplankton instead of Artemia was given as food (Harms et al., 1991), suggesting an indirect endocrine control of feeding activity via the moult cycle. In the zoeal instars of H. araneus, they were described with quadratic equations, in the megalopa as an exponential function of time (¢) (Anger et al., 1989b): F=Fo tat—bt (zoea I, II) [eq. 5] F=Foe™ (megalopa) _—_[eq. 6] The constant F, represents an estimate of the initial (t = 0) feeding rate, and the fitted parame- ters a, b, and m define the curvature of these functions. ; When specific ingestion rates,F,/E (that is:F expressed as a fraction of larval energy content, E [both in Joules]), are plotted against time of development, decreasing values are found, not only within individual moult cy- cles but, on the average, also in successive larval instars (Fig. 2). According to these experiments, early spider crab zoeae may ingest up to almost one half of their own energy content per day, whereas the same instars eat much less (<20%- d’') in late pre- moult. The megalopa shows very low F/E rates throughout the moult cycle, still decreaseing before metamorphosis (Fig. 2). However, it remains uncertain how general these patterns in decapod larvae are, until BIGENERGETICS GF DECAPOD LARVAE data with a comparably high temporal resolu- tion are available for more species. Most ‘average’ ingestion rates reported in the literature (Table 1) are based on single measure- ments made in an unspecified stage of the moult cycle, in some cases even without specifying the larval instar, Thus,.such values must be treated with much reservation, as well as gross growth and assimilation efficiencies calculated from those feeding rates (see below), While the measurement of F suffers from great methodological difficulties, this applies even more to the determination of faceal and other losses summarised as L (Fig, 1), Con- sequently, most authors did not measure L directly, but estimated it from difference, F-4 (eq. 2). Since measurements ol F are nol precise. the same must be true for indirect estimates of L, Among the authors listed in Table 1, only Logan and Epifanio (1978) determined facces production directly in decapod larvae, RESPIRATION (R) Respiration rate is usually measured as oxygen consumption (ug Oyindividual'-t', or d') which can then be converted to metabolic energy toss, with an equivalent of 14.06 Joules per mg © (Gnaiger, 19833). Besides integrated respira- tory losses (R, in Joules per individual), | will distinguish here: (1) individual respiration rate (in ug O, or Joules-individual-h' or d''), for which I will use the widely accepted symbol vo, (instead of “rk”; Gnaiger, 1983b); (2) weight- specific respiration rate (90, ; in py O,in- dividual +h, ord, per unit |mg|of dry weight). The latter is a measure of the intensity of tissuc metabolism. It can be expressed also ws an energy-specific rate (related to energy accumu- lated in biomass; dimension: fraction-d'').. The term ‘respiration rate’ will indiscriminately refer lo both va, or Q0,, Values given in the literature represent Usually an undefined rate, somewhere between basal and active metabolism, normally considered as ‘routine metabolism’. This applies also to all sjudies listed in Table 1. Changes of respiration during individual lar- val moult cycles were studied in only a few decapod species. In first-instar larvae of a freshwater prawn, Macrebrachium olfersit, McNamara et af, (1980) found slightly decreasing metabolic rates. However, this ¢x- ample is very specific, as these larvae reveu! lecithotrephic development fram the egg to the second zocal instar, Also in the megalopa of the hermit crab Pagurus bernhardus, which 293 shows secondary lecithotrophy (Anger, 1989), decreasing respiration was measured during the moult cycle (Dawirs, 1984; Anger ee a/,, 1990), Like most other decapod larvae, the zocal in- stars Of the hermit crab, as Well a$ lobster (Homarus americanus) and crab larvae (Hyas araneus, H, coarctatus, Libiniu ferreirwe), take up food during their entire development, and their respiration increases during the course. of each moult cycle (Sasaki et ul,, !986; Jacobi and Anger, 1985; Anger et al., 1989a,b), No general correlation, however, was found between meta- bolism and feeding rate (Anger ef. al., 1989) or activity of digestive enzymes (Hitche and Anger, 1987; Harms ef a/., 1991), The general patterns that were found in both Hyas araneus and H. coarctatus larvae are il- lustrated, with the former species as an example, in Fig, 3; linear increase of respiration with line of development in the zocal instars, but a cycli- cal pattern in the megalopa, with substantial increase during each ecclysis. In the zoeal instars of Pagurus bernhardus, a lincar increase (z0ea 1, 11}, or a fairly constant respiration rate (zovu TH, (V) was also measured (Anger ef al,, 1990), Unfortunately, no’ data with a high temporal resolution are available for other decapod larvae. so thal generalisation of these patterns is nul possible at present, In Hyas spp. larvae GO, shows patterns of change during development thal are diflerent from those in vO,: high values after each ecdy- sis (postmoult) are followed by low rales throughout the intermoull and early premoull phases, and somejimes hy another increase during late premoult (Fig. 3). The same patterns were observed also in larval lobsters (Sasaki e¢ al., 1986), as well as in spider crab (Libinia Jerreirae) and hermit crab (Pagurus bernhar- dus) larvae (Anger et al., 1989a, 1990). These cyclic changes in the average metabolic activily of tissues may occur generally in crustacean larvae. They should be a result of particularly energy-consuming processes of integumerital growth and differentiation taking place shortly before, during, and after ecdysis (see below: mechanisms of growth). Average Qo, values decrease in most in- stances like during development from the first to the last larval instar. Only in larval lobsters was an increasing tendency observed (Sasaki e¢ al., 1985). The former trend is consistent with the general relationship of decreasing 00, with increasing body weight in animals (Zeuthen, 294 0.4 Hyas araneus = =z 5 Megalopa 2 2 x ial Zoea II = i=) < i) im! 4 ww ve a 7 — 20 30 40 50 Development (d) Hyas araneus Megalopa Excretion rate (J/d) 0 10 20 30 40 50 Development (d) MEMOIRS OF THE QUEENSLAND MUSEUM Megalopa QO, (ug 0,* mg W"* h”) 0 10 20 30 Goa Atomic O/N ratio 0 10 20 30 40 50 Development (d) FIG. 3. Hyas argneus. Changes during larval development in: rates of individual respiration (VO2; Joules ‘individual’ .d ), weight-specific respiration (QO; ; ug O2.[mg dry weight] -h’’), nitrogen excretion (u; Joules ‘individual .d’), and in the atomic O/N ratio (data from Anger et al., 1989b). 1947). This relationship was quantified in larvae of various decapod species (Logan and Epifanio, 1978; Schatzlein and Costlow, 1978; Anger and Jacobi, 1985). However, the patterns shown in Fig. 3 demonstrate that the respiration-weight relationship is superimposed by developmental events that are not neces- sarily associated with growth. NITROGEN EXCRETION (U) Ammonia is assumed to be the major ex- cretory product of larval decapods (Logan and Epifanio, 1978; Capuzzo and Lancaster, 1979; Johns, 1982). Dawirs (unpubl.) found, in addi- tion, some traces of urea production in Car- cinus maenas megalopa. Phosphate excretion has been measured only in some unidentified larvae isolated from plankton samples (Ikeda et al., 1982; values mucher lower than in N excretion) but no data from decapod larvae maintained under controlled conditions are available. Thus, the following review will deal exclusively with the excretion of nitrogenous waste products, namely ammonia, which is assumed to represent the major part of total excretion. It can be converted to energy with a factor of 24.87 J/mg ammonia-N (Elliot and Davison, 1975). ; Most investigators did not measure U as a part of the energy budget in larval decapods (Table 1). Some authors considered it as a part of faecal loss, which is not correct (it belongs to A: Fig. 1; Warren and Davis, 1967). The authors who measured it (Logan and Epifanio, 1978; Johns, 1982; Anger et al., 1989b) found, however, that it constituted only a minor energy flow. In spider crab (Hyas araneus) larvae, we found cumulative excretory energy losses of 2-5% of A (Fig. 7). These measure- ments suggest that nitrogen excretion increases during larval development, not only in absolute terms (per individual) but also in relation to the other energy flows. During individual moult cycles, excretion curves for spider crab larvae consistently showed a maximum approximately in the mid- dle (intermoult and early premoult stages) of the moult cycle (Fig. 3). Since almost no compara- ble information is available from other taxa, it is not known if these patterns are typical of brachyuran larvae. Data given by Sasaki et al. (1986) suggest that at least larval lobsters may RAIOENERGETICS OF DECAPOD LARVAE exhibit quite different patterns, with low excre- tion rates in intermoull. O/N RATIO The atomic O/N ratio may be used as an indica- tor of the relative significance of protein as an energy source (Mayzaud and Conover, 1988). Capuzzo and Lancaster (1979) and Sasaki ev al, (1986) found lower O/N ratios in stage IV lob- sters than in carliér instars, suggesting an in- creasing protein catabolism during larval development. Decreasing average values were also observed during the development of spider crab larvae, however, superimposed by variation during individual moult cycles (Fig. 3). According to these data, protein catabolism in Hyas araneus larvae is at a maximum during imermoull, whereas lipid and/or carbohydrates play a major role in the premoull and postmoult stages, GROWTH (G) Larval growth has been studied in many decapod species (Kurata, 1962; Rice, 1968; Hartnoll, 1982; Gore, 1985; McConaugha, 1985), but different units of measurement have been used: size, moult cycle duration, fresh weight, dry weight, ash-free dry weight, carbon, nitrogen, hydrogen, protein, lipid, or energy (measured by microcalorimetry or estimated from biochemical or elemental composi- tion). Dawirs.(1981, 1983), Anger and Dawirs (1982), and Sasaki et al, (1986) showed that fresh weight 1§. a Very poor measure of growth in crustaceans, as it does not reflect actual changes in living biomass during development or in relation to nutritional conditions. It should never be use«l as a reference unit for biochemical data (although some authors did this). Dry weight and ash-free dry weight are certainly better measures of biomass. Carbon and nitrogen measurements proved to be especially accurate and reproducible. They show highly sig- nificant relationships with the energy content (Salonen etal., 1976) and with the major biochemi- cal components, protein and lipid (Anger and Harms, 1990). These different measures of bi- omass can be converted into each other, either using such empirical relations or a stoichiometric model (Gnaiger and Bitterlich, 1984). Not only different measures of biomass have decn used, butalso conflicting models of growth. Probably the most frequently used ts “Dyar’s rule’ or ‘Brook's law’ (Kurata, 1962). It de- scribes an increase in size or biomass as an exponential function of the number of instars: however, several authors used it to describe 295 growth as a function of time. Empirical data on instantaneous growth rates (s¢e below) show that this is. an crroncous use of the exponential mode), Anger and Dawirs (1982) expressed zoeal bi- omass in Hyay araneus (dry weight, C, N,H, or energy [ug or Joules: individual” ]; in the fatter case is: biamass = £) as a power function of time (2; [d}} within a given instar: F=Fo(t)” Jeq. 7] E, is an estimate of initial (¢ = 0) energy, and mis a fitted constant (the regression coefficient of the linearized form of the equation). This model was later applied also to other larval brachy- urans, Carcinuxs maenas (Dawirs, 1983), Hyas coarctatus (Jacobi and Anger, 1985), Inachus der setensis (Anger, 1988), Liocarcinus holsans (Harms, 1990), anc lobsters, Nephrops. norvegicus (Anger and Piischel, 1986). Another model, a second-order polynomial equa- lion, was applied to describe megalopa growth in Hyas spp., where biomass reaches a maximum in the middle of the moult cycle and then decreases, prior to metamorphosis (Anger and Jacobi, 1985; Jacobi and Anger, 1985), E=Fy+at-hi [eq. 8] £, (as in eq. 7), a, and } are fitted constants. Dawirs et al. (1986) suggested that this model might be better suited than eq, 7 for describing zoeal growth patterns, since they observed in Carcinus maenas zocae a decrease in biomass during late premoult, The same was found also in the zocal instars of the anomuran crabs Pagurus bernhardus (Anger, 1989; Anger et al., 1990) and Galuthea syuamifera (Anger, un- publ.), and in the larvae of the European lobster, Homarus gammarus (Messerknecht, pers, comm. ). ; Both models predict that growth rate (G, de- fined as change of biomass per unit of time, that is the first derivation of cqs. 7 and 8, respec- tively) will decrease during each larval instar: G = Wy = Forte 1 [eq. 9] feq. 10] G=e=a-2b1 G has the dimension [Joules:individual’! «d’'], Eq, 9 gives a hyperbolic, eq. 10a linear pattern of decrease (Fig. 4), Further data from more species 18 required to decide which model is a better description of larval growth patterns, if 4 universal pattern exists. The parabola-shaped bi- 296 MEMOIRS OF THE QUEENSLAND MUSEUM Growth rate (dE/dt) Growth.rate (dE/dt) Hyas coarctatus Hyas araneus zi Megal renee Megalopa 3 62 bnhomaaatormead eS Ai = .! a = oe fs Nt = 0.1 00 > o te Oo Inachus dorsettensis 0.0 -0.4 10 20 30 Development (d) Development (d) Development (d) FIG. 4. Changes in individual growth rates (G, Joules individual |: d') of decapod crustacean species during larval development. (sources of data: Messerknecht, pers. comm. (Homarus gammarus); Anger and Piischel, 1986 (Nephrops norvegicus); Anger, unpubl. (Galathea squamifera); Anger et al.,1990 (Pagurus bernhar- dus); Harms, 1990 (Liocarcinus holsatus); Dawirs et al., 1986 (Carcinus maenas); Anger, 1988 (Inachus dorsettensis); Jacobi and Anger, 1985 (Hyas coarctatus); Anger et al., 1989b, Anger and Harms, 1989 (H. araneus)). omass curve (with a final decrease) described by eq. 8 might be an artifact (although I do not consider this very likely) that could be caused by weak, slow-growing larvae that are proportion- ally more frequent in samples taken very late (after the onset of moulting) from a culture. Although the curvature of growth curves may remain uncertain, Fig. 4 shows one universal tendency in all nine decapod species and in a total of 34 (out of 37) instars considered: larval growth decreases during the course of individual moult cycles. Only in the zoea I and megalopa of Pagurus bernhardus and in the megalopa of Galathea squamifera, was a linear change in biomass, i.e. a constant growth rate (G), found (a negative value in the secondarily lecithotrophic hermit crab megalopa); in no case was an increase observed in G. This is important to note, as some authors attempted to estimate ‘average’ growth rates in plankton populations of decapod larvae, ap- plying an exponential model (see above) that predicts a progressively increasing G with time of development (Incze et al., 1984; Lindley, 1988; Paul et al., 1990). Since this model de- scribes only gross biomass changes in a series of subsequent instars as a function of instar number, not as a function of time, it has very BIOENERGETICS OF DECAPOD LARVAE Homarus gammarus Specifle growth rate (dE/E*dt) Pagurus bernhardus 297 0 Carcinus maenas zi | Zi ZIV Megalopa Specific growth rate (dE/E*dt) 10 20 30 4 zu 0 ai) 20 #30 40 S50 60 Specific growth rate (dE/E*dt) 10 Development (d) 0 Development (d) 30 av Development (d) FIG, 5. Changes in energy-specific growth rates (G/E; fraction ‘dy of decapod crustacean species during larval development (sources of data: as in Fig. 4). poor predictive power when growth within specific instars is studied. Thus, ‘average’ growth rates calculated from it are likely to be physiologically unrealistic (Fig. 4), Such rough estimates, however, may be useful as overall indices of growth, when only a comparison of different environmental conditions is attempted (Paul eral., 1990). Naturally, the absolute growth rate (dE/di) de- pends also on the specific size of a larva: for instance, a late lobster larva may gain 100 times more energy perday than an early portunid crab larva (Fig.4). Thus, itis useful for.direct comparison to calculate specific growth rates: G_ dE _ [eq] E” Edt ~ [eq.7] leq. 11}, G_ dE _ [eq.10] 5 rE Edt [eq.8] [eq.-12], respectively Specific growth rates have the dimension of a fraction (or %) of E [d''|. Fig, 5 shows that post- moult G/E varies in most species and instars be- tween 0.15 and 0.40 (or 15-40 %), It decreases dramatically during later moult cycle stages, often teaching negative values. The average level of daily specific growth in subsequent larval instars remains constant or it decreases. In no moult cycle or series of instars were increasing rates observed. Crustacean growth is further complicated by a partial independence of the moult cycle from mor- phogenesis and growth (McConaugha, 1985). This is particularly obvious in caridean shrimp larvae, where moulting frequency may remain unaltered under suboptimal conditions, while morpho- genesis and growth cease, resulting in a highly variable number and morphology of larva! in- stars (Reeve, 1969; Knowiton, 1974). i) 'o ao Homarus americanus Exuvial loss (% LPM energy) = Exuvial loss (% LPM energy) “1 au ween] PS dossvesssnnetesectonssssusesvesentscnnserateasseceuvenstusstuneunrennnttteassnes ¢ Carcinus maenas Exuvial loss (% LPM energy) Z1 Zi 7 Ml “AV M Larval Stage MEMOIRS OF THE QUEENSLAND MUSEUM Nephrops norvegicus “i “At M Larval Stage FIG, 6, Exuvial loss (% of late premoult, LPM, energy) in successive larval instars of decapod crustaceans; Z I, I] etc.= zoeal stages; M= megalopa, (sources of data: Logan and Epifanio, 1978 (Homarus americanus), Dawirs, 1983 (Carcinus maenas), Anger, 1989 (Pagurus bernhardus): others as in Fig. 4). EXUVIA PRODUCTION (GE) The exoskeleton is an integral part of crusta- cean growth, but equally a loss, as it is cast when ecdysis occurs (Fig. 1). Like total biomass, its absolute quantity (in Joules. per individual) in- creases in successive larval instars at an expo- nential rate (Anger, 1984, 1989; Harms, 1990). In Fig. 6 data are compiled on exuvial Joss in larvae of decapod species, where measurements of late premoult biomass are available as a refer- ence basis. It shows that anomuran and brachy- uran zoeae shed c. 3-7% of their total late premoult energy, whereas the megalopa instar. as well as lobster larvae, lose higher percentages with theit exuviae. Except in portunid crab spe- cies, there is a clear increasing trend not only in absolute (per individual), but also in percentage exuvial loss of subsequent larval instars (Fig. 6). Among the species compared in Fig. 6, Hyas arqneus reveals intermediate G, values. During its complete larval development it casts <6% of total energy ingested as exuvial matter (Anger and Harms, 1989), two thirds of this loss occur- ring in the final (metamorphic) moult from the megalopa to the juvenile crab. In relation to total BIOENERGETICS OF DECAPOD LARVAE chergy assimilated, the exuvial loss amounts here to 5—9% per instar (Fig. 7). The fraction of total growth (G) thal is lost as exuvial energy, increases in Hyas araneus larvac from 9% (zoea I) to 13% (zova TI), and eventually 35% (megalopa). Similar or higher losses were found in larval Menippe mercenaria (Mootz and Epifanio, 1974), Homarus americanus (Logan and Epifanio, 1978), Rhithropanopeus harrisu (Levine and Sulkin, 1979), Carcinus maenas (Dawirs. 1983), and Nephrops norvegicus (Anger and Piischel, 1986). Lower values (mostly <5%) were reported for Cancer trraratus (Johns, 1982), Lio- carcinus holsatus (Harms, 1990), and Pagurus bernhardus (Anger, 1989). In general, the data reveal that G_ tends to increase during larval development both in absolute terms, and as a percentage of either late premoull biomass & SUMMARY BUDGETS AND EFFICIENCIES Quantitative information on uptake of food (F) and on losses that occur prior to assimilation (L = F-A; eq. 2), is in general considered unreliable (see above). Thus, changes that may occur during development in assimilation efficiency (A/F) and gross growth efficiency (K,; ¢q. 3) will not be discussed here in detail, since both indices of food conversion are seriously affected by low precision of F measurements (Pechenik, 1979), Some possible patterns of developmental change were discussed recently by Anger and Harms (1989). For cumulative budgets of complete larval development of decapod crustaceans, Mootz and Epifanio (1974), Logan and Epitanio (1978), Levine and Sulkin (1979), Johns (1982), and Anger and Harms (1989) calculated A/F values ranging from 45-81%. Lower assimilation elfi- ciency (22%) was found by Dawirs (1983). Cumulative K, values of complete larval development were found in most species to range from 27-30% (Mootz and Epifanio, 1974; Logan and Epifanio, 1978 Levine and Sulkin. 1979: Johns, 1982; Anger and Harms, 1989), whereas Dawirs (1983) observed a cumulative K, of only 3% in Carcinus maenas larvae , The overall partitioning of assimilated energy (A) is exemplified with data ftom Hyas araneus (Fig, 7). In this species, the portion of A that is channelled into growth (K,) decreases in sub- sequent instars from 59-26%, while respiratory (R) and excretory losses (UV) increase from 39— 69%, and 2-5%, respectively, Within G, cxuyial loss (G,) increases in successive instars, whereas tissue production (G-,) decreases. Assimilation: 2.72 Sind ‘Total growth: 161 Jind (59 Ge Exuyia: 0.14 And (5%) iY Respiration: 1.05 Sind (49 9%) yas araneus Exovin: 0,35 J/itd (7%) Assimilation: 5.00 Jfiad Total growth; 2.62 Mlid (52 %) Ny] Respiration: 22d Hind (45 4) Neexcrbtion; Cid Jzind CE) Zoea ‘Tissue growin: £80 T/faw 117 %) ‘Total growth: 2.79 Mind (26%) Respiration: N-exeretion: 7.46 Wind (59h) 0,50 Hind (5%) SS | Megalops FIG: 7: Hyas araneus. Partitioning wf assimilated energy (A) in successive larval instars (Joules, in- dividual, and % of A) (data from Anger et al., 1989b; Anger and Harms, 1989), With respect to changes in K, during larval development, some authors (compiled by McConaugha, 1985; Stephenson and Knight, 1980) found an increasing tendency from instar to instar, whereas Reeve (1969) and a number of other authors (Fig, 8) observed the opposite trend. Since K, decreases during larval develop- ment in most species for which sufficiently pre- cise data with a high temporal resolution is available (Fig. 8), this may be considered more likely as a general pattern in decapod larvae. The discrepancy between K, values of early 300 Penaeus monodon Pagurus bernhardus MEMOIRS OF THE QUEENSLAND MUSEUM Carcinus maenas Net growth efficiency (Ky) i] f P21 PZ PZ AU My 7 My liMy 41 PLT a1 Zu Libinia ferreirae Hyas coarctatus zim ZIV Zi zn 2m Ziv M Hyas araneus Net growth efficiency (K2) ZI Zu M ZL Larval Stage Larval Stage Zit M ZW Zu M Larval Stage FIG. 8. Net growth efficiency (K2:G % ofA) in successive larval instars of decapod crustaceans; PZ= protozoea; My= Mysis; PL= postlarva; Z I, 1] etc.= zoeal stages; M= megalopa (sources of data: Kurmaly et al., 1989 (Penaeus monodon); Dawirs,1983 (Carcinus maenas); Anger et al,, 1989a (Libinia ferreirae), others as in Fig. 4). and late developmental instars appears particu- larly great in spider crab larvae. It is caused mainly by events that take place during the premoult (premetamorphic) phase of megalopa development, with feeding activity becoming very low (Fig. 2), and metabolic intensity of tissues remaining high (Fig. 3), As a con- sequence of F) during larval development of decapod crustaceans; Z= zoeal instars (sources of data as in Fig, 4). panied by decreasing grawth efficiency. Ecdysis initiates the next cycle, beginning again with higher K, values (Fig, 9). Since development proceeds and the absolute age of larvae in- creases with each subsequent instar, a decreas- ing trend should be expected also in average efficiencies of successive instars. Thus, it is hy- pothesised that tendencies of decreasing K, during development (Figs 8, 9) may be a typical hioenergetic pattern in decapod larvae. When different taxa are compared, highest avetage K, values (56-88%) were found in larvae of a penaeid prawn, lower values in anomuran zoeae (44-58%; the entirely lecithotrophic hermit crab megalopa is excluded from this comparison), and lowest in crab larvae (660%) (Fig. 8). [tis interesting to note that this sequence might reflect a phylogenetic tendency of decreasing net growth efficiency, from more primitive toward more advanced groups (for tax- onomy of Decapoda see Bowman and Abele, 1982). Since low growth efficiencies are ex- pected in partially lecithotrophic instars or spe- cies, this would suggest a phylogenetic tendency in the Decapoda toward an increasing degree of lecithotrophy and thus, of increasing ecological specialisation. This presumption is corroborated by differences in the average chemical composi- tion of decapod larvae belonging to different infraorders (Fig. 10; see below). However, special adaptations to environmental (including biotic) factors such as life of hermit crabs in a molluse shell, can occur in any taxonomic group and thus, there should be many exceptions to this hypothetically postulated rule. MECHANISMS OF GROWTH AND CONCLUDING REMARKS Available data suggest that the decreasing trends in growth rate (both per individual and per unit of biomass energy), as well as in net growth efficiency during development, may be a bio- energetic tule in larval decapods. These trends have clearly been observed during individu! moult cycles (Figs 4, 5, 9), and they occur in sequences of larval instars (Fig. 8). They may be seen also in phylogenetic development, from primitive toward more advanced groups (see above: K,), Presumably, the existence of such general patterns raises the question as to what mechanisms of growth may be involved and haw these may change during larval development. Data on elemental and biochemical compo- sition of decapod larvae reveal recurrent pat- terns of developmental change that are illustrated, again with Hyas araneus as a weill- documented example (Fig. 10). The carb- on/nitragen (C/N) ratio which is frequently used as an indicator of the lipid/protein ratio, shows here in all Jarval moult cycles an initial increase, followed by a transitory maximum, and a final decrease. When patterns of instan- lancous growth rates in C and N are compared (dC/dt, dN/dt), the following tendencies may be discerned: (1) an initial phase with high G. IL is characterised by particularly strong gain in C (i,e. lipid) and maximum C/N ratios ap- proximately at the end of the intermoult (stage C) phase of the moult cycle. (2) The rate of accumulation tn C (reflecting the lipid frac- tion) décreases dramatically, whereas that in N (protein) decreases more slowly. In late meg- alopa development, these differential slopes of instantaneous growth curves cause a reversal of biochemical patterns, with accumulation of N eventually exceeding thai of C (Fig. 10). These two distinct phases of growth corre- spond to those of an obligatory and a facultative 302 C/N weight ratio Growth rate (dC/dt; dN/dt) Development (d) MEMOIRS OF THE QUEENSLAND MUSEUM Megalopa Development (d) Average C/N weight ratio Caridea Astacidea Anomura Brachyure FIG, 10. Hyas araneus, Changes in the C/N weight ratio and jn carbon- and nitrogen-specific growth rates (dC/dt, closed symbols; dN/dt, open symbols; ug individual «d-) during larval development, A-E, stages of larval moult cycles (after Drach, 1939; Anger, 1983); data from Anger and Hirche, 1990. Lower tight: average C/N weight ralio (x =95% confidence intervals) in larvae belonging to different decapod infraorders (taxonomic position after Bowman and Abele, 1982; data from 3 species of Caridea, 2 Astacidea, 2 Anomura, and 10 Brachyura after Anger and Harms, 1990). feeding period, the latter in principle being inde- pendent of food (Anger, 1987). Thus, one can say that the final phase of the moult cycle (pre- moult) reveals a high degree of secondary lecithotrophy, as further developmentis possible with energy reserves that have been accumulated during earlier stages (postmoult, intermoult). The critical point that must be reached to allow autonomous development (the ‘point of reserve saturation’; Anger and Dawirs, 1981; Gore, 1985; Dawirs, 1986), was identified as the tran- sition between intermoult (stage C) and early premoult (stage Dg) and hence, was termed *D, threshold’ (Anger, 1987). Although larvae will continue to eat when food is available, the facultative feeding period is characterised, independent of feeding condi- tions, by low rates of food uptake (Fig. 2) and growth (Figs 4, 5), high metabolic loss (Fig. 3), and consequently, low net growth efficieny (Fig. 9), Apparently, morphogenetic reconstruction processes and other physiological and anatomical preparations for ecdysis (‘qualitative growth’) have during this developmental phase priority aver mere accumulation of energy (‘quantitative growth’), and their completion is secured by an increased degree of lecithotrophy. In a recent study on nucleic acids in Hyas araneus larvae, Anger and Hirche (1990) sug- gested that these two phases of growth may differ also in the telative significance of two major mech- anisms of growth: cell enlargement (hypertrophy) and cell multiplication (hyperplasy). Assuming constant amounts of DNA per cell and neglecting interstitial materials, the former type of growth may be measured as an increase in the DNA con- tent per individual, the latter as a C/DNA ratio, and synthetic activity of tissues may be indicated by the RNA/DNA ratio (Fig. 11). Mitoses take place continuously from hatch- ing of the zoea | to premoult of the megalopa instar, whereas maximum synthetic activity of tissues and an increase in average cell size were observed mainly in the initial (postmoult) peri- BIOENERGETICS OF DECAPOD LARVAE Hyas araneéus DNA (jg/ind) 303 Megalops C/DNA ratio RNA/DNA ratio 4 Development (d) Development (d) 6 8B Development (d) FIG, 11, Hyas araneus. Changes in DNA content (ug individual’), and in the carbon/DNA (C/DNA) and RNA/DNA weight ratios during larval development (data from Anger and Hirche, 1990). ods of larval moult cycles (Fig. 11). High initial rates of synthesis are suggested also by measure- ments of adenosine nucleotides in Carcinus maenas larvae (Harms et al., 1990b). They sug- gest a high turnover rate of ATP during post- moult and early intermoult, leading to a minimum adenylate energy charge in stage C, in spite of increasing ATP concentrations (Fig. 12). Ultrastuctural evidence (Storch and Anger, 1983), shows that this initial accumulation of energy reserves (mainly of lipids) takes place in R-cells of the larval hepatopancreas, where fat vacuoles are enlarged. Protein synthesis may be associated mainly with epidermal enlargement and reconstruction processes, and with hyper- plasy rather than hypertrophy (McConaugha, 1985, and earlier papers; Freeman, 1986, 1990, 1991; Freeman et al., 1983). Thé latter processes become independent of further exter- nal energy supply, when sufficient internal re- serves of energy and essential substances have been accumulated to allow autonomous development. This energetic status is normally reached in late stage C of the moult cycle, and it may may set the signal for increasing ecdys- teroid production in the larval Y-organs which then gives the stimulus for development through the premoult phase (Spindler and Anger, 1986; Anger and Spindler, 1987). Even when food is available, the premoult Stages are characterised by signs of an increas- ing degree of lecithotrophic development, with catabolism of lipid reserves (Fig. 10), no further increase in average cell size (Fig. 11: C/DNA), and decreasing ATP concentrations (Fig. 12). Like morphogenesis (Anger, 1987), these trends may be fairly independent of feed- ing or starvation commencing after the Dy thre- 304 Carcinus maenas ADP, AMP (nmol/mg protein) ATP (nmol/mg protein) Energy charge Development (d) FIG.12 Carcinus maenas. Changes in adenosine nu- cleotide concentrations (ATP, ADP, AMP: nmol ‘[mg protein] ) and adenylate energy charge during the moult cycle stages (A-E, cf, Fig. 10) of the zoea Linstar (after Harms et al., 1990). MEMOIRS OF THE QUEENSLAND MUSEUM shold (Dawirs, 1983; Anger and Spindler, 1987; Freeman, 1990, 1991; Harms et al., 1990). In the megalopa of Hyas araneus. the pre- metamorphic phase shows particularly strong signs of autonomous development, with recon- struction processes that are associated with dras- tic losses in the lipid fraction (C/N; Fig, 10), and probably with cell lysis (DNA; Fig. 11). If high C/N ratios are considered as indica- tors of a high lipid content and hence, an in- creased ability to develop without external energy supply, then this index suggests signif- icant differerences in the degree of lecithotro- phy among higher taxa of the Decapoda. In Fig. 10, larvae belonging to different infraor- ders were grouped in a sequence of increas- ingly advanced taxonomical position (Bowman and Abele, 1982). They show in this order a significant increase in average C/N ratios. This agreés with the tendency of de- creasing net growth efficiencies in the same sequence (see above; Fig. 8). Caridean shrimps should reveal, on the average, the low- est degree of lecithotrophy, brachyuran crabs the highest. This tendency corresponds to a decreasing number and variability of instars passed during larval development, and an in- creasing degree of morphological change in each moult cycle. The latter trend suggests that, as in insects, there may be an evolutionary ten- dency toward increasingly metamorphic devel- opment, While Caridea can respond to unsuitable environmental factors with addi- tional moults and reduced morphogenesis (Knowlton, 1974), the Brachyura are only mod- erately able to vary their number and morpho!- ogy of developmental instars, and hence depend more on sufficient energy reserves necessary for drastic reconstruction processes. Thus, bioener- getic traits of larvae may reflect phylogenetic trends, with an increasing degree of lecithotro- phy, increasing ecological specialisation, and an increasingly metamorphic type of develop- ment in the evolution of the Decapoda. ACKNOWLEDGEMENTS Our investigations on the bioenergetics of deca- pod larvae have been generously supported by the Deutsche Forschungsgemeinschaft (DFG; grants under An 145-1 and -2). 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Relationship between excretinn rates and body size, Australian Journal of Marine and Freshwater Research 33: 55-70. INCZE, L.S.. WENCKER, D.L. AND ARM- STRONG, D.A. 1984. Growth and average growth rates of tanner crab zoeae collected from the plankton. Marine Biology 84; 93-100, IVLEV, U, 1945. The biological productivity of wa- ters, Uspekhi Soureminnot Biologii 19: 98-120 (Translation, Fisheries Research Board of Canada, No. 394). JACOBI, C.C, AND ANGER, K. 1985, Growth and Tespiration during the larval development of Hyas coarctatus (Decapoda: Majidae). Marine Biology 87: 173-180. JOHNS, D.M. 1982. Physiological studies on Cancer irroratus larvae. Ul. Effects of temperature and BJOENERGETICS OF DECAPOD LARVAE 307 salinity an the partitioning of energy resources during development, Marine Ecology Progress Series 8: 75-85. JOHNSON, D.M., AKRE, B.G. AND CROWLEY, P.H, 1975. Modeling arthropod predation; wasteful killing by damselfly nalads. Ecology 56; LO&1-1093, KNOWLTON, R.E. 1974. Larval developmental Pracesses and controlling factors in decapod Crustacea, With emphasis on Caridea. Thalassia Jugoslavica 10; 139-358, KURATA, H. 1962. Studies on the age and growth of Crustacea, Bulletin of the Hokkaido Regional Fisheries Laboratory 24; )—115, KURMALY, K., YULE, A.B. AND JONES, D.A. 1989. An energy budget for the larvae of Penaeus monodon (Fabricius). Aquaculture 81; 13-25, LEBOUR, M.V. 1922. The food of planktun or- ganisms. Journal of the Marine Bidlogical Asso- ciation of the United Kingdom §2: 644-677, LEVINE, D.M. AND SULKIN, S.D. 1979, Partitioning and utilization of energy during the larval develop- ment of the xanthid crab, Rhithropanopeus harrisit (Gould). Journal of Experimental Manne Biology and Ecology 40; 247-257, LINDLEY, J.A, 1988. Estimating biomass and pro- duction of pelagic larvae of brachyuran de- capods in western European shelf waters, Journal of Experimental Marine Bivlogy and Ecology 122: 195-211. LOGAN, D.T. AND EPIFANIO, C.E, 1978. A labora- tory energy balance for the larvae and juveniles of the American lobster Homarus americanus. Marine Biology 47; 381-389, MAYZAUD, P. AND CONOVER, RB.J. 1988, O:N alomic rao as a tool to describe zooplankton metabolism. Marine Ecology Progress Series 45 289-302, MCCONAUGHA, J.R. 1985. Nutrition and larval prowth. 127-154. In A.M. Wenner (ed.) ‘Larval growth’. (Balkema Press: Rotterdam/Boston), MCNAMARA, J.C., MOREIRA, G.S. AND MOREIRA P.S, 1980, Respiratory metabolism of Macrobrachium olfersii (Wiegmann) zovu during the moulting cycle from eclosion tu first ecdysis. Biological Bulletin 159: 692-699, MOOTZ, C.A. AND EPIFANIO, C.E, 1974, An en- ergy budget for Menippe mercenaria larvae fed Artemiu nauplii. Biological Bulletin 146; 44-55, PAUL, AJ, PAUL, JM. AND COYLE, KO, 1990). Growth of stage I king crab larvae of Paralithades camtschatica (Tilesius) (Decapoda: Lithodidae) in natural communities, Journal of Crustacean By- wlogy 1h: 175-183. PECHENIK, J,A, 1979, Leakage of ingested carbon by gastropod larvae, and its effect on the calculation of assimilation efficiency. Estuaries 2: 45-49, REEVE, M.R, 1969. Growth, metamorphosis and energy conversion in the larvae of the prawn, Palaemon serratus, Journal of the Marine Biologi- cal Association of the United Kingdom 49; 77-96. REGNAULT, M., 1969, Etude expérimentale de lta nulrition d’ Hippolyte inermis Leach (Décapode, Natantia) au cours de son développement lar- vaire, au laboratoire. Internationale Revue det gesamten Hydrobiologie $4: 749-764. RICE, A.L. 1968. Growth ‘rules’ and the larvae of decapod crustaceans, Journal of Natural History 2: §25-530. SALONEN, K,, SARVALA, J, HAKALA, |. AND VILJANEN, M.-L, 1976. The relation of energy and organic carbon in aquatic invertebrates. Limnology and Oceanography 21; 724-730. SASAKI, G.C., CAPUZZO, J.M. AND BIESIOT, P. 1986, Nutritional and bioenergetic considers- tions inthe development of the American lobster Homarus americanus, Canadian Journal of Fish- eries and Aquatic Sciences 43; 2311-2319. SCHATZLEIN, F.C. AND COSTLOW, J.D. 1978. Oxygen consumption of the larvae of the de- cupod crusiaceans, Emerita talpoida (Say) and Libiria emarginata Leach. Comparative Bin- chemistry and Physiology 61A: 441-450, SPINDLER, K.-D, AND ANGER, K, 1986, Ecdys- teroid levels during the larval development of the spider crab Hyas araneus. General and Cam- parative Endocrinology 64; 122-128, STEPHENSON, M.J. AND KNIGHT. A.W. 1980. Growih, respiration and caloric content of larvae of the prawn Macrobrachium rosenbergii, Com- parative Biochemistry and Physiology 6A; 385-341, STICKNEY, A. P, AND PERKINS, H.C, 1981, Ob- servations on the food of the larvae of the north- ern Shrimp, Pandalus borealis Kréyer (Decapoda, Caridea), Crustaceana 40; 36-49, STORCH, V. AND ANGER, K. 1983. Influence of starvation and feeding on the hepatopancreas of larval MHyas araneus (Decapoda, Majidae), Hel- golinder Meeresuntersuchungen 36: 67-75. WARREN, C.E. AND DAVIS, G.B, 1967, Labora- lory studies on the feeding, bioenergetics, and growth of fish, (75-214. In §.D. Gerking (ed.) ‘The Biological basis of freshwater fish produc- tion’. (Wiley & Sons Inc,; New York), WELCH, H. E. 1968. Relationships between assimi- lation efficiencies and growth efficiencies for aquatic consumers, Eculogy 49; 755-759, YOUNGBLUTH, MJ. 1982. Utilization of a fecal 308 MEMOIRS OF THE QUEENSLAND MUSEUM mass as food by the pelagic mysis larva of the the animal kingdom with special regard to the penaeid shrimp Solenocera atlantidis. Marine marine micro-fauna. Compte Rendu des Biology 66: 47-51. Travaux du Laboratoire de Carlsberg, série ZEUTHEN, E. 1947. Body size and metabolic rate in chimique 26: 19-161. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE JOHN A, FREEMAN Freeman, J.A. 1991 09 01: Growth and morphogenesis in crustacean larvae. Memoirs of the Queensland Museum 3t: 309-319, Brisbane. ISSN 0079-8835. Crustaceans grow in a step-wise manner that is a function of the tissue growth during the moult cycle combined with stretch at ecdysis, moull increment. and moult cycle duration, In larvae, growth of the epidermis js also involved in the morphogenesis of integumental structures. To understand the mechanism and regulation of growth and integumental morphogenesis, tissue growth was studied in Palaemonetes larvae and Artemia metanau- plii. Increase in carapace length in Palaemonetes larvae is proportional to the growth of the underlying epidermis. Moreover, growth in the epidermis is highly correlated with that of the muscle. Both tissues show the greatest amount af growth during the first third of the moult cycle. Tissue growth and carapuce size were not affected by rearing temperature or exposure to the moulting hormone (20-hydroxyecdysone), factors that strongly affect moult cycle duration. Another factor, feeding regime, markedly affected tissue and carapace growth. The most critical period for food intake is the first third of (he moult cycle, Lis uncertain, however, whether nutritional state controls tissue growth directly or through other physiological processes. At ecdysts, hydrostatic pressure, under the control of the neurosecretory center, expands the new integument to a point equal to ihe amount of new lissue generated during the previous moull cycle, Although eyestalkless larvae grew more in carapace length than intact larvae, there is no difference in the amount of growth of the epidermis between the two groups, Uptake of water at ecdysis, then. serves to expand the new cuticle but, undernormal conditions, does nol affect tissue growth. Studies on segment morphogenesis in Artemia reveal that patterned cell replication is involved in growth and shape of the tharacic integument and, as a morphogenetic force. leads to regional differ- ences in cell density (hat are integral to formation of the arthrodial membrane and the thoracopod limb bud. The cell replication pattern may, in fact, be an initial step in cell differentiation. Thus, epidermal growth and morphogenesis. in crustacean larvae is a function of both the nutritional stale of the organism and cellular events that contral development. [] Crustacea, larvae, growth, morphagenesis. John A, Freeman, Department of Biological Sciences, University of South Alabama, Mobile, Alabama 36688, USA; 6 July, 1990. The presence of a restrictive exoskeleton in larval and adult crustaceans limits expansion of the integument to periods of ecdysis. The corre- sponding growth curve appears to rise in a step wise manner (Hartnoll, 1982; Botsford, 1985). The growth curve is a function of the time be- tween ecdyses, or moult cycle duration (MCD), and the amount of linear growth that takes place at ecdysis, or moult increment (M1). These fac- tors have been recently reviewed in depth by Hartnoll (1982) and Gore (1985). The growth curve is. generally species-specific and defines the relationship between larval size and duration of the larval period. Variation in the curve can result from sexual maturation, environmental factors (chiefly temperature), nutritional stress, and parasitism (Hartnoll, 1982). Crustacean larvae undergo a series of larval moult cycles, hereinafter referred ta as instars, before metamorphosis to the juvenile form. For each species, the number of instars may be con- stant Of may vary under certain environmental conditions (Broad, 1957b; Knowlton, 1974). Some degree of morphogenetic change is ob- served at each instar, and the schedule of the changes is in most cases so invariant that the morphogenetic state defines that particular instar (Broad, 1957a; Williamson, 1982). Develop- ment may be gradual (direct) with slight change at each ecdysis (e.g. Homarus, Artemia) or there may be one or more major changes in body form (indirect), as exhibited by barnacles and penaeid shrimp (Walley, 1969; Williamson, 1982). For each larval instar, the organism grows in size and changes form. Although these changes are manifested at ecdysis, the tissue changes occur continuously throughout the moult cycle. The constancy of growth and morphogenesis in the larval instars would suggest that both processes are interrelated and may be regulated by a com- mon mechanism. However, this mechanism has yet to be elucidated. aM In our studies of the control of growth and fnrphogenesis in crustacean larvae, we have examined the’process of growth in larvae of the caridean shrimp, Palaemenctes pugto, and growth and morphogenesis in larvae of the brine shrimp, Artemia. Since linear dimension is a function of the cuticle and the epidermis, growth in this tissue was used as 4 tool to differentiate between the factors that regulate moulting and MCDand those thal contro! MI (Fig. 1A,B), The larval epidermis is a two dimensional monolayer of cells whose primary role is to carry out the cyclica] degradation of the old cuticle and syn- thesis OF Ihe new cuticle, The cells actively par- ticipate in this function throughout most of the moult cycle with only a brief resting (inlermoult) period (Freeman and Costlow, 1980; McCo- naugha, 1985; Christiansen, 1988), In addition to its role tn cuticulogenesis, the epidermal cell replicates to increase the area of the monolayer and differentiates lo form specific integumental structures, MOULT CYCLE DURATION A primary component of growth is the moult cycle duration (MCD), The length of the moult cycle is temperature dependent, relatively con- Slant, and species-specific in the larval phases, while the juvenile and adult moult cycles in- crease in length with age. Although the regula- tion of the length of cach stage of the moult cycle remains unclear, it ts widely accepted that the endocrine systent controls the onset of premoult and ecdysis. During most of the intermoult pe- riod, the onset of moulling is blocked by moult- inhibiting hormone (MIR), a peptide secreted by jhe eyestalk neurosecrewory centers (Chang, 1985; Skinner, 1985). Cessation or reduction in production of MIH are presumed to initiate the onsel of proecdysis. This has been shown lot adults (Skinner, 1985) but has not been consis- tently observed in larvac. Eyestalk removal did not stimulate moulting in crab larvae (Castlow, 1966a,b) and shrimp larvae (Little, L469). A more frequent observation schedule revealed that eyestalk removal was effective in shortening the moult cycle (Freeman and Cosilow, 1980), The findings from these studies clearly show that the larvae are traversing the moult cycle at a rapid tale {hat can be only slightly accelerated. Promotion of the onset of premoult is control- Ied by ecdysone and 20-hydroxyecdysone (20H E\(Skinner, 1985), This regulatory step was demonstrated for larvae in barnacles (Freeman MEMOIRS OF THE QUEENSLAND MUSEUM and Costlow, 1983a), and crabs (MeConaugha and Costlow, 1981; Freeman and Costlow, 1984) when larvae exposed to 20HE entered premoult prematurely. Recently, ecdysteroid levels have been determined in lobster larvae (Chang and Bruce, 1981) and in crab zoeas (Spindler and Anger. 1986; Anger and Spindler, 1987). In both studies the hormonal titres resembled those of adults in thal the concentration declined follow- ing, postmoult, remained at a basal level for the short period of intermoult and then peaked during mid premoult. Moreover, by comparison to hormone profiles in adult crustaceans, the premoult rise appears to begin earlier than stage Doin some instars, Chang and Bruce (1980) also showed that the profile was similar during mul- tiple, shortened moult cycles in eyestalkless lob- ster juveniles. The titre increased at (he onset of premoult, which begun earlier, suggesting that the titre can undergo normal cycles even in the absence of MIH. Thus, the regulation of moult- ing hormone levels may be under the control of more factors than just MIH, Temperature has been shown to be a strong regulator of moult cycle duration in cnistacean larvae. There is generally an inverse relationship between temperature and MCD (Knowlton, 1974: Hartnoll, 1982), At the lower temperature range the MCD will be several times longer than thal seen al the optimal temperature. In some cases, the larvae will never moult, At the higher temperature range, the MCD will reach 2 point where il cannot be further accelerated. To find if the amount of growth during an instar was dependent on the MCD, temperature was used to control the MCD in instar JI Palae- moneles larvae, The MCD was inversely propor- tional to a temperature range of 15—30"C with larvae at the lowest temperature (15°C) demon- strating moult cycles of elmost seven days com- pared lo a two day MCD for those ar 30°C (Freeman, 1990b). The MI, however, was greatest at 20 and 25°C with the least amount of growth at 30°C. The results show that growth of {he carapace ther was dependent on temperatare but it Was independent of the MCD. Moreover, since all moult cycle stages were lengthened or shortened proportionately by these treatments, there docs not appear to be one phase of the moult cycle that must be of a certain minimum duration in order for growth to occur. Moulting hormones accelerate the onset of the premoult period and thereby shorten the injer- moult period in larvae of all crustaccans cx- amined (Skinner, 1985: Christiansen, 1988), GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE e * moUET CyoLe \ ~ FOOD SUPPLY (+) ~ 20-Me, MH TT) ~ PEPTIDE GROWTH FACTOR (7) > STRETCH AT ECOYSIS (7) j ( moutr _ { WCAEMENT E c D x. _—~_—. - ! MOULT CYCLE DURATION ' - 20: Lal — MIN t~) ~ TEMPERATURE (m= INSTAR A INSTAR ith a Moul a ari x } x |Maulb Cyc < H Dependen' © TISSUE GROWTH a 7 ~ Cam ay gf - Growth yod CELL DENSITY TNDERSHOOT DUE TO lcuricuLar STRETCH e uv ~ GROWTH FACTORS I=! ~ MOULT HORMONES [7) ~MOULT CYCLE DURATION = NUTRITIONAL CONDITIONS |+)-1 ~ SPECIES SPECIFICITY FIG. 1, Model of the growth process in crustacean larvae. A, Factors that control growth during one moult eyele, shawn as part of a growth curve. The moult cycle is the periad between ecdyses (E) and is divided into pastmoult and intermoult (C) and pre- moult (D) after Drach (1944). Factors that control moult cycle duration include 20-hydroxyecdysone (20HE), moult-inhibiting hormone (MIH), and temperature. The amount of growth at ecdysis, or moult increment, is affected by food supply, stretch ut ecdysis, and possibly moullting hormones and growth factors. B, Growth of tissues during the moult cycle. Growth could be moull cyele stage dependent Vf it occurs primarily during one siage of the moult cycle, or moull cycle stage independent if it occurs throughout the moult cycle. Here for example, the growth occurs during early premoult. When growth of the epidermis is seen as change in cell density.¢he density will increase during the moll cycle and then zelurn to a basal level at ecdysis, as Shown here for the change al ecdysis to instar Ill. After ecdysis, the density will again increase, If a greater than normal amount of stretch occurs, the density value will fall below the basal level (undershoot), The tssue may (compensatory growth) or may not be able to obtain the same density. Tissue growth js influenced by nutritional conditions, genetic factors (species speci- ficity), and, possibly, growth factors, moult control- ling hormones and moull cycle duration. Treatment with 20HE was used as a method to shorten the MCD in order to further examine the relationship of MCD and growth and to explore the role of moulting hormones in the growth process (Freeman, 1990b). Exposure of instar {1 Palaemonetes larvae to 20HE shortened the postmoult and intermoult periods by 33% bul did not noticeably affect the duration of premault. There was no difference in carapace length of the control and hormone-cxposed larvac. These findings support the contention that growth in crustacean larvae is not dependent on the MCD. The results also suggest that moulting hormone does not have any direct influence on growth of the larvae, The endocrine system, then, controls the moult cycle and the rate at which intermoulr (issue growth is tealised at ecdysis. However, the moulting hormone may possibly play a permis- sive role in growth by establishing conditions conducive to growth of the epidermal cells, e.g. cell division in late premoult, The conditions tested (2 day MCD, tempera- ture control; 36 hr intermoult stage C, 2(IHE control) did not permit a continuous attenuation of the MCD below a certain point. At some point in the abbreviation process, the larva would probably lose the ability to accumulate food reserves. At that point the synchrony of the com- plex cellular events would be disrupted, which would lead to decreased growth. Since one da of feeding is required to successfully moult (Freeman, 1990b), this may be the critical dura- tion although even lesser periods may be possible at higher temperatures. An obvious candidate for regulation of MCD is the quality and quantity of the food. Many studies have examined the tole of nutrition in crustacean growth, metamorphosis and survival (Broad, 1957b; Knowlton, 1974; Hartnoll, 1982; Gore, 1985: McConaugha, 1985). As expected, low rations of food limit growth. This result is confirmed during studies on the effect of feeding regime in shrimp larvae (Freeman, 1991). Several studies have clearly shown that normal MCD and morphogenesis is controlled by the nutritional condition of the larva (Broad, 1957b; Anger ef al., 1981; McConaugha, 1982; Anger. 1984; West and Costlow, 1988). MOULT INCREMENT Although increase in linear dimension is ob- served at ecdysis, the growth process occurs throughout the moult cycle (Frank er al, 1975; Sulkin ef al, 1975: Anger et al., 1989). These data, obtained primarily from biochemical ana- lyses. contain little information on the actual growth of the tissues. In this section f consider factors that: 1) play a role in the moult increment (M1) in the organism and influence growth of the tissues during the moult cycle, and 2) control expansion at ecdysis. Any cansideration of a growth mechanism must begin at the level of the gene. The disparate sizes are obviously a function of the genctic 312 2 mechanism that controls the MJ and, to a lesser degree, the MCD. For each species, there ap- pears to be a process that establishes a basa) MI under normal conditions (Rice, 1968; Hartnoll, 1982; Gore, 1985; Freeman, 1990b). External factors may act on this process directly or may control the rate at which the system operates. Future efforts aimed at understanding the genetic control of growth will greatly contribute to general knowledge of growth in crustaceans and other arganisms. Built into the growth controlling system in larvae is the ability to somehaw recognise their size or ‘growth stale” and to grow accordingly. A larva which is smaller than the mean size for that specics/instar/cohorn may grow more than larger larvae of similar age, and vice versa. This has been shown for Palaemon (Harinoll and Dalley, 1981}, barnacle (West and Costlow, 1987), and Palagmonetes (Freeman, 1990b), The manner in which this system functions ts not understood. Temperature appears to affect growth by con- trolling metabolism. There is an optimum temperature at which food conversion and ana- bolic processes take place and, as mentioned above, an optimum temperature for progression through the moult cycle. Growth probably oc- curs most efficiently at a temperature where the optima coincide, For larvae of Palaemonetes pugio this optimum is 25°C. Growth controlling hormones may include those that regulate moulting (mentioned above) and the hormonefs) that regulate hydromineral content. Eyestalk removal! in crustaceans has been shown to significantly decrease the inter- moult penod under conditions where the moull cycle progression is carefully monitored, indi- cating the presence of MIH in larvae. In addition to regulating the MCD, MIM could actually af- fect the growth behaviour of the cells, although na evidence of such a role for MIH has been presented. Growth does not appear to be alfected by MCD and ihe neurosecretory system is in- complete in carly larval instars, Thus, jt is un- likely that M1H participates in growth regulation other than the control of the MCD. In addition to moult cycle acceleration, eye- stalk remoyal results in a postmoult size that is larger than the comparable value for intact ani- mals. This has also been shown to be true for eyestalkless larvae of RAiviropanopeus (Kalber and Costlow, 1966; Freeman et al., [Y83), Ho- marus (Charmantier et al, 1984; Snyder and Chang, 1986), and Palaemonetes (Okazaki evat., MEMOIRS OF THE QUEENSLAND MUSEUM 1989; Okazaki, pers. comm.). The increased size is thought to be dug to enhanced uptake of water as a result of loss of the hormone that controls hydromineral balance (Mantel and Farmer, 1985). The higher than normal hydrostatic pressure stretches the new, soft integument beyond the limits established by tissue growth during the pre- vious instar. Thus, the stretch before hardening of the cuticle supercedes the growth potential, The mechanism of tissue growth under the conditions of supranormal haemolymph hydro- static pressure is beginning to be studied. Freeman et al, (1983) found that the density of the epidermal cells of juvenile Rhithropanopeus harrisii that had undergone four or five moult cycles following eyestalk removal during the larval period was greater than that of intact ani- mals although the carapace was much larger. These results indicated that the epidermal tissues of cyestalkless larvae somehow compensated for increased cuticle area after ecdysis by increasing cell growth and replication. Conversely, Okazaki et al. (1989) found that the increased stretch in eyestalkless larval and adult shrimp was nol accompanied by compensatory growth of the cells, Instead, the density remained lower than that of the intact animals. Comparable stu- dies with different species are needed to find 1) the most common growth process for crustaceans, and 2) if the response to stretch differs between stages of the life cycle within a single species, Not unexpectedly, nutritional state is a strong regulator of growth. Many studies have shown that food deprivation or differences in food qu- ality has a marked effect on growth (Harinoll, 1982; McConaugha, 1985; Anger, this volume), Recently, the feeding regime was used to cx~ amine the growth processes in Palaemonetes larvae (Freeman, 1990a), Feeding during the first two thirds of the moult cycle did not markedly affect the MI, indicating that sufficient food was stored during the intermoult and early premoult periods. Feeding only on the first or second days of the instar, however, resulted in levels of growth thal were intermediate between starved and continuously fed controls with more rowth observed in those larvae fed on day I of the instar. These findings indicate that feeding during the first third of the moult cycle is critical for successful growth, This period corresponds to the ‘point of reserve saturation’ (Angeér and Dawirs, 1981) or the threshold for growth and development (West and Costlow, 1988), while feeding on day 2 may be sufficient to reach the GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE 31 ‘Do threshold’ and moult, but With only slight growth (Anger, 1987), The first third of the moult cyele is clearly a period in which food assimilation is somehow monitored and trans- lated into actual tissue prowth or stored for further growth and morphogenesis. Why this phase should be so essential is not obvious. Several studies have shown that tissue growth occurs al this time (Frank ef al, 1975: Sulkin er al,, 1975; West and Costlow, 1987; Anger ev al,, 1989; Harms ev al., 1990), Feeding may become more active because apolysis and premoult changes have not yet begun. Interestingly. in the Palaemonetes feeding study, some growth oc- curred in starved larvae that survived instar II. This growth may have been fueled by food re- serves accumulated during the previous instar or mav have resulted from tissue catabolism. CELLULAR BASIS OF INTEGUMENTAL GROWTH IN CRUSTACEAN LARVAE To comprehend growth of the cuticle, it is necessary (0 understand how the process occurs in the underlying epidermis, This is best accom- plished by considering the cell cycle with respect to the moult cycle. Following the beginning of premoult, the epidermis increases in cell number by mitosis (Tchernigovtzeff, 1965, Halcrow, 1978), In Some larvae milosis may occur in pe- riods of the moult cycle other than premoult (Le Roux, 1978; Freeman, 1986), In either case, cell replication slightly increases the area of the epidermis. Cell replication and growth may occur to the extent that, in transverse section, the epidermis appears to be folded (Skinner, 1962; Freeman and Costlow, 1980), At ecdysis, the uptake of waler(DeFur et af, 1985) expands the new integument lo a point that will equal ils new size (Freeman, 1990b). Little information exists on the control of the cellular processes by external and internal fac- tors. To establish a conceptual framework, a model of the system relating tissue growth and the moult cycle is shown in Fig, 1B. The instar ID larva of Palaemonetes pugio is well-suited for this model since the epidermal ecclls of dorsal carapace exist as a monolayer which is spatially restricted sa thal its growth can be compared to change in the carapace dimensions (Fig, 2). The epidermal cel! density is found to increase only during the firs) day of the moult cycle in normal larvae (Freeman, 199(0b) (Pig. 3), At the end of this period the predicted prowith can be determined from the cell density. This is also the fab period when maximal growth of the muscle oc- curs (Schaff and Freeman, unpubl,), Preliminary findings show that the increase in cell density is aresull of enlargement of certain cells within the epithelium. The cells jhat enlarge appear t be cells that have divided during premoult of the previous instar. Their expansion slightly com- presses other cells in the monolayer, and results in the enhanced cel] density. Factors that affect MI do so through the growth of the epidermis, Growth of the epidermis in Palaemonetes is greatest at the optimum temperature of 25°C (Freeman, 1990b). Larvae exposed fo moulting hormone show no differ- ences in the epidermal growth, as was the case for MI. The strong effect of nutrition on ME is reflected in the cellular growth. An example of this relationship is. shown in Fig. 4, Starved larvae underwent little growth in the epidermis while larvae fed on day 1 demonstrated cell growth that was intermediate between fed and starved larvae. A direct correlation was observed between the increase in density by day two of the instar and the MI (Freeman, 1990b) The tissue, then, is able to respond to the nutritional state (or food storage) Very rapidly by growth of some cells leading to increased den- sily. Since the density does pot increase as much in starved larvae, the process of enlargement (G1 growth ?) may be controlled by sufficient uptake of food or upiake of certain compounds. The other growth phase ts the premoult period when cell division takes place. Little is known of how this phase is controlled by food uptake. One possiblity is that the cell cycle is controlled hy nutritional state such that a cell will make a decision to continue through 5, G2 and mitosis as a result of same signal propagated after feed- ing. Alternatively, a certain number of cells are stimulated to cycle during the feeding-sensitive period bul that other factors, generated during the remainder of the moult cycle, would contral their division. Several control points in the cu- karyotic cell cycle have been shown to exist A major point is the GI-S (or GLa-GIb) transition (Pardee, 1989), In the shrimp epidermis this may be seen as the enlargement of a few cells. An- olher control point ts the G2-M transition (Mur- ray and Kirschner, 1989). Since mitosis is most often seen in premoult, this decision may be one that is independent of the transition to S$ phase. These imriguing hypotheses must be empirically lested to determine how the epidermal cells are regulated by food intake and nutrition, From our preliminary studies it is clear that only 34 FIG. 2. Nuclei of the dorsal epidermis of live instar II Palaemonetes pugio. The nuclei are vitally stained witha nuclear fluatochtome bisbenzimide (Hoechst, 33342).Fluorescence image. Bar =50 um, certain cells, or a certain number of cclls repli- cate during the moult cycle. This has been found to be true for Palaemanetes larvae where the posits of dividing and enlarging cells appear to e constant. Moreover, positional information may be used to determine if a cell is to divide or remain in the non-cycling compartment. Within the mon- olayer some cells will leave the cycling population as growth and morphogenesis proceed, How nutritional state effects the regulation of these events is not understood. GROWTH AND MORPHOGENESIS The crustacean epidermis represents an un- usual example of cell differentiation in that the function of cuticulagenesis is fully developed at hatching but the cells must also form the mor- phologically different regions of the integument. In this process, they will further differentiate to a more specialised type of epidermal cell. Among the specialised cells are setal cells, tendi- MEMOIRS OF THE QUEENSLAND MUSEUM nal cells, transport cells, and, in developing nau- plii of some species, the neuroblast cells (Free- man, 1959a). Each of these cell types begins as a cell in the general larval epithelium. As the tissue grows and develops, the cell changes and differentiates. Following differentiation, the cell may not grow further ar, if it is part of a growing region of the integument, it may continue to divide as the region grows in proportion to other areas of the integument. For many species of crustaceans another dramatic change will occur when the larva undergoes. metamorphosis. In some instances, this change involves only a transformation from a caridoid to a cancroid form. In others, an extreme change takes place, e.g. the barnacle cyprid (Walley, 1969). While a discussion of all of the cellilar and regulatory processes 1s beyond the scope of this review, the process of cell growth is essential to the genera- tion and maintenance of form and shape of the integument and will be discussed here. Crustacean larvae hatch from the eggs at different stages of larval development (William- son, 1982; Gore, 1985). Some may be advanced and undergo little postembryonic development (e.g. Homarus), while others may hatch at the nauplius, the least developed larval form of the Crustacea. At each ecdysis some amount of growth occurs and developmental complexity increases. For the nauplius, this is seen as the process of segmentation in the thorax and abdo- men, while in the zoea it involves development of limbs in segments that are already formed, Morphogenesis in decapod crustaceans, the group for which most studies have been accom- plished, includes continued development of the Ee) 25 220 5. —_+—_ Sie 5 Sil, Day 1 Si. Day 2 Sil Dey 7 instar, Day FIG. 3. Change in density of the epidermal cells in the dorsal carapace of live Palaemonetes pugio during the second instar, The density increased by approxi- mately five cells during the first day of the instar and returned Lo the basal level at ecdysis to instar III. GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE 31 Cell Density ae | ~« hw Fo a uw o a uw Si Dey 7 Sit Cay 2 i+ No-F Si, Oey 1 instar, Day FIG. 4. Change in cell density of the epidermis under different feeding conditions thal are known lo affect the molt increment (Freeman, 1990a), The density at the beginning of the instar was similar for all groups (SII, Day 1). Fed control larvae underwent the nor- mal increase in density by (he end of day 2 (SII, Day 2) while larvae fed only on day 1 (D-1-F) or starved (No-F) showed less growth of the epidermis during the same period, All larvae that moulted to instar TIT demonstrated the same density early on day 1 (SIII, Day 1). indicating that the larvae that were fed only on day 1 or starved grew less during the instar. abdominal segments and thoracic legs (William- son, 1982). The changes are moderate and ex- pand on an already segmented state in which most of the cell types and tissues has been formed. A major transformation ensues al metamorphosis in crabs when the integument changes from a laterally to a dorso-ventrally compressed form. Segment formation in the nauplius of Arremia begins when the pattern of cell replication changes from one that maintains a longitudinal file of epidermal cells to that of a transverse file (Freeman, 1986, 1989a,b). The first transverse file is positioned ventro-laterally in the middle of the presumptive first thoracic segment (Fig. 5). Segmentation proceeds in a anterior-poste- rior gradient beginning al segment 1 (Weisz, 1946, 1947; Anderson, 1967; Benesch, 1969; Freeman, 1989a,b), The maxillae (cephalon) develop at about the same rate as the first two segments. The first major segregation of integu- mental regions is the formation of the arthrodial membrane (AM) and the thoracopod bud. Cells of the limb bud continue to divide transversely at a faster rate than the AM cells until a well defined difference in the cell density is estab- lished early in instar I] (metanauplius 1). This difference in the spatial arrangement of the cells is essential for the evagination process (Free- a) man, 1989b,c). Within two hours of achieving the differential cell density the AM cells change shape and undergo apolysis earlier than the post- erior regions. As a result of the combination of these events the AM region invaginates as the thoracopad bud region evaginates and segment one is defined. Formation of the thoracopod continues over the next several instars. Throughout this period the spatial and temporal manner of the cell rep- lication is important for 1) outward expansion of the bud, 2) growth of the exopodites, endopo- dites, and epipodites, and 3) placement of cells for differentiation (Freeman, unpubl.). Special cell types differentiate during this period. The major tendinal cell forms at the end of instar IT (Fig. 6) while smaller tendinal cells differentiate in concert with the segmental muscles during instars IV, V, and VI (Freeman, 1989a). The neural precursors leave the epithelium during FIG. 5. The pattern of epidermal cell nuclei in the ventral epidermis of fixed instar IT Artemia larvae. Nuclei are stained as described in Figure 2. Anterior is to the top. A longitudinal file is indicated by single arrowhead. The first transverse file of the first seg- ment is indicated by paired arrowheads. (M= mid- line; Seg | = segment 1), Bar =50 um. 316 FIG. 6. The segmenting region of the presumptive thorax of live instar 1] Artemia larvae. The |hora- copod limb bud (ThB) and the arthrodial membrane region (AM) of segment 1 (Seg1) are shown. The tendinal cell (TC) supporis the invaginated AM re- gion, Bar = 50 um. instar [IL or IV and their position within the epidermis may be identified as early as instar II. Finally, the setal cells differentiate during instar V1 as the thoracopod is completed. Thus, growth in crustacean larvae leads not only to increased size at ecdysis, but also to segmental structures. Although numerous papers have described the development of the larval appendages, none have investigated the cellular basis of this development. We must presume that the changes are, in general, similar to the kinds of morpho- genetic changes observed in the thoracopod of brine shrimp, As a comparison, the AM region would correspond to the joints of the limbs and the tendinal and setal cells would develop in conjunction with the muscles and integumental structures, respectively. The control of this process is not understood at this time. The events may be preprogrammed within the developing epidermis, or, alternatively, the cells may be responding to extrinsic elements. Although the pattern of segmental development is relatively constant, there is some plasticity within the epidermis. This is demonstrated by the limb re- generation process in which non-limb epidermal MEMOIRS OF THE QUEENSLAND MUSEUM cells can generate the entire limb within two moult cycles (Adiyodi, 1972), Cellular activities other than growth and differentiation are involved in larval develop- ment and metamorphosis. Programmed cell death occurs in the antennae of barnacle cyprids following attachment and in the spines of crab zoeas during metamorphosis to the megalopa stage (Walley, 1969; Freeman and Costlow, 1983a,b). This cellular state appears to be developed during the larval period and is acti- vated by hormonal mechanisms. Exactly how growth sets the stage for these events is un- known. SUMMARY The integument of the crustacean larva grows and assumes form by a pattern of epidermal cell replication and differentiation that is regulated in a spatial and temporal manner. Growth is inde- pendent of the moult cycle duration and moult- controlling hormones. Nutritional state is a strong determinant of cellular growth. The cells grow to a point that determines the growth poten- tial that is realised at ecdysis when the new cuticle expands. Segmentation and limb forma- tion result from the spatial pattern of cell replica- tion within the epidermis. Future endeavors will explore the basis of the cellular events involved in integumental growth and development and the regulatory mechanisms that are involved in these processes, ACKNOWLEDGEMENTS IT wish to thank Dr R-K. Okazaki for valuable discussions during the preparation of this manu- script, Supported by grant no R11-89961S2 from the National Science Foundation and grant no. HD2421901 from the National Institutes of Health. LITERATURE CITED ADIYODI, R.G, 1972. Wound healing and regenera- tion in the crab Paratelphusa hydromous. Inter- national Review of Cytology 32: 257-289. ANDERSON, D.T. 1967. Larval development and segment formation in the branchiopod crustaceans Limnadia stanlejana (Conchos- traca) and Artemia salina, Australian Journal of Zoology 15: 47-91, ANGER, K. 1984, Influence of starvation on moult cycle and morphogenesis of Hyas araneus GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE larvae (Decapoda. Majidae), Helgolander Meeresuntersuchungen 38: 21-33, 1987, The Da threshold: a critical point in the larval development of decapod crustaceans. Journal of Experimental Marine Biology and Ecology 108: 15-30. ANGER, K. AND DAWIRS, R. 1981. Influence of Starvation on the larval development of Hyas araneus (Decapoda, Majidae), Helgolander Meeresuntersuchungen 34: 287-311, ANGER, K. AND SPINDLER, K.-D, 1987. Energet- ics, moult cycle, and ecdysteroid lilres in spider crab (Hyas araneus) larvae starved after the Dy threshold. Marine Biology 94: 367-375. ANGER, K., DAWIRS, R.R., ANGER V. AND COSTLOW, J.D, 1981. Effects. of carly starva- tion periods on zoval developmentof brachyuran crabs. Biological Bulletin 161: 199-212. ANGER, K., HARMS, J.. MONTU, M. AND BAKKER, C. 1989. Growth and respiration dur- ing the larva) development of a tropical spider crab, Libinia ferreirae (Decapoda: Mayidae). Marine Ecology Progress Series 54; 43-SO, BENESCH, R. 1969, Zur ontogenie und morphologie von Arlemia salina L.. Zoologisches Jahrbucher, Ableilung Anatomie und Ontogenie der Tiere 86: 307-458. BOTSFORD, L.W. 1985. Models of growth. 171- 188. In A.M. Wenner (ed,) ‘Factors in Adult Development’.Crustacean Issues 3. (A.A. Balkema: Boston). BROAD, A.C. 1957a. Larval development of Palae- monetes pugio Holthuis. Biological Bulletin 112; 144-161, 1957b, The relationship between diet and larval development of Palaemonetes. Biological Bul- letin 112: 162-170. CHANG, E.S. 1985. Regulation of moulting in Crustacea, American Zoologist 25: 179-185. CHANG, E.8. AND BRUCE, M.J. 1980, Ecdysternid titers of juvenile lobsters following moult induc- tion. Joumal of Experimental Zoology 214: 157-160, 1981. Eedysteroid titers of larval lobsters. Com- parative Biochemistry and Physiology 7A: 239-241. CHARMANTIER, G., CHARMANTIER-DAURES, M. AND AIKEN, D. E. 1984. Neuroendocrine control of hydromineral regulation in the Amer- ican lobster Homarus americanus H. Milne-Ed- wards, 1837 (Crustacea, Decapoda) 2. Larval and postlarval stages. General and Comparative Endocrinology 54: 20-34, CHRISTIANSEN, M_E. 1988, Hormonal processes in decapod crustacean larvae, 47-68, In A.A, Fin- cham and P:S. Rainbow (eds) “Aspects of de- capod crustacean biology’. Symposium of the Zoological Society of London Number 59. (Clarendon Press: Oxford), COSTLOW, 1.D. 1966a, The effect of eyestalk extir- pation on larval development of the mud crab, Rhithropanopeus harristi (Gould). General and Comparative Endocrinology 7: 255-274. 1966b. The effect of eyestalk extirpation on larval development of the crab, Sesarma reticulatum Say. 209-224, In H, Barnes (ed.) ‘Some contem- porary studies in marine science’. (George Allen and Unwin: London). DEFUR, P.L., MANGUM, C.P. AND MCMAHON, B.R. 1985. Cardiovascular and ventilatory changes during ecdysis in the blue crab Cat- lineetes sapidus Rathbun. Journal of Crustacean Biology 5; 207-215. DRACH, P. 1944. Etude preliminaire sur le cycle d'inlermue et son condilionnement hormonal chez Leander serratus (Pennant). Bulletin Bi- ologique France et Belgium 78: 40-62. FRANK, 1.R., SULKIN §.D. AND MORGAN, R,D 1975, Biochemical changes duting larval development of the xanthid crab Rhithra- panopens harrisii. 1. Protein, total lipid, alkaline phosphatase, and glutamic oxaloacetictransami- nase, Marine Biology 32: 105-111, FREEMAN, J.A. 1986. Epidermal cell proliferation during thoracic development in larvae of Ar- temia. Journal of Crustacean Biology 6: 37-48. 19894. The integument of Artemia during early development. 233-256. In T.H, MacRae, J.C. Bagshaw, and A.H. Warner (eds) ‘Biochemistry and cell biology of Artemia '. (CRC Press: Boca Raton). 1989b. Segment morphogenesis in Artemia larvae. 77-90. In A.A. Warner, T.H. MacRae, and J.C, Bagshaw (eds) “Cell and molecular biology of Artemia development’. (Plenum Press: New York). 1989c, Region-specific mitosis as a morphogenetic force during epithelial evagination in developing Artemia larvae. Journal of Cell Biology [U9: 156a. 19904, Regulation of tissue growth in crustacean larvae by feeding regime. Biological Bulletin 178: 217-221. 19906. Moultincrement, moult cycle duration, and lissue growth in Palaemonetes pugio larvae, Journal af Experimental Marine Biology and Ecology 143: 47-61. FREEMAN, J.A., AND COSTLOW, J.D. 1980. The moult cycle and its hormonal control in Rhiffiro- 41K panopeus harrisii |arvac. Developmental Bi- ology 74: 479-485. 1983a. The cyprid moult cycle and its hormonal control in the barnacle Balanusamphitrite. Jour- nal of Crustacean Biology 3: 173-182. 1983b. Endocrine control of spine epidermis re- sorption during metamorphosis in crab larvae. Roux's Archives of Developmental Biology 192: 362-365, 1984, Endocrine contral of apolysis in Rhithro- panopeus harrisii larvae. Journal of Crustacean Biology 4: 1-6. FREEMAN, J.A., WEST, T.L., AND COSTLOW, LD. 1983. Postlarval growth in juvenile Rhithro- panopeus harrisii. Biological Bulletin 165: 409-415, GORE, R.H, 1985, Moulting and growth in decapod larvae. 1-65. In A.M. Wenner (ed.) ‘Larval growth’. Crustacean Issues 2. (A.A. Balkema: Boston). HALCROW, K. 1978. Cell division in the carapace epidermis of Daphnia magna Straus (Cladocera). Crustaceana 33: 55-63, HARMS, J., MOAL,J., LECOZ, J.R,, DANIEL, J.¥., AND SAMAIN, J.F. 1990. Nucleotide camposi- tion and energy charge in growing and starving zoea I of Carcinus maenas (Decapoda: Por- tunidae). Comparative Biochemistry and Physi- ology 96B; 405—414. HARTNOLL, R.G. 1982. Growth, 111-196, In L.G. Abele (ed.) ‘The biology of Crustacea, Vol. 2, Embryology, morphology. and genetics’. (Acs- demic Press: New York). HARTNOLL, R.G,, AND DALLEY, R, 1981. The control of size variation within instars of a crustacean. Journal of Experimental Marine Bi- ology and Ecology 53: 235-239. KALBER, F.A., AND COSTLOW, J.D. 1966. The ontogeny of osmoregulation and its neu- rosecretory contral in the decapod crustacean, Rhithropanopeus harrisn (Gould), American Zoologist 6; 22|-229, KNOWLTON, R.B. 1974. Larval development processes and controlling factors in decapod Crustacea, with emphasis on Carides. Thallasia Jugoslavica 10: 138-158, LEROUX, A. 1978. Lacrise milotique dans le proven> iricule des zoés | et 1 de Pisidia longicornis (Linné): sa position en fonction des stades du cycle dintermue, Archive de Zoojogie Experi- mentale ef Generale 159: 353-363. LITTLE, G. (969, The larval development of [he shrimp, Palaemon mtacrodactylas Rathbun. reared in the laboratory, and the effects of eve MEMOIRS OF THE QUEENSLAND MUSEUM stalk extirpation on development. Crustaceana 17: 69-87. MANTEL, L.H., AND FARMER, L.L. 1985. Osmotic and ionic regulation, 53-161. In L.H, Mantel (ed.) ‘The biology of Crustacea, Vol. 5’. (Academic Press: New York). MCCONAUGHA, J. 1982. Regulation of crustacean morphogenesis in larvae of the mud crab, Rhi- threpanopeus harrisit. Journal of Experimental Zoology 223; 155-163. 1985, Nutrition and larval growth, 127-154. In A.M.Wenner (ed.) “Larval growth’, Crustacean Issues 2. (A.A. Balkema: Boston). MCCONAUGHA,J.R,, AND COSTLOW, J.D. 1981. Ecdysone regulation of larval crustacean moult- ing. Comparative Biochemistry and Physiology 68A: 9|-93, MURRAY, A.W. AND KIRSCHNER, M.W. 1989. Dominoes and clocks: the union of two views of the cell cycle. Science 246: 614-621, OKAZAKI, R.K., FREEMAN, |.A. AND LAUREN- DEAU, D.M. 1989. Cell growth and cuticle expansion in eyestalk-ablated Palaemonetes. American Zoologist 29; 62A, PARDEE, A.B. 1989. G; events and regulation of cell proliferation. Science 246: 603-608, RICE, A.L. 1968. Growth rules and the larvae of decapod crustaceans. Journal of Natural History 2: 525-530. SKINNER, D.M. 1962, The structure and metabolism of a crustacean imlegumentary issue during a moult cycle. Biological Bulletin 123: 635-647. 1985, Moulting and regeneration, 43-146. In D.E. Bliss and L.H. Mantel (eds) ‘The biology of Crustacea, Vol 9, Integument, pigments, and hormonal processes’, (Academic Press; New York). SNYDER, M.J. AND CHANG, E.S. 1986. Effects af eyestalk ablation on larval moulting rates and morphological development of the American lobster, Homarus americanus. Biological Bul- letin 170: 232-243, SPINDLER, K.-D, AND ANGER. K. 1986, Ecdys- ieroid Jevels during the larval development of uve spider crab fTyas araneus. General and Com- parative Endocrinology 64; 122-128, SULKIN. S.D.,. MORGAN, R.P. AND MINASIAN, L.L. 1975. Biochemical changes during development of the xanthid crab Rhithre- panopens harrisii. IL, Nucleic acids, Marine Bi- ology 32: 113-117. TCHERNIGOVTZEFF, C. 1965. Multiplication cellulaire et regeneration au cours de cycle d‘in- termue des crustacés décapodes. Archives Zoo- logie Experimentale et Generale 106: 377-497. GROWTH AND MORPHOGENESIS IN CRUSTACEAN LARVAE WALLEY, L.J. 1969. Studies on the larval structure and metamorphosis of Balanus balanoides (L.). Philosophical Transactions of the Royal Society of London (B) 256: 237-280. WEISZ, P.B. 1946. The space-time pattern of segment formation in Artemia salina, Biological Bulletin 91: 119-140. 1947. The histochemical pattern of metameric development in Artemia salina. Journal of Mor- phology 81: 45-89. WEST, T.L. AND COSTLOW, J.D. 1987. Size regu- lation in larvae of the crustacean Balanus ebur- 319 neus (Cirripedia: Thoracica). Marine Biology 96: 47-58. 1988. Determinants of the larval moulting pattern of the crustacean Balanus eburneus Gould (Cir- tipedia: Thoracica). Journal of Experimental Zoology 248: 33-44. WILLIAMSON, D.I. 1982. Larval morphology and diversity. 43-110. In L.G. Abele (ed.) ‘The bi- ology of Crustacea, Vol. 2, Embryology, mor- phology and genetics’. (Academic Press: New York). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM FEEDING AND GROWTH IN MERO.- PLANKTONIC LARVAE OF CALLINECTES SAPIDUS (CRUSTACEA: PORTUNIDAE) Capiure of sufficient qumbers af quality prey to meet the demands of metabolism and growth is w major factor in determining larval survival and recruitment success, Caplure of prey is a function of prey demsily, predator and prey swimming speeds, and handling time. Handling time is re- lated to prey type, size, und natural defences, Feeding rates were determined for the larvil stages of the portumid crab, Callinectes sapidus, using Jaboratory and natural prey. Feeds ing was examined in both light and dark Using laboraiory determined values for energy efficiencies the proportion of daily standard metabolism and growth was determined. Materials and Methods Ovigerous C. supidus were collected from the Chesapeake Bay. Upon hatching, the zova were raised in 1000 mi culture bowls and ted with a diet of 15 000 Branchianus plicatus/l, and S000 Artemia salina/L, The zoea were transferred inta tresh seawater and fed diily. Prey were counted and placed inl 500 ml battles vontain- ing 200 ml of seawater with three replicates of cach enneen- tration of prey. A single replicate. without a zoea was used as a control. Prey included A, saline, (5, 25, 50, 100/L), B. plicatus (25,50, 125, 250/L), and Acartia tonsa (25, 50, 125/L). Zoea of the appropriate stage Were added and the bottles incubated at 25°C. After 10-12 hours illumination each zoea was transferred to a new bottle with the same concentrations of prey and incubated at 25°C in the dark. After cach segment of (he experiment the contents of each bottle were preserved and the remaining prey enumerated, Wild C sapiduy megalopae were collected from plankton samples onboard the NOAA R/V Albatross 1V. Prey items Were sorted from additional plankton samples and identified tw species and developmental stages. Shipbourd feeding siu- dies range in duration from 7-9 hours, Feeding Experiments When fed a combination of rotifers and Artemia nauplii, first und second stage larvae fed exclusively on rotifers. Visual observations suggest that the size of Arfemia nauplii was the selection criteria, Ingestion of rotifers increased al the second stage und remained relatively stable through the Mmegalopae stage. Third stage zoea occasionally capiured Artemia nauplii, (here was A significant increase in ingestion rates of Artemia by the fourth through sixth stage zoeac, A second increase ducing the last zoeal and the megalopa stage TABLE 1, Dally ingestion of Acartia tansa Stage | nauplii by C. sapidus larvae. 49° 3.8 63 85 14. 19.6 %Std Metabolism 1 — 50% = Std > 100%, 2 — 25% > Std >S0%b, 3 — Side< 25% all others > 100% Std. 320 was also evident, Total carbon ingested was low Uhrougl zoeal slage 3 then incregsed in parallel with the increase in ingestion of Artemia nauplii. Our original hypothesis was thal small prey would be dropped from (he diet or be captured in reduced number by late stage larvae due lo handling costs. These data indicate thatsmall prey contribute to the enenget- ics of all stages, Consumption of A, fonsa nauplii was sulli- cient 10 meer 25-100% of energy needs for zoeal slapes 1-6, but fess than 50% of the nevds of megalopye (Table 1) Wild megalopae fed the sixth copepodite stage of Acartia tonsa demonstrated a linege increase in feeding with concen- tration, In contrast, consumption of mate and female Cen- tropages: humeatuy displayed a sharp plateau at 25/L. Consumption of C. Aamegrus nauplii (1, 1) plateaued at 50 10 JO0/L, Megalopae fed cladocerns, Penilla and Evadne, displayed 4 linéar increase in feeding through the highest concentrations tested (100/L). Consumption of Uca sp. zova plateaued ar 25/1, The observed feeding rates are un- doubledly a function of prey size, handling time, and satia- tion. Based on the model of Gerritsen and Strickler (1979) larger prey were encountered, and captured less frequently. Handling time jncreuses with size and natural defenses, 1.c. spines. of Uca 20ea. Smaller first stage C. sapidus zoea with shotier spines are readily consumed by C, sapidus mega- lopae, Diarnal Feeding Patterns All zocal stages led at higher rales at night. Sulkin ee al. (1979) demonstrated that swimming speeds of C, sapidus larvae followed a diurnal pattern with up to 60% increased swimming speeds at night. Based on the Gerritsen and Strick- ler (1979) model increased nighttime feeding can be ex- pluined by changes in swimming speed. Actual feeding rates for various concentrations of prey were equal 10 or less than predicted values. Lower observed rales may reflect prey handling \ime, Megalopae fed at higher rates during daylight hours when offered small prey (rotifers and.A, tonsa nauplii). No difference in feeding rate was noted when large prey. (Artemia nauplii) were offered, Calculation of Manly's (1974) B index for prey selection indicates that megalopae weakly select for Artemia nauplii during daylight hours. Selection for Artemia nauplii was enhanced at night. These data suggest that megalopae can consume small prey bul rely More on visual prey identification than zoeal stages. Literature Cited Gerritsen, J. and Strickler, J.R. 1977. Encounter probabilities and community structure in Zooplankton: a mathemati- cal model, Journal Fisheries Research Board Canada 34: 73-82, Manly, B.4.F, 1974. A model for certain lypes of selection experiments, Biometrics 30: 281-294, Sulkin, S.D., Phillips, 1.and Van Heuklem, W, 1979, On ihe locomotory rhythm of brachyuran crab larvae und its significance in vertical migration, Marine Ecology Pro- gross Series 1: 331-335. J,R, McConaugha, P.A. Tester, and C.S. McConaugha, Department of Oceanography Old Dominion University, Norfolk, VA, National Marine Fisheries Service, Beaufort, NC, USA, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ECOLOGICAL PHYSIOLOGY OF LARVAL EUPHAUSODS, EUPHAUSIA SUPERBA (EUPHAUSIACEA) ROBIN M, ROSS AND LANGDON B. QUETIN Ross, R.M. and Quetin, L.B. 1991 09 (1: Ecological physiology of larval euphausiids, Euphausia superba (Euphausiacea), Memoirs of the Queensland Museum 31: 321-333. Brisbane. ISSN 0079-8835. Studies of the effects of environmental variability on the physiology of the early life history stages of the Antarctic krill, Euphausia superba, suggest that there are several critical periods during the first year of life that will affect survival, and thus recruitment of young krill into the adult population. The tirst cntical period occurs during development of the non-lfeeding stages. Results of a collaborative modelling study suggest that release of embryos over warm deep water (250-400 m) is advantageous for these early larval stages. The geographical distribution of spawning populations combined with the observed pallern in sinking rales of embryvs during development form a reproductive siralegy that maxi- mises survival of the early non-feeding stages. The first winter is the second critical period. Physiological condition (condition factor, lipid content, and growth rate) of Jarvae and juveniles is an index of their nutritional history and ability to survive and enter the adult population the fallowing summer. Significant differences were found in the physiological condition of larvae collected during two winters which differed primarily in the degree af ice cover. Larvae in the heavy ice winter had higher growth rales, higher condition factor and more lipid, Although phytoplankton in the water column were scarce in both winters, ice biota Were.an additional possible source of (ood during the heavy ice winter.) Larval euphausiids, reproductive strategy, recruitment, physiological condition, critical period. Robin M, Ross and Langdon B. Quetin, Marine Science Institute, University of California at Santa Barbara, Santa Barbara, California 93106, USA; 71 February, 199). The most abundant euphausiid in the world’s oceans, Euphausia superba Dana, the Antarctic krill, lives only in the Southem Ocean. This one species is often the dominant herbivore, unlike the case in most other oceans where copepods. are the important grazers of phytoplankton primary production (Clarke,1985). Although Antarctic krill have a ¢circumpolar distribution, high concentrations are found in only a few locations (Marr,1962; Laws, 985). Because krill are concentrated within the area of strong seasonal variation in pack ice cover, many investigators have postulated a close coupling between sea ice and krill populations due to associated food sources (Laws,1985; Quetin and Ross,1991). Sea ice provides a habitat in which microscopic plants and animals can live and grow, la addition fresh water from melting sea ice in the Spring promotes water column stability and ice-edge blooms of phytoplankton several months before the open water blooms (Smith er al., 1988). The annual advance and retreat of sea ice involves about 16 million km? of ocean surface, advancing from a minimum of 4 million km” insummertoa maximum of more than 20 million km in late winter (Garson and Siniff, 1986), Growth and reprodiictive cycles. of krill are keyed to the extreme seasonal cycle of primary production in the Antarctic caused by lack of light in the fall and winter (Quetin and Ross, 1991). Phytaplankton concentrations in the water column are also very low during these periods (0.1 to 0.2 ag chl a I! (Ross et al., 1987: McClatchie, 1988)). Krill are long-lived for a pelagic crustacean, with an estimated maximum life span of seven or eight years (Ettershank, 1984; Siegel, 1987: Berman e/ a/., 1989). They probably begin to reproduce in their third summer. Although the ovary begins to mature in September and October, embryos are not released until the summer months, unlike most other Antarctic zooplankton that spawn in the iri E. superba releases multiple batches of embryos throughout the spawning season if food supplies are sufficient (Ross and Qucetin, 1983, 1986; Cuzin-Roudy, 1987), Spawning intensity will thus depend on regional environmental conditions. Once released, krill embryos sink rapidly out of the surface layers, hatching at 600 to 1000 m after 4.5 to 6 days (Marschall and Hirche, 1984; Quetin and Rass, 1984; Ross and Quetin, 1985). The newly hatched larvae then begin their ascent to the surface. The nonfeeding naupliar stages are usually found below 250 m, but Calyptopis 1 (C1), the first la tt nm larval stage with a mouth and feeding appendages, are usually found in the lighted surface layer with their food source — phytoplankton (Marschall, 1985), Embryos released in mid- to late December appear in the surface layers as Calyptopis | in early to mid-January, about the same time as the summer phytoplankton bloom, Thus, production of embryos and larvae is timed so Cls usually encounter food once they arrive al the surface, Larval developmental times through the three calyptopis and six furcilia stages depend on temperature and food availability, Estimates range from four months with excess food (Ikeda, 1985) to IO-L| months (mid-November) under winter conditions of tow food and temperatures (Ross ef al, 1987; Elias, 1990). Euphausia superba is a* keystone’ species in the Antarctic food web, Because of their high biomass and long life span, Antarctic krill provides a year-round food source. In fact they are often the primary food source for predators in this ceosystem (Laws, 1985). Turnover rales and recruitment success of E, superhe are of particular mterest because of its integral role in the dynamics of the Antarctic ecosystem and the possible impact of the commercial fishery for krill, Fisheries researchers have long recognised that there ure periods during early larval life that are critical (o survival and to the recruitment success or failure of the year class (Hjort, 1914; May, 1974}. More recently the same concept has been applicd to crustacean larvae (Anger and Dawirs, 1981; Dawirs, 1987; Ross and Quetin, 1989). Tdentification of these critical periods and the possible consequences will allow us lo predict vanability m recruitment success from pertinent environmental factors. In this paper we describe recent research that focuses on several factors that influence inter-annual variability in recruitment success of E, superba. By recruitment we mean the abundance of the age class 1+, the youngest subadults, at the beginning of their second summer. Clearly both teproxiuctive output of adults, termed “recrutiment potential’, and survival of the embryos and larvae impact the size of the year class, and are (he sources of annual and peographical variability in recruitment, We will focus on two studits relevimt lo jhe success of early life history stages, Each study identifies one critical period in the first year of life. The approaches used avoid several of the logrstical und theoretical problems inherent in sampling a mobile species with an ocean-wide and patchy distriburion (Hamner e¢ MEMOIRS OF THE QUEENSLAND MUSEUM al., 1983, 1984; Kanda et al, 1982), These approaches yield valuable insight into recruitment dynamics and population maintenance, and are valuable techniques for those wishing to understand processes underlying variability in recruitment of other pelagic crustaceans. The first study is a coupled biological/physical model that integrates laboratory measurements of the physiology and behaviour of the embryos and non-feeding larval stages and the actual vertical temperature structure of the waters near the Antarctic Peninsula (Hofmann er al., in press), The objective was to simulate the descent/ascent cycle under different environmental conditions to explore questions about the relative success of spawning in different hydrographic regimes, The second study documents the effects of inter-annual variabjlity in winter conditions on the physiological condition and thus survival of larvae and juveniles during their first winter (Quetin efal,, in press). Results from these two studies have helped us understand how environmental variability can Icad to success or failure of a year class in E, superba, DESCENT/ASCENT MODEL OF EARLY LIFE HISTORY The first critical period in FE. superba's life history occurs during the descenl/ascem cycle immediately after release of the embryo, Because the embryos and early larvae depend solely on internal reserves until C1 (Quetin and Ross, 1989) the reserves remaining at metamorphosis to Cl is a function of environmental temperature an! its effect on metabolism and development. From our laboratory studies of starvation tolerance during this first feeding stage, we know that the point-of-no-return (PNR) runges from 10 lo 14 days (Ross and Quctin, 1989). After the PNR, even if food does become available, larvae are Unable to recover from the effects of prolonged starvation. They fail to develop normally and eventually die, Thus the level of initial reserves, how fast they are used, and whether food is available shortly after the Cl reaches the surface determine larval success in this first critical period. TIME ANT TEMPERATURF-DEPFNDENT MODFL A time- and temperature-dependent model (Hofmann et al, in press) was developed to answer several questions relevant to the use of internal reserves in the embryos and early larvae: (1) how do water mass characteristics affect the use of reserves?, (2) whaLare the hatching depths PHYSIOLOGY OF LARVAL EUPHAUSIIDS and thus the depth from which the larvae have ta ascend?, and (3) what reserves are still available when the larvae reach the surface? The model simulates the descent/ascent physiology and behaviour of embryo and early larval stages under different hydrographic conditions. Development and definition of parameters of the model included careful consideration of the biology and physiology of the embryos and larvae of FE, superba. Temperature affects developmental and metabolic rates (Ross er al., 1988; Quetin and Ross, 1989), and also has a direct effect on the survival of the carly life history stages. Embryos and larvae reared al -1°C do not continue development past the C1 stage (Ross e/ a/., 1988). We suggest that there may be & temperalure sensilive period a{ some point during early development, and that a necessary developmental process does not take place at negative temperatures. Older stages survive and grow at these low temperatures, so we believe that it is only very early in development that exposure to low temperatures has deleterious effects. We also incorporated the cffects of lemperature and developmental stage on larval ascent rates (Ross et al., 1985). Because sinking rates of the embryos are critical to hatching depths, one important aspect of the model was to simulate the sinking rale pattern of the embryos during development (Quetin and Ross, 1984; Ross and Quetin, 1985), Changes abserved in sinking rales imply changes in the density of the embryo during development, Initially embryos sink rapidly, 175 to 200m d’! After about 24 h, however, sinking rales decrease to 50 to 60 m d'. Just prior to hatching, sinking tates increase to near initial yates. The sinking rate pattern was clear. What was nol clear was whether jhis pattem was important in the life cycle of Antarctic krill, and what, if any advantages suche pattern would confer on the species, High initial velocities serve to remove embryos from schools of feeding adult krill, a probable predator, but the advantages of the subsequent decrease in sinking Tales were nol appirent, With the model we derived depth profiles of the embryo and larva, and ealculuted the decrease in carbon during development under different temperature regimes. The simulated descentund ascent patterns are primarily a result of the effect of temperature on the developmental times of early life history stages. Development in &. superba ts equiptoportianal, 1.@, cach developmental stage occupies the same proportionate amount of time relative to other 323 stages at any constant temperature (Ross ef al... 1988). Because development in Antarctic krill is equiproportional, the biological processes included in the model are formulated in terms of fraction of total developmental time (Hofmann et al., in press), SIMULATIONS Simulations of the descent/ascent cycle were tun for constant temperatures and for actual vertical profiles from the waters. west of the Antarctic Peninsula, particularly at locations around the South Shetland Islands and in the Bransfield Strait (Hofmann ef al., in press), In some parts of This region Warm Circumpolar Deep Water (CDW), warmer than 0°C, is found between 200 and 600 m (Fig. 1). Except for seasonal warming of the surface waters, waters above and belaw the CDW are less than O°C, Simulations with constant lemperatures show the role of temperature in determining the depth of hatching and the total time for the descent/ascent cycle (Hofmann ez al., in press). Longer developmental times affect the total sinking period and the time at high sinking rates, In addition, larvae swim more slowly at colder temperatures and have to ascend from deeper water, increasing the use of energy reserves before reaching the surface, Over deep cold water embryos hatch at depths >L000 m, and metamorphose to Cl] within the lighted surface layer. At warmer temperatures krill larvae reach the surtace well before metamorphosis into the first feeding stage, so have a longer time at the surface to find food betore passing the PNR. However, even at -1°C less than 20% of the total carbon was used during the descent/ascent cyclo (Hofmann er a/., in press), far less than jhe 50% level for the PNR (Ross and Ouetin, 1989)_ The simulations show thal under no conditiuns do larvae pass the PNR belore reaching the surface. However, if the underlying water is cold, Jarvae arrive at the surface with less time before they need to feed, Simulations of the descent/ascent cycle with observed vertical temperature structures emphasised che role of temperature in controlling the hatching depth, the time spent on the bottom before hatching. and the amount of carbor used during the cycle (Hofmann er al. in press). In regions characterised by warm CDW at depth, such as north of the South Shetland Islands where water warmer than (°C is found at all depths greater than 130 m, embryus arrive in walters greater than °C about 1.5 d alter release. 324 60°S 61° Drake Passage 62° 63° Bellingshausen Sea 64° Anvers |s.f 65° 67°W 65° 63° 61° MEMOIRS OF THE QUEENSLAND MUSEUM / Bet George Is. ~ Ke" _ King! /, Weddell Sea 59° 57° 55° 53 FIG. 1. Composite temperature distribution at 500 m in area of study, The distributions were construcied using historical temperature data collected during the last ten years from XBT and CTD observations. Contour interval is 0.5°C, Dashed lines indicate extrapolation of the temperature (data from Hofmann ef al., in press). Distributions of krill schools in 1982 containing gravid (4 ) and nonreproducing females ( A) are plotted (Quetin and Ross, 1984). Because sinking rates are very low during the few days, embryos remain in this CDW until hatching, about 5 d after release and at 680 m (Fig. 2a). In the eastern Bransfield Strait, waters are less than -1°C at all depths. Hatching time is almost 10 days. Slower developmental times mean that the period of high initial sinking rates lasts longer, and embryos reach about 500 m before slowing down, Embryos hit bottom at 1000 m 2 days before hatching, and about 20% of embryonic development occurs on the bottom (Fig. 2b). In contrast embryos released north of the Shetland Islands hatch before they reach bottom. North of the South Shetland Islands, larvae complete their ascent in about 13 days, bringing the total descent/ascent cycle to 18 days. Total carbon use is about 2 1g C, 13% of initial values (Fig. 2c). Ascent rates in the eastern Bransfield Strait, however, are slower so larvae take about 25 days to complete the ascent, for a total descent/ascent time of 35 days, about twice as long as in the area north of the South Shetland Islands (Fig. 2d), Total carbon use throughout the descent/ascent cycle is about 26% of the initial carbon content of the embryo, again twice as much as for the area over CDW. This carbon usage brings the larvae much closer to the PNR of 7.5 ug C, or a 50% decrease, and gives the larvae fewer days in which to find food. These simulations show firstly that embryos PHYSIOLOGY OF LARVAL EUPHAUSIIDS 400 Depth (m) o 3 rx) Carbon (11g) 800 0 2 4 6 8 10 Time (d) T°C 400 -_ DB E = Pi cl Cc € 600 8 oO _ a é 800 eGG eLB ILB 0 z 4 6 8 10 Time (d) 200 5 15 25 35 Time (d) 325 T°C x en est 0 1 2 $ x6 200 15 400 ' 14 a 1 SB —E I 2 ! c = 600 I 13.6 ra ' 8 I () 800 12 1000 11 1 10 oad 5 15 25 35 Time (d) TC Carbon (ig) FIG. 2. Simulation of descent/ascent cycle of the embryos and larvae of Euphausia superba with vertical temperature structures typical of the region west of the Antarctic Peninsula and north of Anvers Island: temperature profile (dashed line), depth profile (solid line) and carbon content (dotted line) of the embryo or larva. a, descent of embryo, north of King George Island (60.8°S, 58.5°W). b, descent of embryo, eastern Bransfield Strait (63.5°S, 61.4°W). c, ascent of larva, north of King George Island (60.8°S, 58.5°W). d, ascent of larva, eastern Bransfield Strait (63.5°S, 61.4°W). (SC= single cell; eG= early gastrula; G= gastrula; eLB= early limb bud; ILB= late limb bud; H= hatch; N= nauplii; M= metanauplii) (from Hofmann etal., in press). 326 developing at cold temperatures may spend some of their developmental time on the bottom, where they may be eaten by benthic animals or buried in sediment. Secondly, that larvae which complete the descent/ascent cycle at cald temperatures have less time after reaching the surface to find food before passing the PNR. And lastly, that most of early development in these regions with no CDW takes place at negative temperatures, so the probability is high that the early stages. have been exposed to cold temperatures during the temperature sensitive period, and will never develop past C1. Embryos released in regions with CDW at depth will thus encounter more favourable conditions for continued development and maximising the reserves available after teaching the surface. REPRODUCTIVE STRATEGY Several investigators have suggested that Waters over the continental slope, and not shallow waters, are favourable spawning areas because early larval ‘stages are regularly abundant on the continental slope and not on the shelf (Ichii, 1990). In addition gravid females are generally found in areas along the continental slope of the Antarctic Peninsula with high chlorophyll a concentrations (Quetin and Ross, 1984b; Endo ef al., 1986; Siegel, 1988; Capellaeral., in press), The energetic requirements of spawning suggest that food availability is a limiting factor for reproduction (Ross and Quetin, 1986) so the co-occurrence of spawning populations and high food concentralions is Hot surpnsing, Since the spawning distribution of £, superba is spatially restricted relative to the distribution of the species, and the distribution of adult krill changes scasonally (Siegel, 1988), the question ariscs as 19 whether this spawning distribution is defined by fiydrographic conditions as is true of many fishes (Sinckair, 1948). Siegel (1988) suggested that adull Krill might actively migrate during summer into offshore waters. and back into shelf waters in the fall, Siegel speculated that this horizontal migration might reduce intraspeerfie food competitron between adults and larvae. The results of the tinve~ and temperature dependent model of the descent-ascent cycle provide an alternate hypothesis: spawning in regions with CDW al depth confers a reproductive advaniage on the population and is thus part of a reproductive Stralegy. In our study region west of the Antarctic Peninsula and northeast of Anvers Island, most schools of reproducing fernales are associated with MEMOIRS OF THE QUEENSLAND MUSEUM CDW (Fig. | for 1951-82 season; Capella et al, in press). Selection of particular waters by spawning krill cannot be thought of as fortuitous, particularly as the presence of mature ferales in continental slope waters oyer CD'W appears to involve a Seasonal horizontal migration. We suggest that a reproductive strategy has evolved in krill in response to its environment that is composed of at least two elements: ihe sinking rale pattern of the embryos, and the specific geographic pattern in population structure. Fisheries scientists first recognised that reproductive strategies, including restricted spawning locations and honzontal migrations, play a definite role in population maintenance and persistence of a species in the late 18{K)s (Sinclair, 1988), Recently, these restricted distributions have been perceived in several groups of fishes as interactions between reproductive strategies and oceanographic conditions (Parrish er al, 1981; Sherman etal, 1986). The general concept is that the life cyele and structure of the population has evolved in response to specific oceanographic or spatial conditions to take advantage of features in the environment thal enhance the survival of the early life history stages (Sinclair, 1988). In the case of E. superba, the hypothesised reproductive strategy confers three advantages. (1) the depth of hatching and time on the bottom is minimised; (2) carbon use before metamorphosis into C148 minimised, with obvious advantages in increasing the time before passing the PNR: and (3) the embryo and carly larvae spend a minimal time in sub-zero waters, where they may be exposed lv very cold temperatures during the postulated tenyperarure sensitive period, Recruitment might be affected in several Ways if embryos are not released above CDW, as may happen in years when changes in circulation patterns shift the surface distributions of adult krill in summer away from CDW (Capella er al,. in press). Mortality of both the larvae and embryos will be increased, because of the temperature sensitive period, deep hatching depths, and preter use of energy reserves. Those larvae that do reach the surface will be less tolerant of subsequent periods of low food availability, Tn 1983-84 krill biomass in the study region (Fig. 1) was very low, as documented by the many researchers involved in SIBEX [Second International BIOMASS are pg This low hiomuss has been altributed to large scale population displacement due to hydrographic changes, and nat to severe mortality in the adult population of ta poor recruitment several years previously (Priddle er a/., 1988). The one area PHYSIOLOGY OF LARVAL EUPHAUSIIDS 427 where gravid females were consistently found was the Gerlache Strait (Capella era/., in press). In this year when gravid females were few relative to other years, and not found in the traditional spawning locations over continental slopes and CDW, spawning success as judged by the abundance of the early life history stages was poor (Witek and Kittel, 1985). PHYSIOLOGICAL CONDITION DURING THE FIRST WINTER The second critical perind is during the first winter, when larvae must survive a six-month period of very low food availability in the water column after a brief summer in which to build up energy reserves. Three lines of evidence suggest that low fond conditions in the winter may present difficulties for the young-ol-the-year who winter over primarily as late furcilia stages or carly juveniles (Guzman, 1983; Ross et al., 1987), First, unlike the adults who satisfy a significant portion of their winter energetic requirements with their lipid reserves (Quetin and Ross, 1991), the small amount of lipid accumulated by the larvae is not enough to contribute significantly to energetic requirements. In the fall about 2% of the wet weight of furcilia 6 and juvenile krill is lipid, compared to 6-8% for adults (Quetin and Ross, 1991; unpubl.). Second, furcilia do not have the same starvation capabilities as adults, supporting the evidence of low lipid reserves, Elias (1990) found that the mean survival time of late furcilia under starvation conditions varied with the age of the laryae (Table 1), The older larvae survived longer than younger larvae, but no stage could survive a winter with no food, unlike adults that can starve at least as long as 211 days (Ikeda and Dixon, 1982), Third, when furcilia larvae ure maintained at food concentrations representative of the range of winter chlorophyll a concentrations in the water column west of the Antarctic Peninsula, larvae at the minimum concentrations (0.09 wg chi a L’) tured to cannibalism while larvae al maximum concentrations (0.28 pg chl a L ) did not (Elias, 1990). The lowest food concentrations appear to have triggered a change in nutritional mode, whether due to a change in behaviour of the larvae or a growing inability of the larvae to escape predation. In the field, however. cannibalism is less likely to occur than in the confined experimental vessels in the laboratory, and larvae may need to find other food sources. These results all suggest that if phytoplankton is the only food source, larvae and early juvenile krill wil! not TARLE |, Starvation tolerance of late furcilia stages ol Euphausia superba, Larvae were collected in April, and kept at ambient food and temperatare for 2.2 ments. In July individuals were isolated and main(ained im filtered seawater until they died (Elias, 1990), Stage at Colleetran Mean Survival Time (Days) Fureilia 4 29 Fureilia 5 59 Fureilia 6 64 be able lo meel their energetic requirements in open waier in the winter when phytoplankton Ievels. are af or near winter minimum concentrations. Their continued development during the winter in the field, inability to tolerate long periods of starvation, and lack of lipid reserves all suggest that larvae need to feed in winter and must utilise a food source other than the phytoplankton in the water column. Many have speculated about the role of ice and the ice-biota in the winter-over existence of E. superba (references in Quetin and Ross, 1991), But quantitative estimates of the importance of the sea ice as either a food source or a refuce from predation, and its impact on recruitment are lacking. We do know, however, that larvae and juveniles feed on the under side of the ice in areas of annual or smooth ice both winter and spring (Guzman, 1983; Kottmeier and Sullivan, 1987; Quetin and Rass, 1988; Daly and Macaulay, 1988; Marschall, 1988). ff larval and juvenile krill are dependent on ice-biota in the winter, then their ability to survive the winter in good condition is indirectly dependent on the timing and extent of pack ice development during the winter. We hypothesise that the condition of the Jarval and juvenile krill and their winter over survival will be higher in years of greater pack ice when food availability is also greater. Inter-annual variation in the maximum extent of pack ice in the winter 1s substantial (Zwally erat, 1983; Smith eral, 1988), and can be dramatic in the region west of the Antarctic Peninsula (Quetin and Koss, 1991), Timing is also variable. In some years pack ice is present by July, bul in others nor until late August, These inter-annual variations im pack ice extent allow us to test predictions based on our hypothesis. The impact of the first winter on recruitment of any one year class into the subadult population will depend on mortality due lo either physiological factors or predation. Although quantifying winter-over 328 survival or recruitment into the subadult population is difficult, we can quantify the physiological parameters that affect survival probabilities. If predation on these young-of-the-year is low, physiological condition and survival should depend on many of the same environmental factors and be well correlated. Because most known predators select the larger size fraction of krill, predation pressure on the furcilia and juveniles will be low (Croxall et al., 1988; Lowry et al., 1988). PHYSIOLOGICAL CONDITION We define physiological condition as a group of three measurements that depend on the nutritional history of the larva: instantaneous growth rate, condition factor, and lipid content (Quetin et al., in press). Instantaneous growth rate experiments are conducted on board ship for four days immediately after collection (Quetin and Ross, 1991). The brevity of the experiment ensures that these growth rates reflect the immediate previous nutritional history, and are not a laboratory artifact. Condition factor, a measure of organic matter per unit body volume, is more frequently used as an index of nutritional history for fish (Ehrlich et a/., 1976), but has occasionally been used for pelagic crustaceans (Omori, 1970; Durbin and Durbin, 1978). Condition factor (ug carbon per length cubed) is higher under better nutritional conditions. Lipid is commonly used by crustaceans as an energy reserve. Both condition factor and total lipid reflect longer term nutritional history than growth rate. These factors allow us to evaluate the relative 50 40 30 Frequency (%) 10 -10 5 % Growth / IMP FIG, 3. Distribution of growth increments per inter- molt of larvae of Euphausia superba in the winters of 1987 (flecked), with heavy pack ice, and 1989 (no fill), with light pack ice. The vertical line is the no-growth line. MEMOIRS OF THE QUEENSLAND MUSEUM ‘fitness’ of the larvae in the field and to distinguish good years from bad. Physiological condition of larval krill from the region west of the Antarctic Peninsula was measured in two winters that differed greatly in pack ice extent (Quetin et al., in press). Pack ice was heavy in the winter of 1987 (9/10 and 10/10 over most of the region), but nearly non-existent in 1989 (Quetin and Ross, 1991). Other possible significant environmental variables were similar in the two years. Chlorophyll a concentrations in the water column were about 0.10 ug chl aL"! in both years, but temperatures were slightly lower in the heavy ice year (-1.6 to -1.8°C versus -0.2 to -1.8°C). Larval krill were collected from open water with paired meter nets on a bongo frame with 505 um mesh, and by divers from under the ice when ice was present. Stages collected ranged from furcilia 3 to 6 to small juvenile young-of-the-year. Growth rates were positive in the heavy ice year, but negative in the light ice year (Fig. 3) (Quetin et al., in press). Growth was 5.43 % per intermoult period in the heavy ice year (n = 21, SD = 4.95, 5 experiments), and -3.42% per intermoult period in the light ice year (n = 8, SD = 3.45, 3 experiments). Intermoult periods in the winter of light ice were twice those during the winter of heavy ice. Although these longer intermoult periods minimised actual shrinkage per day, growth rates were still zero or negative in winters of low ice. Condition factor and lipid content were both significantly higher for all larval stages collected during the heavy ice year than during the light ice year (Fig. 4) (Quetin ef al., in press). The differences were greater for lipid than for condition factor. Total lipid in larvae from the light ice year was only about half that in the heavy ice year, whereas condition factors differed by about 20%. Thus in the winter of heavy pack ice larvae were in better physiological condition: they were growing, and contained more organic matter per volume and more lipid, some of which could presumably be used to meet energetic demands. Shrinkage, and use of lipid and body protein are all mechanisms used by adult krill to survive a winter of low food availability (Quetin and Ross, 1991). In the light ice year larvae appear to be using some of the same mechanisms to supply their energetic requirements as adults do in all years. However, we know that larvae cannot survive starvation for as long as adults. If very low food concentrations continue for the entire winter, the PHYSIOLOGY OF LARVAL EUPHAUSIIDS larvae will continue to deplete their body lipid and protein, and may pass the PNR. Once past the PNR these larvae will not recruit into the juvenile and subadult population in the late spring and early summer. Although the mechanisms underlying these correlations ate still largely unknown, the difference in physiological condition in larvae from a heavy and a light ice winter suggests that enhancement of winter-over survival is mediated by the presence of pack ice. The most probable cause is the presence of an alternate food source which allows the young-of-the-year to continue to grow and develop throughout the winter without using their body reserves to meet energetic requirements. INTER-ANNUAL VARIABILITY IN RE- CRUITMENT Variability in recruitment of a zooplankton population in any one region is caused by a number of factors. The abundance of any one year class is dependent on both the number of embryos actually released and how many of those embryos survive the first year. Spawning intensity in the region varies with the number of reproducing females and the number of embryos each produces. Thus spawning intensity in E. superba will depend not only on large scale hydrographic changes that cause regional changes in population structure (Priddle e/ al., 1988), but also the amount and timing of food availability (Rass and Quetin, 1986). We will term this factor in the recruitment equation ‘recruitment potential’. Mortality of the young-of-the-year is the other major factor. There is evidence for significant inter-annual variability in ‘recruitment potential’ of E, superba in the region west of the Antarctic Peninsula and north of Anvers Island, Brinton er al. (1986, 1987) reviewed available information on early larval and gravid female abundance and distribution, and suggested that eight of the twelve years fram 1965 {o 1984 for which we have information have been successful spawning years for &. superba. In the years with poor ‘recruitment potential’ onc or more of the following was observed: gravid females Were rare in the area (1982-83; 1983-84): spawning, was delayed (1977-78; 1983-84); or larval development was retarded (1966-67). Larval abundance in one of the ‘successful’ years during this period (1980-81) was much greater than in either 1983-84 (Brinton ev al., 1987) or 1976 or 1978 (Hempel, 1985). The 1980-81 year w tt P= 1a) Condition Factor (ug C/mm 4) (b) Total Lipid (ug per larva) Larval Siage FIG, 4, Condition of the three late furcilia stages of Euphausia superba in the winters of 1987 (solid), with heavy pack ice, and 1989 (flecked), with Yjght pack ice. a, condition facior in ug carbon mm~. b, total lipid in wg larva . Lipid content of a group of 5 to 8 individuals of the same stage was determined with a charring technique (Marsh and Weinstein, 1966). Error bars represent standard deviations. Numbers in bars are numbers of individuals for condition factor or number of samples of groups of five to eight of the same stage for total lipid. of high ‘recruitment potential’ followed acold winter, as evidenced by extremely cold air temperatures in this region (Rakusa-Suszezewski, 1955) and heavy winter pack ice in the Weddell sector (Zwally et al., 1983) (Fig. 5), The poor ‘recruitment potential’ years appear to coincide or lag one year behind El Nino Souther Oscillation (ENSO) events (1965-6; 1972-73; 1976-77; 1982-83 (Sahrhage, 1988)) and occur after warmer winters. 33) Evidence for interannual variability In mortality of the later larval stages is scarce. With a Jong-lived species such as £. superba, only when recruitment fails in several years in succession will we be able to detect differences in absolute abundance (Priddle ez a/,, 1988), However, age-specific differences in mortality rates will lead to predictable changes in length-frequency distributions. For instance, high mortality tates for young-of-the-year in the winter would lead to a length-frequency distribution dominated by older, larger krill the following summer, and Jow mortality rates to a high-proportion of the population as juveniles or sub-adults. Using such an analysis to separate out the effects of ‘recruitment potential’ and winter-over survival, however, requires a good estimate of spawning intensity, Siegel (1988) attempted to fallow certain year classes from an analysis of the length-irequency distribution of krill catches. Siegel (1988) suggested that larvae from the 1979-80 season were scarce in later years, but larvae from the 1980-81 season were abundant the following year. The first winter tor both these year classes, i,c. the winters of 1980 and 1981, was cold with heavy ice pack (Fig. 5). Yet recruitment differed significantly. One possible factor is that mean air temperatures in this region in the winter of 1979 were warmer than usual, and reflect the low ice cover that winter and spring (Zwally et al, 1983). Thus winter and spring conditions were not favourable for ‘recruitment potential’ in 1979-50, yet were favourable in 1980-81. The year class of 1980-81 had high ‘recruitment potential’ and probably high winter-over survival. The existing evidence thus suggests that ‘recruitment potential’ and winter-over survival both vary from year to year, and that both appear to be correlated with environmental conditions during the winter and early spring. However, i decrease in one is not necessarily followed by u decrease in the other. “Recruitment potential’ reflects environmental conditions before the Spawning season, and winter survival reflects conditions the winter after the spawning season. ACKNOWLEDGEMENTS The contributions. of our collaborators in these research efforts were invaluable. E. Hofmann and J. Capella created the time-and temperature-dependent model with physiological and behavioral data provided by ourselves, and first recognised the connection between the presence of Circumpolar MEMOIRS OF THE QUEENSLAND MUSEUM 2 (ia km |[ a Winter Temperalure | C} Maximum Area of Pack tce Year FIG, 5. Maximum extent of pack ice in the Weddell Seu sector (Seplember, October) (Zwally et al., 1983; Smith ef al, 1988) and mean winter (June, July, August and September) air temperatures al Admiralty Bay, King George Island (Rakusa-Suszc- zewski, 1988) irom 1973 to 1986. Deep Water and spawning populations. M. Amsler is a valued member of our research team. and was of enormous assistance in organising and conducting the field work in both winters. The work would not have been possible without the assistance of volunteers on both cruises: 1987, D. Martin, M. Elias, W. Connelly, 0. Schofield, D, Steinberg, J. Hydanus; 1989, A. Martinez, E. Stephens, D. Martin, R. Clark TV, J. Aldstadt, C. Stenler, W. Brock, D. Boylan. We also thank the captains and crews of the Polar Duke during two Winter cruises. The research reviewed was supported by NSF, Division of Polar Programs, with grants to E. Hofmann (DP-85-15486) and to R. Ross and L. Quetin (DPP-85-1 8872). LITERATURE CITED ANGER, K., AND DAWIRS, B.R. 1981. Influence of Starvation on the larval development of Myas uraneus (Decapoda, Majidae), Helgolander Meeresunters 34: 287-311, BERMAN, M.S... MCVEY, A.L.. AND ETTER- SHANK, G. 1989. Age determination of Antarc- tic krill using fluorescence and image analysis of size. Polar Biology 9: 267-271 . BRINTON, E., HUNTLEY, M., AND TOWNSEND, A.W.1986. Larvae of Euphausia superba in the Scotia Sea and Bransfield Strait in Match 1984 Development and abundance compared with 1981 larvae. Polar Biology 5: 221-234. BRINTON, E., LOEB, V.J.. MACAULAY, M.C., AND SHULENBERGER, E. 1987. Variability PHYSIOLOGY OF LARVAL EUPHAUSIIDS of Euphausia superba populations near Elephant Island and the South Shetlands: 198] vs. 1984, Polar Biology 7: 345-362. CAPELLA, J,, QUETIN, L-B.. HOFMANN, E.E.. AND ROSS, R.M.1N PRESS. Circulation and temperature effects on the development and dis- tribution of the embryos and larvae of the Ant- arctic krill, Euphausia superba — 111- Lagrangian model, Deep-Sea Research, CLARKE, A. 1985. Food webs and interactions; an overview of the Antarctic ecasystem, 329-350. In W.N, Bonner and D,W.H, Walton (ed.) ‘Key environments — Antarctica’. (Pergamon Press; Oxford). CROXALL, J.P., MCCANN, T.S., PRINCE, P.AL AND ROTHEN, P. 1988. Reproductive per- formance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976— 1987; Implications tor Southern Ocean monitor ing studies. 261-285. In D. Sahrhage (ed.) ‘Antarctic Ocean And resources variability’. (Springer-Verlag: Berlin). CUZIN-ROUDY, J_ 1987. Gonad history of the Ant- arctic krill Euphausia superba Dana during its breeding season, Polar Biulogy 7; 237-244, DALY, K.L..AND MACAULAY.M.C. 1988. Abun- dance and distribution of krill in the ice edge zone of the Weddell Sea. ausiral spring 1983, Deep Sea Research 35: 21-41. NAWIRS, R.R. 1987. Influence of limited starvation periods on growth and elemental composition (C. N. A) of Carcinus maenas (Decapoda: Por- tunidae) larvae reared im the laboratory, Murine Biology 93: 543-549. DURBIN, A.G., AND DURBIN, E.G. 1978. Length and weight relationships of Acartia claus) from Narragansett Bay, R. |. Limnology and Oceano- praphy 23: 958-969, EHRLICH, &.F., BLAXTER, J.H.S.. AND PEM- BERTON, R. 1976, Morphological and histo- logical changes during the growth and Starvation of herring and plaice larvae. Marine Biology 35: 105-118. ELIAS, M.C. 1990. “Effects af phatoperiad, phyto- plankton level and temperature on the growth, development and survival of larval Euphausja superba (Dana)’. Master of Science. University of California at Santa Barbara. ENDO, Y., IMASERI, T., AND KOMARLI, Y. 1986. Biomass and population structure of Anvarctic krill (Euphausia superba Dana) collected during SIBEX IT cruise of R.V. Kaiya Maru. Memuirs of the National tnstitute of Polar Research 44 (Special Issue); 107-117. ETTERSHANK, G. 1984. A new approach to the 33) assessment af longevity in the Antarctic krill Euphausia superba, Journal of Crustacean Bi- ology 4 (Special Number 1): 295-305, GARRISON, D.L.. AND SINIFF, D.B. 1986. An Antarctic perspective, Bioscience 36; 238-242. GUZMAN, QO. 1983, Distribution and abundance of Antarctic krill (Eaphausia superba) in the Bransfield Strait, 169-190. In B, Schnack (ed,) ‘On the biology of krill Buphausia superba’. (Alfred-Wegener-Institule for Polar Research: Bremerhaven). HAMNER, W.M. 1984. Aspects of schooling in Euphausia superba. Journal of Crustacean Bi- ology 4 (Special Number 1): 67-74. HAMNER, W.M., HAMNER, P.P., STRAND, S.W,, AND GILMER, R.W, 1983. Behaviour of Ant- arctic krill, Exphausia superba: chemorecep- tion, feeding. schooling, and moulting. Science 22(); 433-435, HEMPEBL, |. 1985. Variation in geographical distribu- lion and abundance of larvae of Antarctic krill, Euphausia superba, in the Southern Atlantic Ocean. 304-307. In W.R. Siegfried, P.R. Condy and R.M_Laws(eds) ‘Antarctic qutrient cycles and foad webs’, (Springer-Verlag; Berlin). HJORT. J. 1914. Fluctuations in the great fisheries of northern Europe viewed in the light of biolagical research, Rapport Proced Verbaux Reunion Conseil International Exploration de Mer 20: 1-228. HOFMANN, E.E,, CAPELLA, J,E.. ROSS, R.M., AND QUETIN, L.B.IN PRESS. Circulation and lemperature effects of the development and dis- iribulion of the embryos and larvae of the Ant- arclic krill, Euphetusia superba — 1. Time.and lemperature dependent model. Deep-Sea Re- search, ICHIH, T. 1996, Distribution of Antarctic krill concen- trations exploiled by Japanese krill lrawlers and minke whales. 36-36. (Tokyo. Japan: National Institute of Polar Research). IKEDA, T. 1984. Development of the larvae of the Antarctic krill (Euphuusia superba Dana) ob- served inthe laboratory. Journalof Experimental Marine Biology and Ecology 75; 107-117, TKEDA, T.. AND DIXON. P, (982. Body shrinkage as a possible aver-wintering mechanism of the Antarctic krill, Euphaisia superha Dana. Jour- nal of Experimental Marine Biology and Ecology 62: 143-151. KANDA, K,, TAKAGI, K., AND SEKI, Y. 1982. Movement o? the largerswarms of Antaretic krill Euphausia superba populations of Enderby Land during 1976-77 season, Journal of Tokyo University Fisheries 68: 25-42. KOTTMEIER, S.T., AND SULLIVAN, C.W,. 1987, Late winter primary production und bacterial production in sea ice and seawater west of the Antarctic Peninsula. Marine Ecology Progress Series 36; 287-298. LAWS, R.M. 1985. The ecology of the Southern Ocean, American Scientist 73: 26-40. LOWRY, L.F.. TESTA, J.W., AND CALVERT, W, 1988. Notes on winterfeeding of crabeater and seopard seals near the Antaretic Peninsula. Polar Biology %: 475-478, MARSCHALL, H.-P. 1985. Structural and functional analyses of the feeding appendages of krill larvae, 346-354, In W,R. Siegfried, PR. Condy and R.M. Laws (eds) ‘Antarctic nutrient cycles and food webs’, (Springer-Verlag; Berlin), 1988, The overwintering strategy of Antarctic krill under the pack-ice of the Weddell Sea. Polar Biology 9: 129-135. MARSCHALL, H.-P., AND HIRCHE, H.-J, 1984, Development of eggs and nauplii of Euphausta superba. Polar Biology 2; 245-250, MARSH, J.B,, AND WEINSTEIN, D.B. 1966. Simple charring method for determination of lipids. Journal of Lipid Research 7; 574-576, MAY, R.M, 1974. Larval mortality in marine fishes and the critical period concept. 3-19, In J.H.S. Blaxter (ed,) ‘The early life history of fish’. (Springer-Verlag: Berlin). MCCLATCHIE, 8S. 1988. Food limited growth of Euphausia superba in Admiralty Bay, Antare- tica. Continental Shelf Research &: 329-340. OMORI, M, 1970. Variations of length, weight, res- piratory rate, and chemical composition of Cu- lanus cristatus in relation to its fond and feeding. 113-126. In JH. Steele (ed.) ‘Marine food chains’. (University of California: Berkeley). PARRISH, R.H,, NELSON, C,S., AND BAKUN, A. 1981. Transport mechanisms and reproductive success of fishes in the California Current. Bio- logical Oceanography 1(2): 175-203. PRIDDLE, J., CROXALL, J.P.. EVERSON, I, HEY- WOOD, R.B., MURPHY, E.J., PRINCE, P.A., AND SEAR, C.B. 1988. Large-scale fluctua- tions in distribution and abundance of krill — A discussion of possible causes. 169-182. In D- Sahrhage (ed.) ‘Antarctic resources and yariabil- ity’, (Springer-Verlag; Berlin). QUETIN, L.B., AND ROSS, R.M. 19844. Depth dis- tribution of developing, Buphansia superba embryos, predicted from sinking rates, Marine Biology 79: 47-53. 1984b, School composition of the Antarctic krill, Euphausia superba, in waters west of the Ant- MEMOIRS OF THE QUEENSLAND MUSEUM arcic Peninsula, austral summer 1982, Journal of Crustacean Biology 4. (Spec, No, 1): 96-106, 1988. Summary of WINCRUISE II to the Antarctic Peninsula during June and July 1987. Antarctic Journal of the United States 23(5). 149-151. 1989. Effects of oxygen, temperature and age on the metabolic rate of the embryos and early lurval stages of the Antarctic krill Euphausia superba Dana. Journal of Experimental Marine Biology and Ecology t23: 43-62, 1991. Behavioral and physiological characteristics of the Antarctic krill, Euphausia superba, Amer- ican Zoologist 34(1): 117-146. QUETIN, L.B., ROSS, R.M.,, AND AMSLER, M.O. IN PRESS. Physiological condition of larvae of the Antarctic krill, Euphausia superba Dana, in winter. Journal of Plankton Research. RAKUSA-SUSZCZEWSKI 1988. Dilferences in the hydrology, biomass, and species distribution of plankton, fishes. and birds in the Bransfield Straitand the Drake Passage during FIBEX 1981 and SIBEX 1983/84. 214-218. In D. Sahrhage (ed,) “Antarctic Ocean and resources variabil- ily’, (Springer-Verlag: Berlin). ROSS, R.M.. AND QUETIN, L.B. 1953. Spawning frequency and fecundity of the Antarctic krill Euphausia superba, Marine Biology 77: 201- 205. 1985. The effect of pressure on the sinking rates of the embryos of the Antarctic krill Euphausia superba, Deep-Sea Research 32: 799-807, 1986. How productive are Antareuc knill? Bi- oScience 36: 264-269. 1989, Energetic cost to develop to the first feeding slage of Fuphausia superba Dana and the effect of delays in food availability. Journal of Experimental Marine Biology and Ecology 133: 103-127. ROSS, R.M., QUETIN, L.B., AND AMSLER, MO, 1985. Euphausia superba; A preliminary report on three areas of investigation, Antarctic Journal of the United States 19(5): 153-155. ROSS, R.M,, QUETIN, L.B., AMSLER, M.0., AND ELIAS, M.C. 1987. Larval and adult Antarctic krill, Euphausia superba, winter-over al Palmer Station, Antarctic Journal of the United States 22: 205-206. ROSS, R.M., QUETIN, L.B., AND KIRSCH, E, 1988. Effect of temperature or developmental times and survival of early larval slages of Euphausia su- perba Dana. Journal of Experimental Marine Bi- ology and Ecology 124; 55-71, SAHRHAGE, D- 1988. Some indications for en- viroomental and krill resources variability in the Southern Ocean, 33-40, In D. Sahrhage fed.) PHYSIOLOGY OF LARVAL EUPHAUSIIDS ‘Antarctic Ocean and resources variability’. (Springer-Verlag: Berlin). SHERMAN, K., SMITH, W., MORSE, W., BER- MAN, M., GREEN, J. AND EJSYMONT, L. 1984. Spawning strategies of fishes in relation to circulation, phytoplankton production, and pulses in zooplankton off the northeastern United States. Marine Ecolagy Progress Series 18: 1-19. SIEGEL, V. 1987. Age and growth of Antarctic Euphausiacea (Crustacea) under natural condi- tions. Marine Biology 96: 483-496. 1988. A concept of seasonal variation of krill (Euphausia superba) distribution and abundance west of the Antarctic Peninsula. 219-230. In D. Sahrhage (ed.) ‘Antarctic Ocean and resources var- iability’. (Springer-Verlag: Berlin). SINCLAIR, M. 1988. ‘Marine populations: An essay 333 on population regulation and speciation’. (Uni- versity of Washington Press: Seattle). 252p. SMITH, W.O., KEENE, N.K., AND COMISO, J.C. 1988. Interannual variability in estimated pri- mary productivity of the Antarctic marginal ice zone. 131-139. In D. Sahrhage (ed.) ‘Antarctic Ocean and resources variability’. (Springer-Ver- lag: Berlin). WITEK, A. AND KITTEL, W, 1985. Larvae of the species of the genus Euphausia (Euphausiacea, Crustacea) in southern part of the Drake Passage and Bransfield Strait during the BIOMASS- SIBEX (December 1983—January 1984). Polish Polar Research 6(1/2): 117-132. ZWALLY, H.J., PARKINSON, C.L., AND COM- ISO, J.C. 1983. Variability of Antarctic sea ice and changes in carbon dioxide. Science 220: 1005-1012. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum A SATELLITE TRACKED DRIFTER WITH A VERTICALLY MIGRATING DROGUE FOR STUDIES OF LARVAL DISPERSAL Potential larval dispersal is 2 function of time in the plankton and hydrographic regimes. This is further compli- cated by the interaction between environmental cucs and larval responses which dictate changes in vertical disinbu- tion of the larvae within that hydrographic milieu. These changes in distribution can be onlogenetic, cyclic (diurnal or tidal) ora combination of both. The vertical distribution of the larvae is usually measured by discrete sampling over i very short time frame (Rimmer and Phillips, 1979; Roth- lisberg, 1982). Because long-term, yertically-stratified sam> pling of larvae and known environmental simul are impracticable, the advection of larvae is extrapolated from these limited observations using a mean larval behaviour and a fixed circulation (Phillips and Williams, 1986) or estimated from models of both the larval behaviour and hydrographic regime (Rothlisberg er a@/.. 1983), A more direct approach to estimating dispersal pathways and potential is a device that mimics the larval behaviour in situ and can be monitored continuously, remotely and over the length of the planktonic larval life. This was the motivation for the satellite-tracked drifter with a vertically migrating drogue, The current drifter was designed to estimate the larval dispersal of the ornate rock lobsier Panalirus ormadus, in the northern Coral Sea and Gulf of Papua, We have used the behaviour of P, eygnus larvae (Rimmer and Phillips, 1979) as there have been no studies of the larval ecology of P. ornatus. Phyllosomes of P. cygnus undérgo diurmal Vertical migrations. of 100 to 150 m, are planktonic tor periods up to one year and potentially disperse over oceanic basins, The drogue has a fixed diural migration pattern, activated by light intensity, migrating al 10 m min between the surface at night and 130 m by day, The drogue is titted with a sensor so its depth can be monitored. The drifter uses solar power lo operate the winch and contro! electronics while the tele- metry transmitter uses dry cell batteri¢s for power, The lite span of the drifler, as dictated by baltery capacity. is upproxi~ mately one year. The geographic position of the drifter, the depth of the drogue, sutface temperature, seu state and battery METABOLIC RESPONSES OF SOME ESTUARINE CRUSTACEAN LARVAE TO SALINITY VARIATION Esluarine systems, characterised by large varjaftions in environmental parameters, aré widely recounised beth as areas Of high productivity aad as rearing grounds fora variety of marine and treshwarer crustaceans. In arder to hecome successfully adapted to this special environment, larval crustaceans must he able to tolerate such variations, specially in salinity. Although the influence of environmental parame- Terk.on fhe metabolic rare al adulr crustaceans has been the subject of several studies, few papers have dewlt wilh Jarvac. This paper presents data on some crustacean larvae whieh inhabit estuarine waters along the coast of the State of Sap Pauto, Brazil, the adults of whieh Jive in very different biotopes. The metabolic rates of these larvae Were deter- mined in different salinities (0.2, 7. 14,21, 28 and 44 pps) ar MEMOIRS OF THE QUEENSLAND MUSEUM voltage are transmitted 6 to 8 times per day by CLS-Argos tracking telemetry. Sea trials of the device are underway and deployment in the Gulf of Papua is planned for Decomber 1990). Future models of the drifier will ‘react’ ta the environment and will be able to ‘behave’ more realistically, They will be programmed with luxon specific behaviour régimes and ontogenetic changes in behaviour will also be possible. An in site (emperature sensor will monitor the environment and control the ‘growth tate’ of larvae and their allendant be- haviour, An in sit light meter will allaw the drogue to follow iso]umes and react to variable light intensity and penetration, An echu sounder will allaw the drogue to migrate near the bottom, permitting movement through shallow water and entrance into nursery grounds. Literature Cited Phillips, B.F. and McWilliams, P.S. 1986. The pelagic phase of spiny lobster development. Canadian Journal of Fish- eries und Aquatic Sciences 43; 2153-2163. Rimmer, D.W. and Phillips, B.F. 1979. Diurnal migration and vertical distribution of phyllosoma larvae of the western tock lobster Panulirus cygnus George. Marine Biology 54; 109-124, Rothlisberg. P.C. 1982, Vertical migration and its effect on dispersal of penaeid shrimp larvae in the Gulf of Carpen- taria, Australia, Fishery Bulletin of the United Status 80: 541-354, Rothlisberg, P.C., Church, J.A. and Forbes, A.M.G. 1983. Modelling the advection of vertically migrating shrimp larvae. Journal of Marine Research 44; 511-538, PC. Rothiisbere, CSIRO Marine Laboratortes, P.O. Bax 120, Cleveland, Queensland 4163, Australia. 1. Helmond, CSIRO Marine Laboratories, G.P.O. Rex 7538, Hobart, Tasmania 7007, Australia W, Dall, CSIRO Marine Labarateries, P.O. Bax 120, Cleveland, Queensland 4163, Australia. 20°C, using Curtesian diver microrespirometers. Larvae of Ihe vliwohuline or Freshwater species showed salinity inde- pendent metabolic rates over the salinity range 7-28 ppt while larvae of the mesohaline species regulate metabolism overa higher salinity range, 14-35 ppt. Larvae of he marine species (cuhaline), however, regulated metabolism over the salinity range 2)—35 pp. Such resulis tncicare Wat We larvae of these species, although developing in the same biotope, respond differently to salinuly Variations, revealing in some cases, greater metabolic regulation in (he silinity range ape proximating thal of the adult enyjronment, Gloria Sogres Moreinn, Departamento de Fisiologia Geral Inytiiuie de Biocténcias ¢ Instituto de Biologia Marinha, Universidade de San Paulo, San Paulo, Frrazil. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM FACETOTECTA (‘Y-LARVAE’): ONE DAY'S CATCH IN ORINAWA, JAPAN (CRUSTACEA; MAXILLOPODA) The Facetotecta (‘nauplius y’ and ‘cypris y." adults un- known) is classified together with the Cirripedia and Asco- thoracida in the maxillopodan subclass Thecostraca. These “Y-larvae’ were considered rare curiosities until It6 began a series of reports on the estimated 30 species he has found in Tanabe Bay, Honshu, Japan. 1t6"s (1986, 1987a. b, 1990, in press) are the only previously published descriptions of Pacific Facetotecta. In order to confirm whether y-larvae are similarly abundant and diverse elsewhere, | have been col- lecting them in Okinawa in the Ryukyu Islands, Methods Four plankton samples were taken with a small, fine-mesh net during a 24-hour period on 31 Aug and 1 Sept 1989 from the picr of the Sesoko Marine Scicnce Center on Sesoka- jima, Okinawa (26°38.5'N, 127°51.5°E). All y-larvae were immediately pipetted into a common holding dish and, after the last sample, fixed in formalin. Later the nauplii were processed for SEM: dehydration in ethanol, critical point drying from liquid COs, mounting on stubs, coating with gold. Most of the ‘long-tailed’ specimens were lost, so 15 similar ones from a sample taken on 5 Sept 1989 were substituted. In al], 103 nauplii were examined in a Hitachi S-510 scanning electron microscope and most were pholo- graphed. Results and Discussion Fifteen distinct ‘forms’ of nauplius y (1-22 specimens each), some with two or three putative instars, were recog- nised. Facetotéctans are thus diverse and abundant in Oki- nawa, and Tanabe Bay is not unique in this regard. However, nol every ‘form’ may represent a distinct species and instars may nol have been surely discriminated, Such determinations Ttequire the rearing of individual larvae through all their stages (ILO, in press). Of the 15 Okinawan ‘forms’, perhaps five alsa occur in Tanabe Bay. Two correspond to two supposed instars of nauplius y Pacific type 1 (1t6, 1986), that probably actually belong to distinct species. These and three undescribed but similar ‘forms’ are the only likely planktotraphs in the lov One ‘form’ corresponds to nauplius y type VII-c (Tt, 1987b). Two of the three ‘long-tailed forms’ may correspond to nauplius y type XI (Tio, 1987a) and an unnamed type (1t6, in press: fig. 1), but this is less certain. Of the six other undescribed Okinawan ‘forms,’ four ‘whale-shaped’ ones may represen| as few as one or two species. 116 (1990, in press) shows that at least five naupliar instars may be expected, but no more than three were recognised for any ‘form’ here. Some morphological observations may be important in detining the Facetotecta. Three of the present ‘forms’ have few or no cuticular ridges on the cephalic shield; however, many ridge pattern elements are clearly common to all the other ‘forms.’ Only the five supposedly planktotrophic ‘forms’ have a dorsocaudal organ. Frontal filaments are absent except possibly as a pair of swellings in two ‘forms,’ and rudimentary maxillules are also absent. This is the first extensive SEM survey of the nauplii ot any crustacean group, Acknowledgements | thank M. Hidaka for technical advice and the late Tat- sunori [6, to whom this report is dedicated, for assistance during a pilot SEM study and for access to unpublished information. This work was done during a term as a Visiting Foreign Researcher at the Sesoko Marine Science Center, Literature Cited Ir6, T, 1986. Three types of ‘nauplius y’ (Maxillopoda: Facetotecta) from the North Pacific, Publications of the Seto Marine Biological Laboratory 3: 63-73. 1987a. Proposal of new terminology for the morphology of nauplius y (Crustacea: Maxillopoda; Facetotecta) wiih provisional designation of four naupliar types from Japan, Zoological Science 4: 913-918, 1987b, Three forms of nauplius y type VIIT (Crustacea: Facctotecta) from the North Pacific. Publications of the _ Seto Marine Biological Laboratory 32; 141-150, 1990, Naupliar development of Hansenocaris furcifera Nd (Crustacea: Maxillopoda:Pacetotecta)from Tanabe Bay, Japan. Publications of the Seto Marine Biological Laboratory 34: 201-224 In Press. Observation of the larval development of nauplius y (Crustacea; Facetotecta) in the laboratory, Annual Report of the Seto Marine Biological Laboratory 4. M.J. Grygier, Sesako Marine Science Center, University of the Ryukyus, Sesoko, Motobu-cho, Okinawa 905-02, Japan (current address: [4804 Notley Road, Silver Spring, Maryland 20905, USA). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 336 ORIGIN AND BEHAVIOUR OF POST-LARVAL PENAEID PRAWNS IN TWO ESTUARIES ON THE NATAL COAST OF SOUTH AFRICA The northern Natal coast is the southern limit of commer- cially viable populations of penacid prawns on the east coast of Africa. The major centres of abundance are the St Lucia lakes and Richards Bay and the offshore Tugela Bank. The major commercial species are Penaeus indicus, Metapenaeus monoceros and P, monodon. The Natal fishery is associated with soft substrata and turbid water conditions, This type of habitat is relatively common in Natal estuaries but is less common in the offshore habitat where the shallow Tugela Bank is separated from the Mocambique grounds by some 400 km of deep, clear water overlying sandy substrata. Links between Mocambique and Natal prawn stocks ate unclear. The southward flowing Agulhas current could pro- vide a larval input which would influence population fluc- tuations in Natal. There is however, no information on the occurrence of post-larvae in this part of the Agulhas current, As there does not appear to be any indication that post-larvae are capable of selecting specific estuaries it was assumed thal larvae migrating into estuaries are representative of offshore populations. Plankton samples were taken overnight during spring flood tides at St Lucia on the northern edge of the LABORATORY REARED LARVAL STAGES OF A MANGROVE CRAB, SESARMA EDWARDSI DE MAN 1887 (DECAPODA : GRAPSIDAE) The complete larval development of a mangrove crab, Sesarma edwardsi, has been described from animals reared Under laboratory conditions at a femperature of 26+ 1°C and asalinily of 25 p.p.1. Larvae were fed freshly hatchedArtemia nauplii daily. Four zoeal stages and a megalopa appeared prior to metamorphosis to the first crab stage. Development time through to this stage was 16 days, intervals between zoeal Stages being 2 days except the final zoea (3 days) and MEMOIRS OF THE QUEENSLAND MUSEUM Tuyela Bank and also at the Agulhas dominated Kosi Bay just south of the Mocambique. border. Some ebb tide sam- pling was also done to provide comparative data on tdal behaviour in the turbid St Lucia and clear Kosi systems. Post-larvae of P. japonicus, a commercially unimportant species in Natal, totally dominated samples at Kosi Bay. Similar densities of this species were recorded at St Lucia but it was matched by the numbers of P, indicus while P. mono- don, P. semisulcatus and M. monoceros were also regularly present. The numbers of P. japonicus at St Lucia suggest a possible influence of the Agulhas current on recruitment but the other species recorded in this system indicate an addi- tional larval source. [Lis significant that the additional species are commercially important and thal these appear to be derived trom Natal waters rather than further north. Only P. japonicus occurred in sufficient numbers to allow comparison of post-larval tidal behaviour in both areas. This psammophilic species was present in the water column over flood and ebb tides in the muddy St Lucia system but in negligible numbers over ebb tides in the sandy Kosi estuary. Movement into the water column thus seems lo be influenced not only by the presence of tidal currents but also by the nature and suitability of the substratum, A.T. Forbes, Department of Biology, University of Natal, Durban, South Africa. megalopa (7 days). Unlike other species of Sesarma, brighily coloured chromatophores throughout the body in all larval stages are characteristic of 8. edwardsi. The setal formula of 0, 0, 6 on the endopod of the second maxilliped of zoeal stages, and the presence of 4 lateral setae on the telson separale §. edwardsi from others. of the genus so far de- scribed, T, Kannupandi and K. Pasupathi, Marine Ecology and Coastal Aquacuture Unit, Centre of Advanced Study in Marine Biology Annamalai University, Parangipettai 608 502, Tamil Nadu, India, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum PENAEID PRAWN RECRUITMENT: GEOGRAPHIC COMPARISON OF RECRUITMENT PATTERNS WITHIN THE INDO-WEST PACIFIC REGION D.J, STAPLES. Staples, D.J, 1991 09 01: Penaeid prawn recruitment: geographic comparison of recruit- ment patterns within the Indo-West Pacific region, Memuirs of te Queensland Museum 31: 337-348, Brisbane, ISSN 0079-8835, Despile many years of study, the basic seasonal dynamics and life-history parameters, such as longevity and generation lime. still remain poorly understood for many penacid prawns. Even in the better known commercially important species, considerable controversy still exists ag to whether the generation lime is one year or six months. This confusion appears (0 drise mainly from the extreme variability seen both between species and Within species in the seasonal dynamics of migrations, growth and abundance which underlies the seasonal cycles of Spawning and recruitment at the population level, These in turn have been modified, in many cases, by the impact of fishing, making comparisons of natural cycles extremely difficult. In an allempt to understand this variability, trends in the timing of the main life history events were related to factors which change with increasing latitude (and depth), An equatorial pattern of two generations per year provides the basis for (he description of many of the variants seen throughout each species range. Farther from the equator, one or other of the generations tends to dominate, resulting in what is essentially 4 one year generation time, In more temperate waters, most penaeids become strictly annual with one spawning period and one recruitment period euch year. A study of (hese changes With latitude in Penaeus mergudensis is used as an example to demonstrate these latitudinal differences. 1) Penaeids, reerutment, life history, Inde- West Pacific. DJ, Staples, CSIRO Marine Labaratories, P.O, Bax 120, Clevelund, Queensland 4163 Australia. Present Address: Bureau of Rural Resources, GPO Rox 858, Barron, Canberra, Australian Capital Territory 2000; 4 Qcteber, 1990, The world’s yield of penacid prawns is now in excess of 700,000 tons (Garcia, 1988) and forms one of the world’s most valuable fisheries, Despite this important position, the outlook for the fishery as a whole is not good. The high price of prawns on the export market during the 1970s. and 1980s has stimulated rapid development with inadequate controls. This has lead to exces- sive fishing effort, over capitalisation, excessive production costs and in some cases depleted stocks. Because many of these fisheries operate in developing countries, reliable stock assess- ments are few but those available have indicated that the stocks are overexploited resulting in less. than optimal returns for the effort expended in their capture. Growth overfishing (capture of individuals at size too small to produce the opti- mal yield) is common and despite carlicr us- sumptions concerning the resilience of prawn stocks to fishing pressure, recruitment overfish- ing (fishing effort at a level which will depress future spawning stocks and recruitment) has also been detected in several stocks (Penn and Caputi, 1985). Management measures addressing these problems include the limitation of fishing in space and time (area and seasonal closures) and limitation of effort through input controls. Both the detection of overfishing and subsequent re- medial action require detailed knowledge of the dynamics of the prawn's life history in terms of the distribution of the different life-history stages in both space and time. This information is not readily available for many of the world’s prawn stocks, The basic life cycle of penaeid prawns appears to be relatively uniform across the family; all shed eggs directly into the water column, pass through a relatively short larval life consisting of three stages (nauplius, protozoea, and mysis), and develop through postlarval, juvenile, sub- adult and adult stages. In contrast, the spatial and temporal distribution of these stages is extremely variable. Although many of the more commer- cially important species spawn at sca and spend their postlarval and juvenile stages in estuarine and nearshore coastal waters, there is a broad continuum of cycles ranging from species which are entirely estuarine to those which are entirely marine (Kutkuhn, 1966; Dall ef al., 1990). The temporal variability appears to be even grealer. In this paper I will concentrate on the temporal dynamics of penaeid life histories, starting with 338 a detailed examination of one species (Penaeus merguiensis) in Australia, moving on to a com- parison of life history patterns of other species throughout the world and finally give a brief account of a comparative study on the seasonal- ity of (P. merguiensis) across the Indo-West Pacific, In this way, I hope to provide an assess- meni of the current knowledge of penaeid life histories as well as future research needed in this field. PENAEUS MERGUIENSIS IN AUSTRALIA Munro (1975) provided the first detailed ac- count of the life history of P. merguiensis in the Gulf of Carpentaria, Australia, based on field sampling of adult prawns in the south eastern Gulf and juveniles in one of the adjacent man- grove estuaries. Because Munro observed spawning and immigration of postlarvae to occur only in spring, he concluded that the cycle was essentially annual. In a more detailed analysis of P. merguiensis from a range of locations, Staples (1979) showed that a simple annual cycle as suggested by Munro, could not explain the rather complex geographical differences in the sea- sonal timing of postlarval and juvenile prawns that occurred in different areas of the Gulf. Four areas in the Gulf, each characterised by its own pattern of seasonality were recognised and it was suggested that these geographical differences could be explained on the basis of semi-annual cycle of spawning, with peaks in spring and autumn. This pattern of spawning was later con- firmed by Crocos and Kerr (1983). Geographical differences in the differential survival of these generations in different areas of the Gulf sug- gested that the life cycle in the north was domi- nated by the survival through to juveniles of the autumn spawning whereas the life cycle in south was more influenced by the higher survival of the spring generation. A further complicating factor was that juvenile P. merguiensis emigrate out of the estuary to offshore waters mainly during periods of rain (Staples and Vance, 1986) and because rainfall is extremely seasonal in the Gulf of Carpentaria (only one wet season each year) only one pulse of prawns recruit each year into offshore waters. Based on more recent evidence the life history pattern was reviewed by Rothlisberg er al. (1985). In the southern Gulf, larvae from the spring spawning period reach the estuaries as post- larvae 2-3 weeks after hatching and spend 2-4 months as juveniles before emigrating offshore MEMOIRS OF THE QUEENSLAND MUSEUM during the summer wet season. After approxi- mately 2 months migration offshore, subadult prawns recruit into the offshore fishery (4-7 months old) and form the basis of the autumn fishery. A proportion of these young recruits become sexually mature and spawn giving rise to the autumn larvae. Most of these larvae never reach the estuarine nursery areas (Rothlisberg et al., 1983) and it is the prawns which escape the autumn fishery and survive through to the next spring which provide the spawning stock to re- peat the cycle (Fig. 1). In the north the spring component of the cycle is similar but many more larvae produced from the autumn spawning re- cruit into the estuaries. More recent information on the seasonal distribution of postlarvae in the northern areas, suggests that the strength of the spring generation of postlarvae and juveniles may have been underestimated in previous stu- dies (Vance et al., 1990) but the general conclu- 30/4 Southeastern Gulf Egg production index Larvae (no, m-?) ae ey o- nw & Postlarvae 03 @ Planktonic — Benthic rol b \ (no. m-2) 1 °o a (no, 10 m-3) Benthic postlarvae o Planktonic postlarvae o Juveniles (no. m-?) Emigrants (no. h~") Gatch (tonnes) n 5 Aduits (no, n7") oo FIG. 1, Seasonal dynamics in the abundance of the main life-history stages of Penaeus merguiensis in the southeast Gulf of Carpentaria (from Rothlisberg etal., 1985). PENAEID PRAWN RECRUITMENT sions have remained unchanged. Because of the unimodal rainfall pattern and offshore recruit- ment, autumn juveniles contribute less to the offshore fishery than those from the spring generation (Fig. 2). Rothlisberg et al. (1985) suggest that the life history seen in the Gulf was derived from a basic pattern of two equal spring and autumn popula- tions, each contributing to the next generation 6 months later with some survivors of this group contributing again in 12 months, i.e. two inter- locking cycles of 6 and 12 months. This implies two wet seasons per year and two periods of offshore recruitment, Another notable feature of P. merguiensis in the Gulf is the mismatch be- tween the size of the spawning population and the size of its contribution to the next generation. This is especially apparent in the southern Gulf where the extremely small spring population of females gives rise to the large number of post- larvae and the subsequent offshore fishery. Gar- cia (1988) has argued that because of the extremely heavy exploitation of P. merguiensis, (approximately 80% of the population is caught in the 2 months following recruitment (Lucas ef al,, 1979), this represents a severe distortion of the basic life cycle, and without fishing the Spring spawning would constitute the main re- productive input. Because the life history of P. merguiensis is composed of two interlocking cycles with peri- ods of 6 months and 12 months, there has been some controversy in the literature about the generation time for this species and penaeids in general. At an individual Jevel, generation time is defined as the time between egg and first spawning is 6 months, At the population level, Garcia (1988) argues that the gencration time should be defined as the time between the aver- age date of birth of the main generation and the average date of birth of the main group of off- spring from the generation. Using this definition, the main generation in the Gull is obviously the spting generation and the generation time is 12 months, REVIEW OF WORLD LIFE HISTORY PATTERNS The life span of most coastal penaeids is be- jween | and 2 years in the tropics but is probably longer in temperate waters. The length of time spent in the different life history stages is a function of the growth rate. Environmental fac- tors such as temperature that vary with season, 339 Albatross Bay Egg production indes Larvae (nom *) Prelinrewn 412 BH Prenhlonie — Berle. Bemhic poctisrvee (no me) ° in o n Planktonic post layvar {no Won 3) \ i c \ 3 i Aver elie Dverwinver duveniles faa m*) Calon tonnes) Adults (no no'), Time (menths] FIG. 2, Seasonal dynamics in the abundance of the main life-histary stages of Penaeus merguiensis in Albatross Bay, northeast Gulf of Carpentaria (from Rothlisberg et.al, 1985), latitude and depth, therefore, also contro) the time to first maturity, and consequently the genetation time_ Latitudinal trends reflecting changes in temperature and rainfall patterns, therefore, are extremely important in consider- ing penaeid life history patterns. Similar trends in life-history parameters will also occur with changes in depth. In an attempt to standardise for these effects, | will consider the three latitudinal zones: equatorial (+5", tropical/subtropical (5— 25°) and temperate (>25°), recognising that this is a oversimplification and will not account for areas influenced by local events such as upwel- lings. However, despite these local events, the classification does assist in the interpretation of observed life-history patterns. EQUATORIAL PATTERN Little information is available on penaeids in equatorial regions. However, close to the equa- tor, individual prawns appear to be capable of spawning all year round (Hall, 1962), although seasonal cycles in abundance in prawns Will MEMOIRS OF THE QUEENSLAND MUSEUM Six months Six months Six months Six months Six months Six months FIG. 3. Schematic life histories of equatorial penaeid prawns, A, alternation of annual generations. B, interlocking six-monthly and yearly generations (from Dall er al., 1990). result in seasonal spawning activity at the popu- lation level (Garcia, }977). Population cycles are affected by seasonal rainfall, often associated with seasonal monsoons or seasonal temperature changes brought about by the seasonal shifts in the winds, especially in localities clase to conti- nental land masses. At the population level, this appears to result in two main periods of increased spawning in each year, even in populations close to the equator (Hall, 1962; Pauly et al., 1984; Staples and Rothlisberg, 1990). These periods of increased spawning tend to occur during the intermonsoonal months of September — Novem- ber and March — May, periods characterised by decreased winds and currents. By analogy with temperate regions, these periods will be called spring and autumn. Hall (1962), suggested that this bimodal pat- tern of spawning was maintained by an alterna- tion of the generations in which the generation time is one year; the spring generation gives rise to the spring generation of the following year and the same for the autumn generation (Fig. 3A), It must be stressed that this interpretation of penaeid life histories is based on an assumption that it took the main species observed, Mera- penaeus moyebi, one year to reach maturity. We know from the work of Crocos and Kerr (1983) thal Penaeus merguiensis can mature in 6 months in a sub-tropical area, and a more likely interpretation is that the equatorial penaeids ex- hibit combinations of 6-monthly and 12-monthly cycles aS suggested as a basic scheme for P, merguiensis by Rothlisberg et al, (1985). This concept has been extended to produce hypothe- tical scheme for an equatorial pattern which has equal contributions from both the 6-monthly and 12-monthly cycles (Fig. 3B). Obviously more re- search on equatorial populations is required includ- ing more information on the size and age of first maturity and the proportion of the two generations which mature and spawn within their first 6 months of life. The next section of this paper describes a study in the Indo-West Pacific aimed at providing some of this information. The hypothetical equatorial pattern, although substantiated with few data at this time, does serve as a useful conceptual model for discussing other latitudinal patterns. All of the patterns seen in both the tropical and temperate regions can be derived by the removal or modification of appro- priate links, TROPICAL/SUBTROPICAL PATTERN Bimodal spawning and recruitment are also extremely common in the slightly higher latitudes, PENAEID PRAWN RECRUITMENT 341 Six months Six months Six months Six months Six months Six months Six months Six months Six months FIG. 4. Schematic life histories of tropical and temperate penaeids. A, ‘typical’ tropical Penaeus pattern (after Garcia, 1985). B, Penaeus merguiensis in southeast Gulf of Carpentaria (after Rothlisberg et al., 1985). C, temperate pattern with summer spawning (from Dall et al., 1990). but in contrast with the equatorial pattern, it appears that seasonal rainfall and lower winter temperature results in either the spring or autumn generation being dominant in the offshore phase. Penaeus merguiensis in Gulf of Carpentaria fits into this pattern but is rather extreme in its asym- metry (Fig. 4B). Other examples include P. notialis in Senegal (Garcia, 1977; Lhomme and Garcia, 1984), P. semisulcatus and M. affinis in Kuwait (Mathews et al., 1987), P. semisulcatus in northern Australia (Crocos, 1987; Somers, 1987), P. indicus in Madagascar (Le Reste, 1971, 1978; Le Reste and Marcille, 1976) and M. dobsoni, P. indicus and Parapenaeopsis stylifera in India (Kurup and Rao, 1975), P. notialis and P. schmitti in Cuba (Perez et al., 1984a, b). Bimodal postlarval recruitment pat- terns have been recorded for P. merguiensis, P. japonicus, P.semisulcatus and P. monodon in the Philippines (Motoh, 1981) and P. japonicus in Natal (Forbes and Benfield, 1986), in Japan (Mito, 1972) and in Korea (Pyen, 1974). Similarly, sea- sonal postlarval patterns of M. brevicornis, M. dobsoni, M. monoceros, P. monodon, P. semisul- catus, and P. indicus have been reported for several estuaries along the coast of India. A summary of these presented by Babu and Babu (1987) shows that despite considerable local variability, all spe- cies show two peaks of increased postlarval abun- dance within the year in most locations. Bimodal recruitment into offshore fisheries which link to the bimodal pattern of postlarval abundance in India has also been reported by several authors (Kurup and Rao, 1975). Pérez Farfante (1969). provides a comprehen- sive summary of the life history of several west- ern Atlantic species, In the tropical/subtropical regions, P. aztecus, P. duorarum and P. setiferus are known [g have both spring and autumn generations. This fact has caused considerable confusion in earlier interpretations of Gulf of Mexico prawn life histories. For example. Bax: ter and Renfro (1967) reported that the postlarval peak in abundance was 6 months out of phase with the peak of larval abundance observed by ‘Temple and Fischer (1967). On the basis of this mismatch, Temple and Fischer suggested that P. aztecus must overwinter in the postlarval stage. A more likely interpretation is that one group of workers had observed the spring generation while the other had observed the autumn generation. Because a life history pattern with dispropor- tionate spring and autumn generations appears to be common in the tropics, Garcia (1985) sug- gested that this was the typical pattern for the genus Penaeus as a whole (Fig. 4A). In this scheme he describes a large spring spawning peak whictr produces a strong spring generation which reeruits into the adult population the fol- lowing autumn and spawns again the following spring to give a generation time of J year for lhis main generation. A small proportion of the new FeCrusts Spawn in autumn giving rise to a small more intermittent autumn generation (Fig. 4A), Garcia, in proposing this model accepted that it may be an Gversimplification but that it provided a stimulus for discussion, The literature shows that several Penaeus species do not fit the Garcia model. P. merguiersis , for example, although having an apparently overall patlern, differs in one important point (compare Fig. 4A and 4B). The proportion of prawns spawning during autumn is much greater and as a result the gutumn spawning becomes the major event, Several other studies have also reported that this is the case, including P. senmisulcaius and M. affinis in, Kuwait (Mathews er al, 1987), P, notialis in north Senegal (Lhomme and Garcia. 1984), P. notialis and P. schmitiiin Cuba (Perez etal., 1984 a, bj. Gareia, bowever, argues that spring phytoplankton blooms are 4 globsl occur- rence and as a tesult of increased larval food at this time, natural selection would favour a larger spring spawning biomass. Because all the ex- amples given above arc heavily fished stocks, he suggests that in {hese cases. the spring spawning MEMOIRS OF THE QUEENSLAND MUSEUM population may have been severely reduced asa result of fishing the autumn recruits and the populations do not truly reflect the pre-fishing situation, More research on the seasonal dynam- ies of phytoplankton throughout the tropics would help resalve this debate. TEMPERATE PATTERN The influence af temperature on the life history dynamics becomes much more obvious further from the equator, There is a trend for the bimodal spawning pattern seen in many species in the tropics ta become unimodal in temperate lati- tudes, This is usually associated with one well- defined period of recruitment into the offshore fishery each year and the species becomes truly annual witha generation time of 1 year (Fig. 4C), In many species the spawning season shifts to the summer period when temperatures are similar to those experienced during the spring or autumn in more tropical areas of the species distribu- tions. Reported examples of this trend oecur in both P, aztecus and P. duerarum in the western Atlantic. Penaeus aztecus spawns both in spring and autumn in Florida Bay, but there as only summer spawning further north along the Carolina coast (Pérez Farfante, 1969), Penaeus Japonicus is another species with wide geo- graphic range which shows a Strong geographi- cal irend in its Jife history dynamics. Spawning is bimodal over much of its range (as described above) but is confined to the summer months in the Mediterranean (Tom and Lewinsohn, 1983), in Japan (Hudinaga, 1942) and in Korea (Lee and Lee, 1970). In Australia, P. latisnicatus has all year-round spawning with two peaks in northern regions, Which becomes reduced to a single peak in southern Australia (Penn, 1980). Penaeus merguiensis, although exhibiting bimodal spawning over most of its range, is unimodal in the south China Sea with a peak of spawning in spring (Liu, 1986). Several species with geographical ranges re- stricted to the ternperate zone also have spawn- ing seasons restricted to one period each year. Penaeus setiferus shows a unimodal pattern over ils entire range. In the Pohai Sea (37° —45°N}, P, chinensis [= orientalis] exhibits an extreme adaptation lo a cool temperate climate (Chang Cheng, 1984). Adults spawn in shallow water in early spring at 13°C and juveniles begin leaving the nursery grounds of the Pohai Sea in summer and migrate into deeper waters, where after over- wintering offshore they return to ihe Pohai Sea as mature adults. to spawn. In some other cases, PENAEID PRAWN RECRUITMENT 34 prawns spawn in late summer or autumn and it a the juvenile stage which overwinters in the nursery grounds. e.g, P, plebejus, Ruello, 1975; MW. macleays, Glaister, 1978; M. bennevee. Coles and Greenwood, 1983, As expected, several penacid species have been shown to have depth related changes in their life history which parallel those seen in changes with latitude. Penaeus aztecus, in the Gulf of Mexico, spawns from spring to early winter at 27m depth, with a period of greatest activity from October-December and a smaller peak from March-May. At greater depths. spawning is more or less continuous (Cook and Lindner, 1970). PENAEUS MERGUIENSIS IN THE INDO-WEST PACIFIC As seen from the above review several issues require further research. These include: 1. Does the hypothetical life history pattern of interlocking 6-monthly and 12-monthly cycles exist in (he equatorial region? 2. Can the life history pattern of penacids throughout their range be derived from this hy- pothetical model? 3. In tropical penaeids, is the seasonality of spawning adapted to the seasonality of phyto- plankton production where the spring spawning event is the main spawning season as suggested hy Garcia (1985)? 4. Asa resultof 3, is the generation time always one year (defined as the average date of birth of the main generation and the average date of birth of the offspring from this generation)? 5. What other environmental factors are re- sponsible for the variability in life-history pat- terns seen across a species geographical range? {nan attempt to answer [hese questions and to provide a better management-orientated re- search programme for several countries across the Indo-West Pacific region, the Penacid Re- cruitment Program (PREP) was established in 1988 under the auspices of the Intergovernmen- tal Occanographic Commission (1OC) and the United Nations Food and Agriculture Organisa- tion (FAQ). By selecting study sites in 6 coun- tries (Philippines, Thailand, Malaysia, Indonesia, Papua New Guinea and Australia) the life history dynamics of Penaeus merguiensis cun be compared across a range of latitudes, climatic regimes and fishing activities. Addi- tional sites in Brunei, Darussalam and Peoples Republic of China are soon to be included_Inall ~ siles, we are attempting to collect data on the seasonal abundance of the major life history stages of P. merguiensis and then lo compare (hen across the region. A full deseription of the study has been pub- lished by Staples and Rothlisberg (1990). Spawning follows a bimodal pattern in most countries (not all countries are able to collect spawning data) during periods roughly coincid- ing with the (@mperate spring and autumn sea- sons. Most data for subadult and adult prawns come fram commercial catch sampling and al- though many other interpretations are possible, iL is assumed al this stage that these show sea- sonal trends in abundance and hence reflect re- cruitment into the offshore area (Fig. 5). Close to the equator at the Malaysian site the catch per unit effort (CPUB) is high in all months with higher catch rates being recorded from Mareh— May and from September—December (Fig. 5C). Further frorn the equator at the Indonesian and Thailand sites, recruitment becomes more asym metrical with the Septermber-December peak dominating, In Papua New Guinea, asymmetry also occurs but the peak is in April—July. At higher latitudes, in (he Philippines and Australia, rectuitment into the offshore fishery resulted in one major peak in catch rate from October— January in the Philippines and from February— April in Australia. To date, the programme has demonstrated a clear latitudinal trend from a bimodal recruit- ment pattern near the equator to an unimodal pattern at higher latitudes, There is also general agreement in the timing of recruitment peaks across the region. Unlike the ‘typical’ pattern of the genus Penaeus, however, the autumn recruit: ment is not always dominant. An interesting example is that of Indonesia and PNG where although both sites are situated on 8°S, the pewks in recruitment are several months out of phase. Becausé of the strong correlation between the timing of rainfall and the emigration of juvenile prawns out of the estuary (Staples and Vance, 1986) in Australia, the seasonal timing of rainfall in the six sites was examined to determine whether this factor alone could account for the variability in the pattern of recruitment seen across the region. In general, the seasonal patlern in the CPUE closely followed the seasonal pat- tern of rainfall in all sites (Figs 5, 6). Australia is the extreme example where the one distinct wet season forces an extremely distinct seasonal pulse in recruitment, In the Indonesian and PNG cases, the phase shift in the recruitment timing 344 also appears to be related to the phase shift in rainfall, with a September—December peak in rainfall in the Indonesian site and a May—July peak in PNG. In Fig, 7A, the hypothetical equatorial pattern is represented by a bar diagram which joins the two main generations from their time of spawn- ing to their time of recruitment into the offshore region 6 months later. Superimposed on these progressions is a bimodal seasonality of rainfall which coincides with the periods of spawning and subsequent recruitment. Of the 6 PREP study sites, the Malaysian site is the closest rep- resentative to the hypothetical equatorial situa- tion. Unfortunately, we do not have spawning data yet, but juveniles and adults appear to closely follow the hypothetical pattern with a bimodal recruitment pattern coinciding with the two wet seasons. In Indonesia and Thailand, a marked asymmetry in both rainfall and recruit- ment occurs. In both these localities, tracing the zs (a) Philippines : Sorsogon Bay _— —~ ap a 8 be a ° 2 = 2 S Oo > 10 (c) Malaysia :; Larut Matang oO P. rr ° 2 =) a ui 2 o oO J FMAM 3 J A S ON D 12 (e@) Papua New Guinea : Gull of Papua z= 10 = a & =< 6 wu 3 a o o 2 0 A Ss O N D J oF MAM J Jd Month MEMOIRS OF THE QUEENSLAND MUSEUM two recruitment pulses back to their spawning origins, shows that in both cases the main recruit- ment event (spring in Indonesia and autumn in Thailand) originated from the smaller of the two spawning peaks (shown as narrow bars in Fig. 7C, E). In Australia and the Philippines, with only one main wet season, one generation Is lost almost entirely from the population. From these preliminary results we can start to answer the questions posed above. It would ap- pear that the different life history patterns seen in P, merguiensis across the Indo-West Pacific can be derived from modifications of the hy- pothetical equatorial scheme. It would also ap- pear that the hypothetical pattern can be found close to the equator in areas experiencing two equal wet seasons each year such as that ob- served in west Malaysia. More research is needed to establish whether the two generations show a true aliernation of generations as sug- gested by Hall (1962), or whether the pattern is soo , (OD) = Thailand ; Gulf of Thailand 400 (g/hr) CPUE FMA Md J A S ON D Indonesia 60 (d) > Cilacap (kg/boat-day) CPUE Australia : Albatross Bay soo, (f) CPUE(No./trawl) J oF MA MJ J A S OW D Month FIG, 5. Seasonal distribution of catch per unit effort (CPUE) of Penaeus merguiensis from six localities across the Indo-West Pacific (from Staples and Rothlisberg, 1990). PENAEID PRAWN RECRUITMENT 34. 600 (a) Philippines : Sorsogon bay (mm) 8 200 Rainfall 600 (c) Malaysia ; Larut Matang (mm) 3 200 Rainfall Oo N OD 600 (e) Papua New Guinea : Gulf of Papua (mm) 400 200 Rainfall 0 J F MAM J J A S O N D Month tn goo - (6) Thailand : Guit of Thailand E E 400 S = 200 a rea 0 Jd F MAM J JS A S O WN D 600 (d) Indonesia ; Cilacap E E 400 S £ w rea soo. ~ (1) Australia : Albatross Bay — E 400 = c 200 ‘a c 0 J F MAM JS J A S ON OD Month FIG. 6, Seasonal distribution of rainfall at six localities across the Indo-West Pacific (from Staples and Rathlisberg, 1990). an interlocking of 6-monthly and 12-monthly cycles. Based on the Australian results | suggest that the latter is most likely. Without seasonal phytoplankton results it is also not possible to determine whether the seasonal spawning dy- namics is in phase with phytoplankton biomass as suggested by Garcia (1988). However, from the limited data available it does seem likely that the major spawning can occur in either spring or autumn. An obvious reason for the shift is that for P. merguiensis the spawning intensity al the population level is greatest at the time of maxi- mum recruitment (large number of small ripe females). This appears to be true in both Thai- land and Indonesia, for example, the main spawning season (spring and aulumn, respec- tively) occurs during the time of major recruil- ment, this event itself being under the influence of rainfall. A testable hypothesis is that the major spawning occurs during or following the major Wet season (as a result of major recruitment). This may also link with increased phytoplankton productivity, but not necessarily a spring bloom. CONCLUSIONS 1. Penaeus merguiensis in Australia exhibits a rather unusual life history pattern with two spawning seasons each year, but the main generation of prawns in autumn arising from a rather minor peak of spawning in spring. In some areas of the Gulf of Carpentaria, offspring from the large autumn spawning do not contribute significantly to the subsequent offshore popula- tion because of high larval and postlarval mor- tality. 2. There are many examples of bimodal spawning within the year in tropical penaeids, Eggs & larvae Postlarvae (a) Juveniles § Subadults § Adults ; Philippines Eaqgs & larvae {b) Adults Thailand Eggs & larvae \ Postlarvae (c) Juveniles Subadults Adults - Malaysia (d) Juveniles Subadults Adults Indonesia Eggs & larvae Postlarvae (e) Adults Australia Eggs & larvae Postlarvae (f) Juveniles Subadults Adults n i MAMwsdJA4S ON FIG. 7. Seasonal life-history dynamics of Penaeus merguiensis as indicated by the cycles of abundance of the main life history stages from five sites across the Indo-west Pacific shown together with a hy- pothetical equatorial pattern. Light and heavy shaded areas denote minor and major wet seasons (from Staples and Rothlisberg, 1990). and in many cases a disproportionate survival produces one main and one subsidiary genera- tion (it can be either spring or autumn, but com- monly spring). In these cases, description of the generation time is difficult and depends largely on the definition used. 3. Itis hypothesised that all these asymmetrical life history patterns are derived from asymmetri- cal equatorial pattern where both generations interlock in 6-monthly and 12-monthly cycles. 4, In higher latitudes, the bimodal spawning pattern becomes reduced to a single spawning season and the generation time is definitely one year. MEMOIRS OF THE QUEENSLAND MUSEUM 5. By comparing the life history dynamics of P, merguiensis across the Indo-West Pacific, the derivation of the many variants seen in local life-history patterns can be derived from the hypothetical equatorial scheme. 6. Further research on the factors affecting recruitment strength and timing is needed across a broad geographic range before the basic life history dynamics of penaeids is fully understood. ACKNOWLEDGEMENTS This paper represents the work of many scien- tists. In particular, | thank Peter Rothlisberg and Peter Crocos, CSIRO, Cleveland, Australia for the use of their data to complete the description of the dynamics of Penaeus merguiensis in Australia. The collaboration and assistance of scientists in the Philippines, Thailand, Malaysia, Indonesia and Papua New Guinea is also grate- fully acknowledged. A large part of the Australian studies were supported by the Fisher- ies Industry Research and Development Council and the southeast Asian collaborative program was carried out with assistance of grants from the Inter-Governmental Commission of UNESCO (IOC) and the United Nations Food and Agricul- ture Organisation (FAO). LITERATURE CITED BABU, K.S. AND BABU K.S. 1987. Recruitment patterns of penaeid prawn postlarvae into the Upputeru Estuary, India. 345-350. In M.F, Thompson, R. Sarojini, R. Nagabhushanam (eds) ‘Biology of benthic marine organisms techniques and methods as applied to the Indian Ocean’. (A.A. Balkema: Rotterdam). Indian Edition Series 1,2. BAXTER, K.N. AND RENFRO, W.C. 1967. Sea- sonal occurrence and size distribution of postlar- val brown and white shrimp near Galveston, Texas, with notes on species identification. Fish- ery Bulletin of the United States 66: 149-158. CHANG CHENG, YE. 1984. The prawn (Penaeus orientalis Kishinouye) in Pohai Sea and their fishery. 49-60. In J.A. Gulland and B.J. Rothschild (eds) ‘Penaeid shrimps — their bi- ology and management.’ (Fishing News Books Ltd: Farnham). COLES, R.G. AND GREENWOOD, J.G. 1983. Sea- sonal movement and size distribution of three commercially important Australian prawn spe- cies (Crustacea:Penaeidae) within an estuarine PENAEID PRAWN RECRUITMENT system, Australian Journal of Marine and Fresh- waler Research 34; 727-743, COOK, H.L, AND LINDNER, M.J. 1970. Synopsis of biological data on the brown shrimp Penaeus aztecus aztecus Ives 1891. FAO Fisheries Re- ports 57; 1471-1497, CROCOS, P.C. AND KERR. J.D. 1983. Maturation and spawning of the banana prawn Pernceus iere@ulensts de Man (Crustacea; Penuegidue) in the Gulf of Carpentaria, Australia. Journal of Experimental Marine Biology and Ecology 69: 37-59, CROCOS, P.J. 1987. 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Gulland (ed.) ‘Fish population dynamics’, Seo- ond Edition, John Wiley and Sons Ltd: Chi- chester, U.K.) GLAISTER, J.P. 1978, Movement and growth of tagged school prawns, Metapenaeuy macleayi (Haswell) (Crustacea: Pengcidac), in the Clarence River region of northern New South Wales. Australian Journal of Marine and Fresh- water Research 29; 645-657. HALL, D.N.F, 1962. ‘Observations on the taxonomy and biology of some Indo-West-Pacilic Penaeidae (Crustacea, Decapoda)’. Colonial Of- Tice, Fishery Publications No.17. (Her Majesty's Stationary Office: London). 229p, HUDINAGA, M. 1942. Reproduction, development and rearing of Penaeus japonicus Bate, Japanese Journal of Zoology 10; 305-393, KURUP, N.S. AND RAQ, P.V. 1975. Population characteristics and exploitation of the important marine prawns of Ambalapuzha, Kerala, Indian Journal of Fisheries 21: 183-210. KUTKUHN, IF. 1966. The role of estuaries in the development and perpetuation of commercial shrimp resources. American Fisheries Society. Special Publication 3; 16-36, LEE, T.Y, AND LEE, B.D. 1970, Ovarian cycle and oogenesis in Penaeus japonicus Bate. Publica- tions of the Haewundae Marine Laboratories a: 45-52. LE.RESTE, L. 1971. Rhythme saisonnier de la repro- duction, migration et croissance des postlarves el des jeunes chez la crevette Penaeus indicus H, Milne Edwards de la baie d'Ambaro. Cate N.O, de Madagascar. Cahiers ORSTOM Séries Océanographique 9: 279-292, 1978. Biologie d'une population de creveties, Penacus indicus H, Milne Edwards, sur la cite nord-ouest Madagascar, Travaux el Documenis. ORSTOM 99; 1-291, LE RESTE, L. AND MARCILLE, J. 1976. Biology of the shrimp Penaeus indicus H. Milne Edwards in Mudayuscar: growth, recruilment migrations, reproduction, mortality; A contribution to the study of an eutrophic tropical bay. Cahiers ORS- TOM Series Oceanographique 14: 109-127, LIU, J.¥. 1986, *Penueoid shrimps of the South China Sea’. (Agricultural Publishing House: Beijing), 278p. [In Chinese]. LHOMME, F. AND GARCIA, S. 1984. Biologie et exploitation de la crevelle penaeide au Senegal. Hl-144. In JA. Gulland and BJ. Rothschild (eds) “Penaeid shrimp — theit biology and man- agement’. (Fishing News Books: Farnham, Eng~ land). LUCAS, C.. KIRK WOOD, G. AND SOMERS, I. 1979, An assessment of the banana prawn Penaeus merguiensis in (he Gulf of Carpentaria, Australian Journal of Marine and Freshwater Research 30); 639-652, MATHEWS, C.P., AL-HOSSAINI, M., ABDUL GHAFFAR, A.R. AND AL-SHOUSANI M. 1987. Assessment of short-lived stocks with special reference to Kuwait's shrimp fisheries: a contrast of the results obtained from traditional and recent size-based techniques. 147-166. In D. Pauly und G.R, Morgan (eds) ‘Length-based methods in fisheries research’ ICLARM Confer- ence Proceedings 13. MITO, S, 1972. Investigation on the pursuit of artifi- cially produced prawn larvae liberated into the sea. Proceedings of the Indo-Pacific Fisheries Council 13; 215-223, MOTOH, H. 1981. Studies on the fisheries biology of the giant prawns, Penaeus monodon in the Phil- ippines, Southeast Asian Fisheries Development Center Technical Report 7; 1-128. MUNRO, LS.R. 1975, Biology of ihe banana prawn (Penaeus merguiensis) in the south-east corner of the Gulfof Carpentaria. 60-78, In P.C. Young (ed,) ‘First Australian national prawn seminar . (Australian Government Publishing Service: Canberra, Australia). PAULY, D., INGLES, J, AND NEAL, R. 1984. Ap- plication to shrimp stocks of objective methods for the estimation of growth, mortality and re- cruitment-related parameters from length- frequency data (ELEFAN | and ELEFAN II). 220-234. In J.A. Gulland and B,J, Rothschild (eds) ‘Penaeid shrimps — their biology and management.’ (Fishing News Books: Farnham England), PENN, J.W. 1980. Spawning and fecundity of the western king prawn, Penaeus latisulcatus Kish> inouye, in Western Australian waters. Australian Journal of Marine and Freshwater Research 31: 21-35, PENN, J.W. AND CAPUTI, N. 1985. Stock recruit- ment relationships for the tiger prawn, Penaeus esculentus, tishery in Exmouth Gulf, Western Australia, and their implications for manage- ment. 165-173. In P.C. Rothlisberg, BJ. Hill, and DJ. Staples (eds) ‘Second Australian nstional prawn seminar’ NPS2_ (Cleveland: Australia), PEREZ, A.R., PUGA, R. AND RODRIGUES, J, 1984a. The stock assessment and management of Cuban shrimp stacks. 48-119, In C.P, Mat- thews (ed.) ‘Proceedings of (he shrimp and fin fisheries management workshop’ Vol, |, KISR 1366/MB-48. (Kuwait Institute for Scientific Research: Kuwait), PEREZ, A.R., PUGA, R, AND VENTA, G. 1984b Studies on the recruitment and stock recruitment relations in the Cuban Shrimp population. 163- 206, In C.P. Mathews (ed.) ‘Proceedings of the shrimp and fin fish fisheries management work- shop’, Vol 1, KISR 1366/MB-14. (Kuwait Insti- tute for Scientific Research; Kuwait). PEREZ FARFANTE, I. 1969. Western Atlantic shrimps of the genus Penaeus, Fishery Bulletin of the United States 67: 461-591. PYEN, C.K. 1974, Studies on the spawning seuson of Penaeus japonicus Bate in the Geaje Do area, Bulletin of the Fisheries Research Development Agency, Pusan 13: 39-36. ROTHLISBERG, P.C.. CHURCH, J.A. AND FORBES, A.M.G. 1983. Modelling the advec- MEMOIRS OF THE QUEENSLAND MUSEUM tion of vertically migrating shrimp larvae. Jour nal of Marine Research 41: 511-538, ROTHLISBERG, P.C., STAPLES, D.J. AND CRO- COS, PJ. 1985, A review of the life history of the banana prawn, Penaeus merguiensis in the Gulf of Carpentaria, 125-136. In P.C, Roth- lisberg, B.J, Hill and DJ. Staples (eds) ‘Second Australian national prawn seminar’, NPS2, (Cleveland: Australia). RUELLO, N.V. 1975. Geographical distribution, growth and breeding migration of the eastern Australian king prawn Penaeus plebejus. Australian Journal of Marine and Freshwater Research 26: 343-354. SOMERS, LF. 1987. Sediment type as a factor in the distribution of the commercial prawn species of the western Gulf of Carpentaria. Australian Jour- nalof Marine and Freshwater Research 38: 133- 149, STAPLES, DJ, 1979. Seasonal migration patterns of postlarval and juvenile banana prawns, Penaeus merguiensis dé Man, in the major rivers of the Gulf of Carpentaria. Australian Journal of Marine and Freshwater Research 31; 635-652, STAPLES, DJ. AND ROTHLISBERG, P,C. 1990, Recruitment of penseid prawns in the Indo-west Pacific. 847-850. In R. Hirano, and H, Isao (eds) ‘The Proceedings of the second Asian lisheries forum.’ Asian Fisheries Society, Tokyo, Japan. (The Asian Fisheries Society: Manila, Philip- pines). STAPLES, D.J, AND VANCE, D.J. 1986. Emigration of juvenile banana prawns Penaeus merguiensts from mangrove estuary and recruitment to offshore areas in the wet-dry tropics of the Gull of Carpentaria, Australia, Marine Ecology Pro- gress Series 27; 239-252. TEMPLE, R.F. AND FISCHER, C.C. 1967. Seasonal distribution and relative abundance of planktonic-stage shrimp (Penacus spp.) in the northwestern Gulf of Mexico, 1961. Fishery Bulletin of the United States 60; 323-334. TOM. M. AND LEWINSOHN, C, 1983. Aspects of the benthic life cycle of Penaeus (melicertus) Japonicus Bate (Crustacea Decapoda) along the southeastern coast of the Mediterranean. Fisher- ies Research 2: 89-101. VANCE, D.J.. HAYWOOD, M.D.E. AND STAPLES, DJ, 1990. Use of a mangrove estu- ary aS a nursery area by postlarval and juvenile banana prawns, Peneaus merguiensis de Man, in northern Australia, Estuarine, Coastal and Shelf Science 31; 689-701. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum SPATIAL AND TEMPORAL PATTERNS IN RECRUITMENT FOR AMERICAN LOBSTER, HOMARUS AMERICANUS. IN THE NORTHWESTERN ATLANTIC ROBERT W. ELNER AND ALAN CAMPBELL Elner, R.W. and Campbell, A, 1991 09 01; Spatial and temporal patterns in recruitment for American lobster, Homarus americanus. in the northwestern Atlantic. Memoirs of the Queensland Museum 31: 349-363. Brisbane. ISSN G0N79-8835. The labster. Homarus americanns, is a long-lived crustacean that has been heavily exploited along the northeast coast of North America for over 100 years. Catches revived markedly in many lobster fisheries during the 1980s after prolonged declines trom peaks al the turn of this century. Because of high exploitation rates, the increased yields are assumed to reflect real changes in lobster abundance, although there is no consensus on why recruitment should have improved, Geographic comparisons of time series of landings.. larval surveys and oceanography have indicated tentative stock boundaries bul there is little understanding of stock-recruitment relationships. To-date, none of the numerous biotic and ahiotic factors that have been hypothesized as controlling lobster recruitment have proven reliable for forecasting yields. Work on the behavioural ecology ofthe eryptic early benthie stuges has invoked various density-dependent mechanisms as population controls in local ateas; however, these mechanisms may nol account for larger-scale recruiiment events. Changes in climate, and Jo a lesser extent. reduced exploitation rates in the last 20 years may have caused a general increase in recruitment, producing yields to match historic highs in same Jobster fisheries. There are implications for both tradtiional fisheries models and management if lobster stocks are dominuled by ‘supply-side’ recruitment dynamics under the control of an unpredictable climatic phenomenon. C1) Lobster, life history, fishery, density-dependence, recruitment mechanisms, research approach. Robert W. Elner, Biological Sciences Branch, Department of Fisheries & Oceans, P.O. Box 550, Halifax, Nova Scotia, B31 287, Canada; Alan Campbell, Biological Sciences Branch, Pacific Biological Station, Department of Fisheries & Oceans, Nanaimo, British Columbia, V9R 5K6, Canada; 6 July, 1990. The American lobster, Homarus america- nus, is the latgest and most abundant species of ‘true’ or clawed lobster (Nephropoidea). Some specimens have been reported to achieve a live weight over 19 kg (Wolff, 1978). The species has a largely boreal dis- tribution along the northeastern coast of North America, from the Strait of Belle Isle through the Gulf of St, Lawrence, and the Gulf of Maine to Wilmington, North Carolina (Williams, 1984). The Gulf Stream around Cape Hatteras, North Carolina ap- pears. to present a thermal barrier at the southern limit (Fig. 1). The total range of the species extends over 15 degrees of latitude. Lobster (Note: throughout the text lobster refers to the American lobster, H. amer/- canus, unless indicated otherwise) usually occur within 20-25 km of the coast at depths shallower than 50 m; however, populations exist on the continental shelf and offshore banks, extending to depths of over 700 m in the canyons of the continental slope. Before commercial exploitation began, American lobster was common even in inter- tidal areas and collected for food by Indians and, later by the early European settlers. Lobster was so abundant it was reportedly used for agricultural fertilizer (DeWolf, 1974). Lobster fisheries have been of major economic and cultural importance for over one hundred years, Commercial harvesting started in Massachusetts in the early 1800s and had reached Maine by 1840 (Herrick, 1911). Lobster fishing in Canadian waters expanded rapidly after the introduction of canneries ta Nova Scotia in 1851, Lobster landings began in Quebec in 1871, New- foundland in 1874 and the Magdelen Islands in 18735; the Canadian fishery was con- sidered to be fully developed by the 1890s (Robinson, 1980; Pringle e al., 1983). Monitoring and regulation of the various lobster fisheries began as early as 1873, bi- ological research soon after (Herrick, 1896). Although American lobster appears one of 50 45 40 35 30 350 Canada 65 MEMOIRS OF THE QUEENSLAND MUSEUM Gulf Stream ATLANTIC OCEAN 60 55 50 45 FIG. 1. The geographical distribution of American lobster, Homarus americanus (shaded) along the coast of North America; note, major fishing areas (black), the most intensively studied and popularly rec- ognized marine crustaceans there remain large gaps in understanding of its life history and the ecological mechanisms controlling abundance. Consequently, powers to predict recruitment are limited, and determining the consequences of fish- eries management initiatives is problematic. The pre- sent paper reviews the biological basis to recruitment, the development of the commercial fishery and postulated recruitment mechanisms. Progress in describing lobster life history dynamics and un- derstanding the factors that influence recruitment patterns is argued to have been hindered by the lack of an effective postlarval collector, long-term data sets on oceanographic events and the overall scientific approach. RECRUITMENT PATTERNS FOR HOMARL'S BIOLOGICAL BASIS TO RECRUITMENT A female lobstercarnies between 7,000 10 97.000 eggs, depending on body size and origin, un her abdominal pleopods for 9-12 months. Brooding time is strongly related to temperature (Tem- pleman, 1940a; Perkins, 1972). Ovigerous females undertake seasonal depth migrations that appear associated With maximizing degree days needed for egg development: hatching eggs in relatively shallow, warm waler increases survivorship of larvae by decreasing develop- ment time to the benthic stage (Campbell, |Y86a. 1990a, Campbell and Stasko, 1986). The cggs hatch during summer (July — September) and the four stages of free-living pelagic larvae remain in the water column for I-2 months. depending. on temperature (Templeman, 1940b), Stage [V larvae become benthic in late summer, settling into preferred substrates such as gravel (Cobb, 1971, 1977; Cobb er al,, 1983, 198¥), Mortality during the larval stages is probably high, due to predators, starvation and physical factors (Scar- ratt, 1964, 1973; Caddy, 1979; Harding ev ail., 1982). Early postlarvae are cryptic and burrow into preferred substrates where they are less sus- ceptible to predation and may filler feed (Poitle and Elner, 1982; Lavalli and Barshaw, 1986, 1989: Barshaw and Lavalli, 1988), There is un- certainty whether the few inshore sctilement sites that have been discovered should be con- sidered ‘nurseries’ (areas preferentially selected for settlement) per se or merely areas with ap- propriate bottom characteristics where postlar- val survival and, hence, density, is higher than other settlement sites, Lobster above approxi- mately 40 mm carapace length (C,L,) frequently forage outside their burrows, roaming progres- sively further afield as they become larger and mature (Lawton, 1987). However, substrate characteristics, particularly size and availability of shelters, continues to strongly influence lob- ster distribution and abundance (Scarratl, 1968; Cobb, 1971; Cobb er al., 1986, Hudon, 1987). Recruitment-related variables such as growth rate, size at maturity and spawning charac- teristics vary with environmental conditions, no- tably temperature (Aiken and Waddy, 1986). Lobster attain the current legal minimum size, for most grounds around Nova Scotia, of 81 mm C.L, after five to eight years. In some areas, such as the Gulf of St. Lawrence, ‘canner’ lobsters of 64 mm C.L are fished and recruitment into the fishery may occur at an even earlier age. In addition, summer temperatures over much of the 35] southern Gulf of St. Lawrence may be suffi- cienUy high to permit two moults per year, iN- stead of the usual one, for newly recruited lobster. Offshore lobster also grow relatively fast, allaiming fishable size after 4—5 years, as compared to the 7-12 years required for those on some nearshore grounds (Cooper, 1977), Mast lobster reach fishable size before attaining sexual maturity (Ennis, 1986; Cobb and Wang, 1985), Although tagging and laboratory studies have provided extensive information on moult- ing and growth for immature and early adult stages (Milleret a/., 1989), estimating the age of alder adulls is problematic, as the intermoulc period becomes longer and less predictable after the onset of maturity, Aging is further compli- culed because mature females can delay moult- ing in order to extrude a further batch of eges (Waddy and Aiken, 1986). There is no consensus on the natural life-span for lobster. Cooper and Uzmann (1977) com- puted a yon Bertalanffy growth equation, using Ly values of 270 mm C.L, (males) and 240 mm C.L. (females), that provided maximum esti- mates of }00 years for offshore specimens. Esti- mates by Campbell (1983a) suggest more rapid growth whereby males and females reach 200 mm C.L. in 20 and 30 years, respectively, For American lobster, as for most marine in- vertebrales, critical linkages between oceano- graphy and larval life-histary phases are lacking, and the existence of a stock-recruitment relation- ship is largely a matter of faith (Cobb and Wang, 1985). Sources of recruitment and larval mixing are only superficially’ understood, and con- sequently so are mechanisms for variability in recruitment patterns, Development of predictive models hus been slow. Studies in the Northum- berland Strait (Scarratt 1964, 1973) have failed {o. demonstrate «correlation between abundance of stage T lobster larvae and the parent stock or 4 predictive relationship between the production of stage 1V larvae and subsequent recruitment into the fishery (but see Fogarty and Idoine (1986) for a re-evaluation). However, Campbell (1990b) derived a prerecruit abundance index from commercial raps 10 predict recruitment for lobster grounds off southwestern Nova Scotia !—2 years later. For the purposes of this paper, a stock is de- fined as ‘a population of organisms which, shar- ing a common gene pool, is sufficiently distinct tO Warrant consideration as a self-perpelnating system that can be managed’ (Larkin, 1972), We define recruiiment broadly as survival ftom same earlier life-history stage to the minimum legal size for {he commercial fishery, The eon- (inuity of the stock in time and space depends on the larvae or @ later life-history phase returning to the brood urca to complete the genetic cycle, Ege hatching locations are often far from habi- tats favorable to juveniles, which, in turn, may differ from areas preferred by adults. Ifa species hus not evulved a reproductive strategy that re- turns recruits to the fishing grounds regularly, the stability of the stock cannot be assumed and ii will be practically impossible to predict re- eruiment, The delineation of stacks and the mechanics of stock-recruitment relationships are problems fundamental to fisheries science. Presumably if stocks can be identified, effective management regimes can be imposed to optimise exploitation of the resource, Ennis (1986) detailed five re- quirements for determining a stock-recruitment relationship: 1, 4 population that is more or less discrete, both geographically and biologically (i.e, 4 stack); 2. measure of stock size over a time period when abundance ranged widely; 3, measure of recruitment to the stock which coincides with the same time period, 4. understanding of the effect of variation im tactors-other than stack size on recrutiment var- iability; and, 5, understanding of recruitment processes lor the stock, Although components of all five have been studied for A. americanus there has been no concerted allempt lo integrate results and re-de- fing management areas. Campbell and Mohn (1983) examined historical catch data from the Canadian Maritime Provinces and Maine and defined broad geographic population boundaries for Jobster on the basis of coherence in temporal trends in landings over several decades. A simi- lar exercise performed by Harding eral, (1953) suggested the same major groupings, Although morphometric studies have indicated some segregation of inshore and offshore lobster (Saila and Flowers, 1969) the movement pat- terns of mature lobster and the propensity for larval exchange suggest that genetic mixing ac- curs al least within the Gulf of Maing system (Campbell and Stasko, 1985, 1986). To date. attempts to delineate lobster stocks on the basis of parasites (Uzmann, 1970; Boghen, 1978; Stewart, 1980; Brattey and Campbell, 1486) have had only hmited success. Protein electro- MEMOIRS OF THE QUEENSLAND MUSEUM phoresis indicates that Armenean lobster tren various areas are genetically similar, with the exception of a single enzyme thal allows dis- crimination between lobsters from Prince Ed- ward Island and south of Cape Cod (Tracey et al., 1975), Mark-recapture studies in Canada (Miller et al., 1989) have shown that while immature com- mercial-sized lobster travel only short distances (Campbell, 1982), mature lobsters undertake ex- tensive movements (> 100 km) and tend to return to the location where they were initially marked (Pezzack and Duggan, 1986; Campbell, 1986a). This homing behaviour may involve atound trip movement of up to 400 km in one year (Camp- bell, 1989), In addition, short, seasonal inshore- offshore, or shallow-deep, migrations have been noted in the Gulf of Maine, on Georges Bank and off the Magdelen fslands (Saila and Flowers, 1968; Dow, 1974; Cooper and Uzmann, L980; Krouse, 1980; Campbell and Stasko, 1986). The movements appear associated with maintaining maximum local temperatures (Cooper and Uz- mann, 1971; Campbell and Stasko, 1986), In comparison, tagging studies Off eastern Nova Scotia, around Newfoundland and, generally, in the Gulf of St. Lawrence have revealed only small-scale movements (< 15 km) (Ennis, 1984), Movement patterns for lobster larvae are poorly known and investigators have usually related Jarval pathways to residual surface cur- rents. Various allempts have been made to cluci- date larval sources for the Nova Scotian Atlantic coast and the rich inshore fishing grounds off southwestern Nova Scotia. While Stasko (L978) hypothesised that Browns Bank was the source of larvae for southwestern Nova Scotia, Harding et al. (1983) suggested the larvae originate from Georges Bank (but see also Harding and Trites, 1488, 1989; Pezzack, 1989), Dadswell (1979), on the assumption thal circular currents relain larvae within an area while longitudinal currents carry larvae away, proposed thal there are six lobster-reeruitment cells for the Canadian Man- times. More recent work has shown that lobster larvae exhibit pronounced diurnal vertical mi- gration behaviour and should not necessarily be considered passive surface drifters (Harding er al,, 1987), If lobster larvae resemble other de- capod larvae, this behaviour may maintain their position (Sulkin, 1986). Lobster larvae were col- lected only at the surface and only with onshore winds during a study in a nearshore area off Newloundland, also suggesting thal a nearshore Teléntion mechanism exists (Ennis, 1983), RECRUITMENT PATTERNS FOR HOMARUS THE FISHERY For over 100 years, American lobster have been predominantly caught by traps, both in Canada and the U,S.A.. Prior to the late 1860s lobster were captured by a variety of methods including hooks, spears and hoop nets (DeWollf, 1974; Dow, 1980). The majority of offshore fisheries use large traps but in some offshore areas of the U.S.A. otter trawling has occasion- ally supplemented trapping (Dow, 1980; Fogarty ef al., 1982; Pezzack and Duggan, 1983). The various inshore and offshore lobster fisheries are partitioned into management areas based on socideconomic considerations rather than bio- logical criteria (Dow, 1980; Pringle er al., 1983; Campbell, 1989). Depending on the area in- volved, conservative management of these lob- ster fisheries has included a combination of regulations : minimum and maximum sizes, pro- tection of ovigerous females, effort restrictions through license and trap limitations. and season openings and closures, plus quota restrictions for the offshore fishery (Dow, 1980; Fogarty e7 al., 1982; Pezzack and Duggan, 1983; Pringle e7 a/., 1983; Campbell, 1986b, 1989), Without ade- quate empirical stock-recruitment data deter- mining whether these regulations have been effective conservation tools is impossible. Historically, landings have fluctuated consid- 70000 60000 50000 40000 30000 20000 Total Landings (mt) 1860 1880 1900 ©1920 353 erably (Fig. 2) but in recent years they have generally risen for most areas (Fig. 3). Total North American landings exceeded 60,000 t (Ennis, 1956) and Canadian lobster landings reached over 45,000 t per annum in the last century. Record lows in the 1960s and 1970s have been followed by all time highs in the 1980s; total Canadian lobster landings doubled between 1977 and 1986 and in some areas rose by an order of magnitude. The main reason for the rise. appears to be an increase in the absolute abundance of lobster (Miller et al., 1987). Al- though there has been some increased fishing effort and expansion to new grounds, catch rates have also increased, In addition, management measures, including more stringent enforcement of regulations and a reduction in the number of licenses, have helped sustain the recovery in Canada. Historical fishing effort trends are not as well known as landings for the American lobster. Fishing effort can fluctuate with many factors such as market demand (Dow, 1980) and in- creases in fishing gear efficiency; also, trapabil- ity can vary from location to location depending on lobster activity and physiological condition (McLeese and Wilder, 1958; Elner, 1980), How- ever, because effort is high (currently, there are about [0,000 licensed Jobster vessels in Canada and exploitation rates have been estimated at TOTAL CANADA USA 1940 §=1960 1980 §=2000 YEAR FIG, 2, Annual landings of American lobster for Canada and the U.S.A., 1870-1989. 354 Maine 12000 10000 Ce E = = z Ey = 6000 z 4 4 z z = 4000 S 2000 1880 1900 1920 194 1960 1980 2000 YEAR Prince Edward Island 10000 8000 z = a & 3 6000 3 4 E 2am : 2000 1880 1900 1920 too 1960 1980 2000 YEAR MEMOIRS OF THE QUEENSLAND MUSEUM Nova Scotia 30000 2000) 10000 1980) 1900) 1920 1940 1960) 1980 2000 YEAR Newfoundland B00 6000 4000 2004), 1880 1900 120 1940 1964) 1980 2000 FIG. 3. Annual landings of American lobster for Maine, Nova Scotia, Prince Edward Island and Newfoundland, from the late 1880s—1989. 60-90% (Anthony, 1980; Campbell. 1980; Miller ef al., 1987)) catches mainly comprise lobster that are newly-recruited to commercial size and the assumption is that landings are a reliable indication of the total fishable biomass. Therefore, major fluctuations in recruitment (lobster molting into the fishery) will be re- flected in the landing trends. Recent increases in exploitation of large mature lobster, an impor- tant source of recruits, concurrent with high ex- ploitation of newly recruited lobster in the inshore fishery has caused concern that the amplitude of landing fluctuations could increase until recruitment failure occurs (Campbell, 1989), RECRUITMENT MECHANISMS Throughout their extensive geographical dis- tribution American lobster are found in a diverse array of habitats, from the intertidal zone to a variety of coastal sublittoral habitats to the cany- ons of the continental slope (Cooper and Uz- mann, 1977). Because physical and biological factors vary widely (e.g. temperature can be from 0°C to 25°C) their influence on recruitment will change in time and space (Aiken and Waddy,. 1986); thus, understanding recruitment mechanisms is a challenging task. After a cen- tury of research fundamental factors such as the relationships between the seasonal movements of adult lobster, distribution of broad stack, lar- val recruitment processes and oceanographic features are still unclear. The numerous attempts to explain fluctuations in lobster abundance have included factors and mechanisms such as: — Temperature variation (Flowers and Saila, 1972; Dow, 1977; Fogarty, 1988) which acts strongly to regulate activity and trapability of commercial-sized lobster (McLeese and Wilder, 1958) and the growth rates of all life-history stages. The probability of moulting is strongly temperature related and the proportion of lobster that moult can decrease by nearly 50% in cold years (Campbell, 1983b). — Freshwater river discharge (Sutcliffe, 1973) which influences food production and, hence, larval survival. Other workers (Sheldon et al., 1982) suggest that increased discharge intensi- RECRUITMENT PATTERNS FOR [fOMARUS fies stratification, causing higher heat retention, faster larval development and improved survival. — Excessive exploitation rates, which reduce eggs per fecrult (Robinson, 1979, Campbell and Robinson, 1983) causing recruitment lailures and declines in landings, Egg predators (Campbell and Brattey. 1986; Fogarty and Idoine, 19) and an- thropogenic factors (Aiken and Waddy, 1986) have also been hypothesised as reducing egys per recruil, — Ecosystem productivity changes (Wharton and Mann, 1981) and competition with sea urchins for space (Garnick, 1989) which affect recruitment. We do not intend to account forall the hypothe- ses that have arisen (Ennis, 1986), but rather de- scribe the general history and progress of research to elucidate. lobster recruitment patterns, In the 1970s, during the period of collapsed lobster landings along the Atlantic coust of Nova Scotia, workers suggested several causes for the slump: tecruit overfishing (Robinson, 1479), ecosystem deterioration due to a populatian ex- plosion of sea urchins triggered by overfishing lobster (Wharton and Mann, 1981) and closing (he Strait of Canso blocking an important source of larvae (Dadswell, 1979). Subsequently, the recruitment failure was attributed by Harding e/ al, (1983) to all three scenarios: excessive fish- ing of immature lobster between the 1890s and 1920 depleted the breeding stock and caused the initial decline in landings; climatic cooling and the closure of the Straitof Canso further reduced lobster stocks and, in the absence of predation by lobster, destructive grazing of macroalgal beds by sea urchins reduced the carrying capacity of the environment for lobster. None of these ex- planations was subjected to thorough scientific testing and cach had its proponents and critics (McCracken, 1979; Pringle et al, 1982; Elner ing Vadas, 1990), Meanwhile, apart from reduc- ing the number of licensed vessels. fisheries managers took little action and, from either iner- tia or their conservative nature, Were still con- sidering the situation when landings started to recover during the early 1980s, The sea urchins suffered mass mortality from disease and mac- roalgal beds recovered while landings increased (Miller and Colodey, 1983; Miller, [985a: Scheibling and Raymond, 1990). The cause of the upturn is as enigmatic as explanations lor the decline, especially with respect 10 the role of macroalpae, However, no reliable evidence links labster production to macroalgac (Miller, 1985b; Elner and Campbell, 1987). Indeed, lobsters re- sponsible for {he increased landings in the early- hay LA LF to-mid 1980s spent their pre-recruit years during the mid-t970s on the urchin barrens, The appear- ance and virulence of the sea urchin pathogen in 1980 has been linked to unusually warm seu- water temperatures (Scheibling and Stephenson, 1484; Miller, 1985a; Margosian et a/,, 1987). Possibly urchin die-offs and revived lobster landings are caused by the same environmental factor(s) (Fig. 4), The dramatic turnabout in the lobster fishery during the 1980s was a surprise given the argu- ments that inshore stocks should, in theory, have been exhausted by the high exploitation rates and Jow survival tu maturity, Only the existence of refugia for reproductive lobster was thought fo prevent collapses in many arcas (Anthony and Caody, 1980), To-date, only two hypotheses have been advanced for the recruitment pulse ; 1) a large-scale climatic change; and 2) a decrease in fishing mortality during the 1970s, However. there has been no testing of postulated mechanisms. More recent studies have concen- trated on larval transport problems (Hudon et af,, 1986; Harding and Trites, 1988, 1989) and the ecology of early benthic stages (Hudon, 1987; Hudon and Lararche, 1989). The current debate centers partly on the behavioural ecology of the cryptic early benthic stages and possible density- dependent cantrols in Jacal areas. Various mech. anisms linking lobster larval settlement and subsequent recruitment mio the fishery have been postulated (Aiken and Waddy, 1986). Several authors have stressed the importance of protective habital availability for juveniles to lobster population dynamics (Cobb ee al,, 1986; Fogarty and Idoine, 1986, Garnick, 1989). Thus, limited suitable bottom may Be a ‘bottleneck’ that stabilises and strengthens the resilience of the fishable stock. bul, also, hmits recruitment into the fishery. A similar scenario has heen advocated for settling larvae of Norway lobster, Nephrops norvegicus (Hill and White, 1990), Fogarty and Idoine (1986) applied their argu- ments on shelter-mediated, density-dependent regulation of prerecruit lobster to ecological theary for ammals with complex life cycles (Wilbur, (980). American lobster may be can sidered K-seclected strategists (life-history char- acterised try low [ecundily, large egy size, parental investment in brooding eggs, repeat spawning insuecessive seasons, large body size, late sexual mamurity, and longevity) which typi- cally have low recruitment variability and gre adapted for exploiting physically stable environ- meats coutralled Jargely by density-dependent t La > St Andrews " i % * t ; V $s 1900 10 in 196 tone 2900 a a Halifax Dy i 5 1 = . - = = = i { Po L i 3 E = 10H) wa joai 1960 190 2000 = = = Noothbay tarhour 12 n 0 9 a 7 a 5 1900) i920 wo 18H) 7980 2000 YEAR FIG. 4. Mean annual sea surface temperature profiles for St, Andrews, New Brunswick; Halifax, Nova Scotia; and Boothbay Harbor, Maine; note gener- ally elevated values in late 1970s/ early 1980s. forces (Barnes and Hughes. 1982). In contrast, other crustaceans such as shrimp with small bo- dies, rapid growth, early sexual maturity and high fecundity are opportunistic, r-selected, or- ganisms adapted to physically unstable environ- ments and subject to wide fluctuations in recruitment. Applying Wilbur’s (1980), criteria, the American lobster could be classified by ‘Density-Dependent Regulation Only During the Larval Stage’. Theoretically, the adult popu- lation varies with the productivity of the larval habitat (substitute early-stage, benthic, juveniles in the case of lobster), and if adults are long- lived, the age structure would reflect the relative ‘larval’ success of recent year classes. However. while such theory may have been suilable for guiding research on lobster recruitment mecha- nisms in the 1970s, the current improved recruit- ment trend is more reminiscent of an t-selected MEMOIRS OF THE QUEENSLAND MUSEUM strategist, and accepted life-history theory up- pears to have little application. Rather, the scenario seems akin to the current ‘supply-side’ paradigm where recruitment levels can change internal controls normally operating within a system (Gaines and Roughgarden, 1985; Lewin, 1986: Underwood and Fairweather, 1989), American lobster yields have always been geographically variable, Although landings im- proved in all fishing areas during the 1980s, yields from some increased far more than in the traditionally stable areas off Maine and New- foundland (Fig. 3). Pezzack (in press) distin- guished areas stable between 1947-1986, including Maine, Newfoundland, Grand Manan, southwestern Nova Scotia, the Gulf of St. La- wrence, Quebec, northeastern Cape Breton and Massachusetts. The areas which have exhibited Wide fluctuations in landings are the eastern shore of Nova Scotia and southeastern Cape Breton. Lobster fishing grounds along the Atlan- tic-coastof Nova Scotia have displayed differing degrees of response to the improved recruitment of the 1980s (Fig. 5). Inter-ground stability differences could be due to differences in conti- nental shelf area, which effect retention of larvae and substrate and food availability for juveniles, as well as physical environment. DISCUSSION Although a fundamental appreciation of the American lobster’s life history was achieved early in this century with classic studies by Her- rick (1896, 1911) and Hadley (1906, 1908) the subsequent history of research into stock-recruit- ment relationships has been somewhat ad hac, apparently suffering from a lack of a concerted approach, Research thrusts seem to have changed opportunistically with ecological fads (Abrahamson e7 al., 1989) rather than doggedly addressing fundamental questions until they were solved. Work during the 1940s and 1950s focussed mainly on growth and movement of lobster that had already recruited into the fishery in an effort to prevent growth overfishing (Wilder, 1947, 1948, 1958). During the 1960s to mid-1970s there were various attempts both to identify stocks (Saila and Flowers, 1969; Barlow and Ridgeway, 1971; Cooper and Uzmann, 1971; Tracey et al., 1975) and to explain trends in landings through environmental influences such as temperature (Dow, 1961) and river dis- charge (Sutcliffe, 1973). Lobster research from the mid-1970s to early 1980s was influenced by RECRUITMENT PATTERNS FOR HOMARUS Shelburne Co., N.5. =o = 3 3000 £ u & 2000 a a = 000 0 \BB0 «6900 «1920s 1940 960 198G0)~=—- 2000 Lunenburg Co. N.5. 2000 = oc < = 1000 c s sg o pz 0 1680 1906 1920 1940 Year 1960 1960 2000 357 Yarmouth Co,, NS. 5000 4000 3000 2000 foo0 0 1850 1900 1920 1940 1960 1960 2000 Guysborough Co.,.N.S. Jono 2000 1000 Oo 1a8o 1900 1920 \940 1960 1980 2000 Year FIG. 5. Annual landings of American lobster for representative historically stable (Shelburne County. Yarmouth County) and collapsed (Lunenburg County, Guysborough County) fishing grounds along the Atlantic coast of Nova Scotia, to illustrate various degrees of response lo the general increase in yield during the 1980s; for geographic areas that have remained more stable throughout see profiles for Maine and Newfoundland (Fig. 3). vigorous arguments over the impact af the cause- way across the Strait of Canso (McCracken. 1979) and the ecological implications of destruc- tive grazing by sea urchins (Elner and Vadas, 1990). The controversy subsided without clear resolution as Jandings recovered, and the empha- sis of research changed again. Recent investiga- tions focus on larval transport and the movement of adult lobsters although work on the population ecology of early life-history stages has con- tinued. While the numerous studies on H. amer- icanus over the past century provide a valuable general understanding, they reach no consensus on the major factors influencing recruitment. The recent recruitment pulse and major in- crease in landings in Canada started around 1981 and has unshackled both the Sutcliffe model correlating Quebec lobster landings and river tun-off (Drinkwater ef a/., in press) and stock discrimination based on historical landings pat- terns (Campbell and Mohn, 1983). We believe that the causitive mechanism(s) must be very powerful to have effected virtually all lobster fisheries. Landings increased more or Jess in unison throughout coastal Nova Scotia and the southern Gulf of St. Lawrence, but in varying degrees in local areas, suggesting that large en- vironmental force(s) may have acted during the same general time period to influence recruit- ment. The various density-dependent mechanisms invoked as population controls of the cryptic early benthic stages of lobster in local areas are un- likely to aecount for large-scale recruitment events. Changes in climate coupled, perhaps, with decreased exploitation rates in the last 20 years are a more probable cause. We speculate that larval and early juvenile survival was en- hanced during several years in the late 1970s-to- carly-1980s through increased growth and food availability probably due to an increase in water temperature (Fig, 4). Also, low fishing mortality in some areas during the late 1970s could have allowed more females to produce eggs and the increased number of eggs per recruit may have swollen recruitment into the fishery 5-8 yr later (Campbell, 1990b). Subsequently differential in- dividual growth rates spread this cohort into the fishery over several years, resulting in 3-5 years of record landings. Coupled with increased lob- ster abundance, fishing effort.and total mortality of lobster increased dramatically tm sume areas (Campbell, 1990b). ‘Supply-side’ lobster recruitment controlled by an unpredictable climatic phenomenon has profound implications for fisheries manage- ment. Most management initiatives are based on the understanding thal fishing mortality can have a strong impact on annual recruitment and that regulation of fishing pressure can preempt re- cruitment problems, If, as the events with lobster in the northwestern Atlantic over the past 10 years suggest, recruitment can be independent of fishing pressure then proactive management be- comes essentially impotent, with managers only being able to react to changes in stock abundance as they occur. The situation would make recruit- ment predictions largely dependent on under- standing and forecasting the causative environmental mechanism(s). Traditional fish- eries models based on concepts such as surplus production and stable recruitment would be largely redundant. While much is known about the biology of American lobster a conspicuous inability to un- derstand recruitment remains compared to the successes achieved for the western rock lobster, Panulirus cygnus (Caputi and Brown, [986: Phillips, 1986), Progress appears to have been hindere’d by three factors. First. the numerous attempts to develop a passive collector to inter- cept and index the recruitment strength of Amer- ican lobster postlarvae at settlement have all failed. Instead, trial collector designs have succecded in capturing early benthic stages of ihe commercial rock crab, Cancer ifroratus (Beninger et al., 19&6). Second, comprehensive long-term data sels on oceanographic events (other than sea surface temperature and river discharge), prerequisites to exploratory correla- tion analysis. and effective generation of hy- potheses on physical controls on lobster recruitment, have not been available. Thirdly, the overall scientific approach appears to lack rigor, Although numerous explanations for re- cruitment patterns in American lobster have been advanced there has been little actual experi- mental lesting of actual hypotheses and no con- certed attempt to sequentially advance by ‘strong inference’ (Elner and Vadas, 1990), We believe that only by effectively addressing these three luctors together can a realistic model of a bio- logical lobster stock, integrating physical and oceanographic parameters with the complete life-cycle and ecology in a defined area through lime, be achieved, Such a model of the whole MEMOIRS OF THE QUEENSLAND MUSEUM system 18 required before the various system components can be viewed in context, their rela- tive influences explored, and predictive models developed. ACKNOWLEDGEMENTS R.W.E. is grateful to the organisers of the International Crustacean Conference for finan- cial support in presenting this paper. We thank D. J. Noakes and M, D. 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AND WANG, D, 1985, Fisheries biology of lobster and crayfishes, 167-247. In D.E, Bliss (ed.) ‘The biology of Crustacea’, Vol X. (Aca- demic Press: New York). COBB, JS, , WANG, D, RICHARDS, R.A. AND FOGARTY, M.J. 1986. Competition among lohsters and crabs and its possible effects in Narragansett! Bay, Rhode Island, Canadian Special Publication of Fisheries and Aquatic Sciences 92: 282-290. COBB, J.S, WANG, D. AND CAMPBELL, D.B. 1989, Timing of settlement by postlarval lob- sters (Homarus americanus): tield and labora- tory evidence. Journal of Crustacean Biology 9: 6(-66, COOPER, R.A. 1977. Growth of deep water Ameri- can lobsters (Homarus americanus) from the 360) New England Continental Shelf, Common- wealth Scientific and Industrial Research Or- ganization, Division of Fisheries and Oceanography, Circular 7: 35. COOPER. R.A. AND UZMANN, JR. 1971- Migra- tion and growth of deep-sea lobsters, Homarus americanus, Science, New York 171: 288-290, 1977, Ecology of juvenile and adult clawed lobsters Homarus americanus, Homarus gamunarus, and Nephrops norvegicus, Commonwealth Scientific and Industrial Research Organization, Division of Fisheries and Oceanography, Circular 7: 187-208. 1980. Ecology of adult and juvenile Homarus, 97- 142. In J. S. Cobb and B. F, Phillips (eds) ' The biology and management of lobsters’. Vol.2. (Academic Press: New York). DADSWELL, M-J. 1979. A review of the decline in lobster (Homarus americanus) landings in Chedabucto Bay between 1956 and 1977 with an hypothesis for a passible effect by the Canso Causeway on the recruitment mechanism of eastern Nova Scotia lobster stocks. Fisheries Marine Service Technical Repori 834(3): 113- 144, DEWOLF, A.G,. 1974. The lobster fishery of the mari- lime provinces: Economic effects of regula- tions, Bulletin of the Fisheries Research Bourd of Canada 187. DOW, R.L. 1961, Some factors influencing Maine lobster landings. Commercial Fisheries Review 23: 1-11, 1974, American lobsters lagged by Maine commer- cial fishermen, 1957-1959. Fisheries Bulletin 72: 622-623. 1977, Relationship of sea surface temperature to Amencan and European lobster landings, Jour- nal for the International Council Exploration of the Seas 37; 186-190. 1980. The clawed lobster fisheries, 265-316. In J.S. Cobb and B.F. Phillips (eds) ~The biology and management of lobsiers”. Vol. 2,(Acadentic Press: New York). DRINKWATER, K.F., HARDING, G.C., VASS, W.P, AND. GAUTHIER, D. IN PRESS, A study of environmental influences on the Quehec lpb- ster fishery, Canadian Journal of Fisheries and Aquatic Sciences, ELNER, R.W. 1980. Lobster gear selectivity — a Canadian overview. Canadian Technical Report of Fisheries and Aquatic Sciences 932; 77-83, ELNER, R.W. AND CAMPBELL, A. 1987. Natural diets of lobster Hamurus americanus (rom bar ren ground and macroalgal habitats off south- westemm Nova Scotia, Canada. Marine Ecology Progress Series 37: 131-140. MEMOIRS OF THE QUEENSLAND MUSEUM ELNER, R.W, AND VADAS, R. L. 1990. Inference in ecology: the sea urchin phenomenon in the Northwestern Atlantic. American Naturalist 136; 108-125, ENNIS, G.P, 1983, Annual variations in standing stock ina Newfoundland population of lobsters. North American Journal of Fisheries Manage- ment 3: 26-33, 1984. Small-scale movements of the American lob- ster Homarus americanus. Transactions of the American Fisheries Society 113; 336-338. 1986. Stock definition, recruitment variability, and larval recruitment processes in the American lobsier, Homarus americanus, A review. Canadian Journal of Fisheries and Aquatic Sciences 43: 2072-2084, FLOWERS, J.M. AND SAILA, S.B, 1972. An analy- sis of temperature effects on the inshore lobster fishery. Journal of the Fisheries Research Board of Canada 29; 122[-1225, FOGARTY, M.J. 1988. Time series models of the Maine lobster fishery: The effect of temperature. Canadian Journal of Fisheries and Aquatic Sciences 45; 1145-1153. FOGARTY, MJ. AND [DOINE, J.S. 1986. Recruit- ment dynamics in an American lobster (J/o- marus americanus) population. Canadian Journal of Fisheries and Aquatic Sciences 43: 2368-2376. FOGARTY. M.IJ., COOPER, R.A.. UZMANN, J.R. AND BURNS, T. 1982. Assessment of the U.S.A. offshore American lobster (Homarus americanus) fishery. International Council for the Exploration of the Sea Committee Meetings 1982/K:; 14, GAINES,.S, AND ROUGHGARDEN, J, 1985, Lar- val settlement rate, Proceedings of the National Academy of Science U.S.A, 82; 3707. GARNICK, E. 1989. Lobster (//omarus aniericanus) population declines, and ‘barren grounds’ : a space-medialed competition hypothesis. Murine Ecology Progress Series 58; 23-28. HADLEY, P.B. 1906. Observations on some in- Nuences of light upon the larval and early ado- lescent stages of Homarus americanus: preliminary report. Rhode Island Conimission on Inland Fishing Annual Report 36; 237-257, 1908. The behaviuurof larval and adolescent slages of Homarus. americanus, Journal of Compara- tive Neurology and Psychology 18; 199-301, HARDING, G.C.. VASS, W.P. AND DRINK- WATER,K.F. 1982. Aspects.of larval American lobster (Homarus americanus) ecology in St. Georges Bay, Nova Scotia, Canadian Journal of Fisheries and Aquatic Sciences 39: 1117-1129. RECRUITMENT PATTERNS FOR FTOMARUS HARDING. G.G., DRINKWATER, K.F. AND VASS, W.P. 1983. Factors influencing the size of American lobster (Homarus americans) stocks along the Atlantic coast of Nova Scotia, Gulf of St. Lawrence, and the Gulf of Maine, 4 new synthesis, Canadian Journal of Fisheries and Aquatic Sciences 40: 168-184, HARDING, G.C., PRINGLE, J.D., VASS. W.P,. PEARRE, S, AND SMITH, §, 1987, Vertical dis- tnbution and daily movements of larval Homarus americanus over Browns Bank, Nova Scotia, Marine Ecology Progress Series 441; 29-41, HARDING, G.C. AND TRITES, R.W. 1988. Disper- sal of Homarus americanus tarvae in the Gulf of Maine from Browns Bank, Canadian Journal of Fisheries and Aquatic Sciences 45: 416-425, 1989. A further elaboration on ‘dispersal of [/o- marus americanus larvae in the Gulf of Maine from Browns Bank,’ in response lo comments by D.S. Pezzack, Canadjan Journal of Fisheries and Aquatic Sciences 46; 1077-1078. HERRICK, F.H. 1896. The American lobster: a study of its habits and development. Bulletin of the United States Fish Commission 15; |-252, 1911. Natural history of the American lobster, Bul- letin of the United States Bureau of Fisheries 29: 149-405, HILL, A.E. AND WHITE, R.G, 1990. The dynamics of Norway lobster (Nephraps norvegicus. 1.) populations on isolated mud patches, Journal of the International Council for the Exploration of the Sea 46; 167-174. HUDON, C. 1987. Ecology and growth of postlarval und juvenile lobster Homarus americanus, ott Nes de la Madeleme (Quebec). Canadian Journal of Fish- eries and Aquatic Sciences 44; 1455-1869. HUDON, C. AND LAMARCHE, G, 1989, Niche segregation between American lobster Homarus americanus and rock crab Cancer trrorarus, Marine Ecology Progress Series $2; 155-168, HUDON, C., FRADETTE, P. AND LEGENDRE, P. 1986. La repartition horizontale et verticale des larves de homard (Homarus arericanus) autour des iles de la Madeleine, golfe du Saint-Laurent, Canadian Journal of Fisheries. and Aquatic Sciences 43: 2164-2176, KROUSE, J.S, 1980. Summary of lobster, Homarus americans, lagging studies in American waters (1898-1978), Canadian Technical Report of Fisheries and Aquatic Sciences 932: 135-140, LARKIN, P.A, 1972, The stock concept and manage- ment of Pacific salmon, 23). In ‘Lectures in Fisheries University of British Columbia’. (PLR. MacMillan: Vancouver, B.C.). LAVALLI, K.L. AND BARSHAW, D.E. 1986. Post- FA larval American lobsters (Homarus americanus) living in burrows may be suspension feeding. Marine Behaviour and Physiology 15; 255-264. 1989. Burrows protect postlarval lobsters Homarus americanus {tom predaiion by the non-burraw- ing Cunner Tautogolabrus adspersus, but not from ihe burrowing mud crab Neopanape tax- anj. Marine Ecology Progress Series 32; 13-16, LAWTON, P. 1987, Diel activity and foraging be- haviour of jovenile American lobsters, Homarus americanus, Canadian Journal of Fisheries and Aquatic Sciences 44: 1195-1205. LEWIN, R. 1986. Supply-side ecology. Science 234; 25-27, MARGOSIAN, A,, TAN, F.C., CAT, D. AND MANN, K.H, 1987. Scawater temperature ré- cords from stable isotopic profiles in the shell of Modiolus modiolus. Estuarine, Coastal and Shelf. Science 25; 81-89, MCCRACKEN, F.D. 1979. Executive summary, Canso marine environment workshop, Fisheries and Marine Services Tectinical Report 834, MCLEESE, D.W. AND WILDER, DG, 1958, Thy activity and: catchability of the lobster (Homarirs americanus) in relation to temperature, Journal of Fisheries Research Board of Canada f5: (345-1354, MILLER, R.J, 1985s, Succession in sea urchin 2nd seaweed abundance in Nova Scotia, Canada, Marine Biology 84; 275-286. 1985b. Seaweeds, sea urchins, and lobsters: A te- appraisal. Canadian Journal of Fisheries and Aquatic Sciences 42: 2061-2072. MILLER, RJ. AND COLODEY, A.G, 1983, Wide- spread mass mortalities of the green sea urchitt in Nowa Scotia. Canada, Marine Biology 73: 263-267. MILLER, R.J., MOORE, D.S. AND PRINGLE, J.D. 1987. Overview of the inshore lobster resources in the Scotia—Fundy Region. Canadian Atlantic Fisheries Scientific Advisory Commitlee Re- search Document 87/85. MILLER, R.J., DUGGAN, R.E,, ROBINSON, D.G. AND ZHENG, Z. 1989. Growth and movement of Mamarus americanus on the outer coast of Nova Scotia. Canadian Technical Report of Fisheries und Aquatic Sciences 1716. PERKINS, H.C, 1972. Development rates at various iemperatures of embryos of the northern Jobster (Homarus americanus Milne-Edwards), Fisher- jes Bulletin of the United States 70; 95-99. PEZZACK, D.S. 1989. Comments on ‘dispersal of Homarus americanus larvae in the Gulf of Maine from Browns Bank’ by G. C. Harding and R. W. Trizes, Canadian Journal of Fisheries and Aquatic Sciences 46: 1079-1083, IN PRESS. A review of lobster (Homarus ameri- canus) landing trends in the Northwest Atlantic 1947-87. Journal of the Northwest Atlantic Fisheries Organization, PEZZACK, DS. AND DUGGAN, D. 1983, The Canadian offshore lobster (Homarus americanus) fishery 197|-1982. Shellfish Commission, ICES, CM. (1983)/K. 1986, Evidence of migration and homing of lobsters (Homarus americanus) on the Scotian Shelf. Canadian Journal of Fisheries. and Aquatic Sciences 43; 2206-2211. PHILIPS, B.F. 1986, Prediction of commercial catches of the westem rock labsier Panulirus evenus, Canadian Journal of Fisheries and Aquatic Sciences 43; 2126-2130, POTTLE, R.A. AND ELNER, R.W. 1982. Substraie preference behaviour of juvenile American lab- sters, (Tomarus americanus, in gravel and sill- clay sediments, Canadian Journal of Fisheries and Aquatic Sciences 39; 928-932, PRINGLE, J.D., SHARP, G.J. AND CADDY, J.F. 1982. Interactions in kelp bed ecosystems inthe northwest Atlantic; Review of a workshop, In M.C. Mercer (ed.) ‘Multispecies approaches to fisheries management advice’, Canadian Special Publications of Fisheries and Aquatic Sciences $9; 108-115, PRINGLE, J.D.. ROBINSON, D.G., ENNIS, G.R. AND DUBE, P. 1983 An vverview of the man- agement of the lobster fishery in Atlantic Canada. Canadian Journal of Fisheries and Aquatic Sciences Manuscript Report 1704; 1()3, ROBINSON, D.G. 1979. Consideration of the lobster (Homarus americanus) recruilment overlishing hypothesis; with special reference lo the Cunso Causeway. Fisheries Marine Services Technical Report 834: 77-99, 1980. History of the lobster fishery on the eastern shore of Nova Scotia, Canadian Technical Re- port of Fisheries and Aquatic Sciences 934; 8- 23. SAILA, 8.B. AND FLOWERS, J.M. 1968, Move- ments and behaviour of berried female lobsters displaced from offshore areas to Nurragansell Bay, Rhode Island. Journal of Conservation 31: 342-351. 1969, Geographic morphometric vuriation in the American lobster. Systematic Zoology 18: 330- 338. SCARRATT, D.J, 1964. Abundance and distribution of lobster larvae (Homarus americanus) in MEMOIRS OF THE QUEENSLAND MUSEUM Northumberland Strait. Journal of the Fisheries Research Board of Canada 21: 661-680, 1968, Anartificial reef for lobsters, Homarus amer- icanus, Journal of the Fisheries Research Board of Canada 28: 1733-1738. 1973, Abundance, survival, and vertical and diur- nal distribution of lobster larvae in Northumber- land Strait, 1962-63, and their relationships with commercial stocks, Journal of the Fisheries Re- search Board of Canada 30: 1819-1824. SCHEIBLING, R.E. AND RAYMOND, B.G, 1990, Community dynamics on a subtidal cobble bed following mass mortalities of sea urchins, Marine Ecology Progress Series 63; 127-145. SCHEIBLING, R.E. AND STEPHENSON, R.L. 1984. Mass mortality of Strongylocentrotus droeba- chiensis (Echinodermata: Echinoidia) off Nova Scotia, Canada. Murtne Biology 78: 153-64, SHELDON, R.W., SUTCLIFFE JR. W.H. AND DRINKWATER, K. 1982, Fish production in multispecies fisheries, Canadian Special Publi- cation of Fisheries and Aquatic Sciences 59: 28-34. STASKO, A.B, 1978. Inshore-offshore lobster stock interaction: An hypothesis. Canadian Atlantic Fisheries Scientific Advisory Committee Re- search Document 78/37. STEWART, J.E. 1980. Diseases, 301-342. In J.S. Cobb and B,F, Philips (eds) “The biology and management of lobsters’, Vol 1. (Academic Press! New York). SULKIN, 8,D, 1986. Application of laboratory stu- dies of Jarval behaviour to fisheries problems. Canadian Journal of Fisheries and Aquatic Sciences 43; 2184-2188, SUTCLIFFE, W.H, 1973, Correlations between sea- sonal river discharge and local landings. of American lobster (Homarus americants) and Adantic halibut (Hippoglossus hippoglossus) in the Gulfof St. Lawrence. Journal of the Fisheries Research Board of Canadi 30: 856-859, TEMPLEMAN, W, 1940a, Embryonic developmen- tal rates and egg-laying of Canadian lobsters, Journal of the Fisheries Research Board of Cunada 5: 71-83. 1940b. Lobster tagging on the west coast of New- foundjand 1938. Newfoundland Department of Natural Resources Fisheries Research Bulletin 8: 1-16, TRACEY, M.L., NELSON K., HEDGECOCK, D., SHLESER, R.A. AND PRESSICK, M.L, 1975, Biochemical genetics of lobsters: Genetic varia- tion and structure of American lobster (Homarus americanus) populations. Journal of the Fisheries Research Board of Canada 32: 209 |-2101., RECRUITMENT PATTERNS FOR HOMARUS UNDERWOOD, A.J. AND FAIRWEATHER, P.G. 1989. Supply-side ecology and benthic marine as- semblages. Trends in Ecology and Evolution 4: 16-19. UZMANN, J.R. 1970. Use of parasites in identifying lobster stocks. Proceeding of the 2nd International Conference on Parasitology 56: 12-20. WADDY, S.L. AND AIKEN, D.E. 1986. Multiple fertil- ization and consecutive spawning in large Ameri- can lobsters, Homarus americanus. Canadian Journal of Fisheries and Aquatic Sciences 43; 2291-2294. WHARTON, W.G. AND MANN, K.H. 1981. Relation- ship between destructive grazing by the sea urchin, Strongylocentrotus droebrachiensis, and the abun- dance of American lobsters, Homarus americanus, on the Atlantic coast of Nova Scotia. Canadian Journal of Fisheries and Aquatic Sciences 38: 1339-1349. 363 WILBUR, H.M. 1980. Complex life cycles. Annual Review of Ecological Systems 11: 67-93. WILDER, D.G. 1947. The effect of fishing on lobster populations as determined by tagging experiments. Journal of the Fisheries Research Board of Canada Atlantic Progress Report 37: 10-14. 1948, The protection of short lobsters in the market lobster area. Journal of the Fisheries Research Board of Canada Atlantic Biological Station Circu- lation 11. 1958. Regulation of the lobster fishery. Canadian Fish Culturist 22 (May). WILLIAMS, A.B. 1984, ‘Shrimp, lobsters and crabs of the Atlantic coast of the United States, from Maine to Northern Florida’. (Smithsonian Institute Press: Washington. D.C.). 55Op. WOLFF, T. 1978. Maximum size of lobsters (Homarus) (Decapoda, Nephropidae). Crustaceana 34; 1-14. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 364 LIFE HISTORY CHARACTERISTICS OF LITHODES FEROX (ANOMURA: LITHO- DIDAE) OFF NAMIBIA Lithodes ferox (Filho) is a deep waler anomuran crab that lives on the upper continental slope off West Africa. It constitutes an important by-catch of the demersal hake fishery (AbellG and Macpherson, 1986) and of the red crab trap fishery (Melville-Smith, 1982) in Namibia, Despite its abundance and its potential as a fishery resource, little is known of ils biology and ecology. L, ferax was sampled off Namibia in the Benguela up- welling region during ten fishery Tesearch cruises per- formed between 1983 and 1989 on board freezer-trawlers. The study a7ea was between latitudes 23°S and 30°S and depths between c. 50 and 500 m, Some deeper rawls were oceasionally performed. The area was divided into strats of one degree latitude and 100 m depth Sex, carapace length, presence of epys or Gag remains on the female pleapods, and occurrence of a rhizocephalan purasile were noted for al] crabs, Occurrence of epldionts was also noted in some cruises. Sex-ratio analysis wis performed When more than 10 individuals were caught in a trawl, Fecundity was calculaled from recently extruded eggs from dry weight proportions. Distribution Some interesting features have been identitied in the distribution patterns of L. ferax: (1) Occurrence of a sea- sunal bathymetric migration, The species rarely occurs at depths fess than 400 m in summer. while there is a dlisper- sion of the population towards shallower walers (¢300 m) in winter. These movements appearto be related to: (a) The reproductive biology of the species: Almost all of the females occurring in the shallowest strata (300-400 m) jn winler are ovigerous, ihe proportion clearly decreasing with depth; and (b) Upwelling-telated hydrographic events. Oxypen levels on the bottom show seasonal decreases (Chapman and Shannon, 1985; Mas-Rieraefal., 1990), Lowest levels ure found jn summer. (2) Recruitment 10 the adult population takes place in deep waier. Juvenile crabs are found almost exclusively in areas deeper than those inhabited by the adull population. The mean size of both mates and temales decreases with depth. (3) Sex-ratio patterns. Sex-falio distribution shows a clear tendency for the species to form unisexutal groups. Males tend to be captured with other males and females with other females. Reproductive Biology As staled above, the seasonal movements performed by (he population can he partially considered as a repro- ductive migration, A high proportion of ovigeruus females is found in all seasons, Most adult females are ovigerous. The size of female sexual maturity, calcu- lated. from the oecurrence of ovigernus females. lies between 75 and 90 mm carapace length (CL) The num- ber of eggs carried by ovigerous lemales ty related 10 size and {luctuates between 2500 and 8000, The mean diameter of recently extruded egps is 1.97 om The patiorns of epibiosis by the pedunculare barnacle Poectlasma kaempferi indicale several features related to the reproductive and moulting biology of the host: (4) MEMOIRS OF THE QUEENSLAND MUSEUM Jifferent moulting patlerns occur between the sexes; (b) the approximate size of puberiy moult lies between 80-90 mm CL in males and berween 70-80 mm in females; (c) mules do not have a terminal moull; (d) females apparently have a terminal moult; (¢) there is a close match of the oviger- ous/size pattern with the epibiosis/size pattern. Reproductive and cpibiosis patterns sugpest that (a) puberty moull coincides with terminal moult in females. This Would imply (b) that females would accordingly only undergo one reproductive cycle A small proportion of adult crabs is infested by the rhizucephalan Briarasaceus callasus: 2.6% females and 4.36% mates. These crabs are not able to reproduce, Discussion Several features of the life history of L. ferax may be infertcu, Ovigerous females migrate in winter towards shallower (300-400 m) waters, where hatching pre- sumably occurs. Larvae may then be carried to the surface by the upwelling waters and dispersed northwards and offshore by the Benguela current. Recruitment takes place i deeper Walers, aS happens in other deep-water crabs (Wigley ev al, 1975). As crubs grow they mave into shallower waters. as shown by size frequency distributions and mean size per trawl, Adult crabs then segregate into unisexual groups in the main habitat (muddy bottams, 300-500 m depth), In summer, the population moves into deeper waters, presumably in relation to the seasonal decrease in batlam oxygen levels, Puberty moult apparently coincides with terminal moull in females, bul not iq males. Females could accordingly only undergo one reproductive cyele, A small part of the pupulation is parasitized by a rhizocephalan and would not therefore be able (0 reproduce. Literature Cited Abello, P. und Macpherson, E, 1986, Biolowia de algunos. crusticeos decipodos de lax costas de Namibia: dis- tribucian y abundancia. Calleetion of Scientific Papers International Commission tor \he Southwast Atlanii¢ Fisheries 13: 7-23. Chapman, P.and Shannon,.L.V. 1985, The Benguela ecosys- tem. Part 1, Chemistry and related processes, Ocean- ograpy and Marine Biology Annual Review 23; [83-251 Mas-Ri¢ra. J., Lombarite, A., Gordoa, A, and Macpher- son, E. 1990. Influence of Benguela upwelling on the structure of demersal fish populations off Nami- bia. Marine Biology 1U4; 175-182, Melville-Smith, R. 1982. A bricf exploitation of the stone crab Likodes murrayi (Henderson) off South West Aftica, 1979/80. Fishery Bulletin South Africu 16- 45-55, Wigley, R.L. Theroux, R.B. and Morray, WE. 1975. Deep- seated crab, Geryon quinquedens, survey off the north- eastern United States. Murine Fisherics Review 37: 1-21 P. Abell and E. Macpherson, Instiiul de Ciéncies del Mar (C.8.LC.), Passeig Nacional, 08039 Rarvelona. Spain MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum SPATIAL AND TEMPORAL RECRUITMENT PATTERNS OF DUNGENESS CRAB IN THE NORTHEAST PACIFIC GLEN 5S. JAMIESON AND DAVID A, ARMSTRONG Jamieson, G.S.and Armstrong, D.A. 199] (1901; Spatial and temporal recruitment patterns af Dungeness crab in the northeast Pacific, Memoirs of the Queensland Museum 31; 365-381, Brisbane. ISSN 0079-8835, The Dungeness crab. Cancer magister, is the main crustacean species exploited in the northeastern Pacific from central California to Kodiak, Alaska, Abundance along the coast south of British Columbia has Nuctualed ina generally cyclical manner which a number of studies have tried to expla. but several unreluled competing, hypotheses currently remain preventing resolution of this question. A combination of mechanisms seems a likely pense and additional data appears necessary before understanding is achieved. There Ss geneyal agreement that {luctuation in calch is a reflection of variable yvear-class strength and recent studies of farval and (+ crab have investigated the importance of abiotic and biotic factors. Dungeness crab are regionally umque in that while many of their pelagic larvae move tens of kilometres offshore. they musi return to shallow waler Lo survive as juveniles. Oceanographic and meteorological conditions seem to be particularly influential in determining the magnitude of dispersal and unshore movement, and the conditions which allow successful settlement off Vancouver Island have now been described. Strong settle- ment does not necessarily equate wilh a strong year class al harvesting, though, and biotic factors primarily determine survival of juvenile crab, Finally, there is increasing evidence that the crab population in Georgia Strait and Puget Sound, i.e, in the ‘inland sea’ inside of Vancouver Island, may be a distinct stock with dispersal, recruitment and population dynamics characteristics unique from the population found on the open outer coast. Comparison of common features betwee the two stocks is allawing evaluation of the relative importance of major factors influencing population abundance and ultimately, landings. [] Dungeness crah, Cancer magisrer, fishery, reeruitment, larvae, dispersal, pupulation dynamics, northeast Pacific. Glen S. Jamieson, Pepariment uf Fisheries and Oceans, Bialagical Sciences Branch, Pacific Biological Station, Nonainio, B.C, Canada, VOR SKO; David A. Armstrong, School of Fisheries, University of Washington, Seattle; WA, USA 98195; 6 July, 1990. Studies of larva) and juvenile stages of com- mercial Decapoda have generally been done for purposes of describing ecology, reproductive bi- ology, population dynamics, habitat require- ments, and predator/prey relationships. While quantitative studies of catch-per-unit-effort (CPUE) and density have been used to estimate the next year’s recruitment for incorporation into fisheries. management plans, data have been rarely amenable for accurate predictions. in excess of one year (Cobb and Caddy, 1989). Although predictive capability is a desirable aspect for management, in the case of Decapoda, this is often frustrated because of high seasonal and spatial variability, as well as tremendous interannual variability, caused by a suite of biotic and abiotic factors (Jamieson, 19863, b; Botsford et al., 1989). This is particularly the case for quantitative data on Jarvae, and such data are typically of limited use in definition of stack-re- cruitment relationships or prediction of ultimate year-class strength in the fishery- Only a few attempts have becn made to esti- mate adult abundanee from measures of larval abundance and female fecundity. Nichols er al, (1987) calculated female stock biomass of Ne- phrops lobster in the Irish sea from estimates of larval production and female fecundity and in- corporated these data into a multi-species model of lobster and cod interaction. Application of this same technique was.used by Nichols and Thom- pson (1985) to estimate stock size of the edible crab, Cancer pagurus, Similarly, Incze et al. (1987) accounted for significant differences in interannual densities of larval tanner crab (Chionoecefes optlio) based on quantitative changes in number of adult females. However, their suggested relationship did not hold in all years of their study, nor did it apply well to a congener, C. bairdi. Use of indices of juvenile abundance in Deca- poda to predict adult spawning stocks or relative strength of fisheries have only been developed successfully in a few instances, Relative year- class strength of juvenile rock lobster (Panulirus cygnus), aS measured by an index of puerulus settlement, Was correlated to the strength of cam- mercial fisheries four years later (Caputi and Brown, 1986; Phillips, 1986, Phillips and Brown, 1989), A similar approach was used in slock-recruitment analyses of blue crab (Cal- linectes sapidus) populations in Chesapeake Bay (Tang, 1985). A more thorough study was re- cently presented by Lipcius and Van Engel (1990) based ona thirty year time series of data, from which they concluded thal a significant correlation exists between juvenile abundiince and spawning stock size. In this paper, we review recruilment of Dunge- ness crab, Cancer magister Dana, considering all three major life stages: embryo, larvae and juveniles. We define recruitment as abundance change between consecutive life history stages, culminating ultimately in an annual increase in abundance of the fished population since larger crabs only moult once annually. We emphasise recruitment to both larvae and juvenile life his- lory stages, since these are periods of great mor- lality, and generally the times when relative yeur-class Strengths at recruitment to the fishery are typically established for this species. Events progressively occurring throughout the life his- tory cycle are discussed as these will bear on the abundance of crabs at each successive life his- tory stage leading to recruitment to the fishery. We also consider recruitment in four major geo- raphic regions: 1) the outer coast from San tancisco, California, to Cape Flattery, Wash- ington; 2) off the west coast of Vancouver Island: 3) north of Vancouver Island to Kodiak Island, Alaska: and 4) the Georgia Strait-Puget Sound (GS-PS) complex. These specific locations were selected on the basis of broad-scale oceano- graphic boundaries, unique oceanographic sin- pularities, and available data on local Dungeness crab population dynamics. DUNGENESS CRAB LIFE HISTORY Dungeness crab ranges from the Pribilofs Is- lands to Magdalena Bay, Mexica, in the north- eastt¢rn Pacific (Hart, 1982; Jensen and Ammstrong, eet} and is commercially exploited from northern California to Kodiak, Alaska, This spatial distribution overlaps generally recog- nised oceanographic domains (Dodimeud et al, 1963; Thomson, 1981; Ware and McFarlane, 1989) for coastal areas of the norjheastern Pacific Ocean, and this probably influences ob- served recrifilment patterns and makes causative generalisations inappropriate for the coast as a whole. Dungeness crab have a relatively long pelagic larval period, with fiye zocal stages and one MEMOIRS OF THE QUEENSLAND MUSEUM megalopal stage before settlement to the ben- thos. Total larval period is about 110 days at ambient temperatures (Poole, 19466; Lough, 1976; Reilly, 1983), with about 28 days spent as megalopac (Hatfield, 1983), [t is somewhat unique among nearshore benthic species in that a portion of its larvae is commonly found con- siderable distances offshore, with later stage zova and early stage megalopae tending lo be found furthest offshore (Reilly, 1983; Jamieson and Phillips, 1988; Jamieson ef al., 1989). Late intermoult stage megalopae are found in abun- dance progressively closer inshore (Hatfield, 1983; Jamicson and Phillips, 1988), but mecha- nisms which would bring megalopac located more than about 30-40 km offshore to appro- priate nearshore locations (<64 m depth) for enhanced survival as juveniles (Carrasco ev al., 1985) have not yet been satisfactorily deter- mined (Jamieson ef al., 1989), Offshore move- ment presumably facilitates larval dispersal, but i may be that most nearshore settlement results from those larvae which remained shoreward of region-specific, mostly as yet undetermined, oceanographic boundaries. Most larval settlement is typically in May and June along the outer coast, with selllement in both estuarine and nearshore locations. Much recent study in Washington (Gunderson ef ai., 1990) has been focused on the relative impor- tance of some of the region's major estuaries (Willipa Bay and Grays Harbor, Washington), compared with the arca shoreward of the 50 m isobath along the outer coast, in terms of their habitat contribution to overall regional recruit- ment, Juvenile dynamics of Dungeness crab in both these locations have been relatively well desertbed, and it has become evident that consid- erable annual variation can occur, Female crab extrude their first egg mass as 2 y-olds at about 115 mm, notch-to-notch carapace width (CW), while males are larger than females at puberty and begin mating successfully at about 140 mm CW (3-yolds}. Males mostly recruit to the fished population al 34 y of age. THE PHYSICAL ENVIRONMENT REGIONAL CIRCULATION The general surface current pattern over the continental shelf has been described by a number of recent reports, including Hickey (1979, 1989), Freeland er «tf, (1984), and Thomson ev al, (1989), The west coast of Vancouver Island borders the bifurcation zone of the Subaretic Current. an extensive, albeit poor defined, zonal flowing, cross-Pacific surface current (Fig, 1), Seaward of the continental shelf, this current RECRUITMENT PATTERNS OF BUNGENESS CRABS splits into the pole-ward flowing Alaska Curreni and the equator-ward flowing California Cur- rent. Direct observation of a persistent northward near-surface flow off Vancouver Island indicates that the offshore circulation there is dominated by the Alaska Current (Thomson e7 al,, 1989), Dungeness crab occur in two of the three princi- pal oceanographic domains recognised by Ware and McFarlane (1989), namely the Coastal Up- welling and the Coastal Downwelling Domains (Fig. 2). The former extends from Baja Cal- ifornia to the northern tip of Vancouver Island and is defined by the normal summer paticrn of Wind stress curl and Ekman divergence, 1.¢. up- Welling (Parrish ef al, 1981), Generally north- west winds from May to September resull in southward-flowing Shelf-Break Current (SBC) centred on the outer margin of the continental shelf, This causes upwelling of intermediate depth, cold water onto the continental margin and offshore transport. Southwest winds domi- nate this Domain during the winter, causing downwelling, onshore transport and poleward transport of surface waters in.a seasonal current called the Davidson Current. The annual transi- tion between the predominantly upwelling and downwelling seasons occurs inthe spring (Mar.— Apr.) and fall (Sept,—Oct,) with The seasonal reversal in psevalling alongshore winds and cur- rents (Thomson ef al., 1989), The Coastal Downwelling Domain extends from the northern tip of Vancouver Island north- ward along the coast of southeast Alaska and then westward along the Aleutian Islands. The Alaska Current flows adjacent to the coast of North America seaward of the coastal margin. being driven by a wind stress.curl and augmented by freshwater addition and an along-shore, wind-induced sea level gradient. Freshwater runoff causes a poleward Mowing coastal cur- rent, extending to about 40 km offshore. The transilion in prevailing coastal winds in the spring is weak, bul due to the general behaviour of the cyclonic meteorological systems in the Tegion, wind stress tends to augment the baro- clinic component of the coastal circulation by confining it close ta shore. As a consequence, from central British Columbia north ta about Kodiak Island, there is a generally persistent downwelling except for a few months in the summer (Ware and McFarlane, 1989), The southern boundary of this Domain is not sharply defined from a strictly oceanographic viewpaint- The continental shelf off Vancouver Island, although not a recognised Domain itself, being part of the Coastal Upwelling Domain, has. a Unique oceanographic feature which for Dunge- ness crab makes this area intermediate between the two Domains discussed. The outflow from Juande Fuca Strait, being of lower density runoff from rivers entering the GS—PS complex, forms the source of the Vancouyer Island Coastal Cur- rent{VICC), This.is a persistent pole-ward flaw- ing coastal curren(, confined mostly landward of the 100 m jsobath on the cantinental shelf, that extends Io about the northern tip of Vancouver Island (Thomson et al,, 1989), After the spring transition, this current flows counter to the pre- vailing northwesterly winds along the outer coast and the Shelf-break Current while after the fal] transition, it flows with and merges with the Davidson Current, TorOGRAPHY Washington, Oregon and California typically have broad, extensive, sandy beaches extending for scores of kilometres, with few bays or head- lands. The coast of British Columbia and south- east Alaska is mostly rocky and fjordal, with many headlands, tslands, small bays, and rela- lively small, crescent-shaped beaches. Dunge- ness crab most commonly occur in a habitat of extensive sand, and so available optimal habitat is generally less north of Washington State. Georgia Strait and Puget Sound consist of a variely of habitats, with Tjordal inlets predami- nant On Ure eastern side tn Canada and gently sloping, gravel-sand bottams predominant in Pugel Sound and the southeastern side of Van- couver Island. The Gulf and San Juan Islands are in the middle of this region and have mostly sleep, rocky shores. which are of marginal suita- bility the Dungeness crab. LIFE HISTORY STAGES AND THEIR RECRUITMENT Parent PoruLaTion AND FECUNDITY The extensive pelagic larval duration of Dungeness crab in areas of strong along-shore ocean currents apparently prevents development of discrete, genetically distinctive populations on the ouler coasi (Soulé.and Tasto, 1983). There is no evidence 16 supgest thal crab larvae have the navigational abihty to ‘home’ and return to the specific: location where they were hatched, In the Coastal Upwelling Domai, larvae hatch in January-February during a period of strong, northward-flowing nearshore currents, which aboul two months later typically reverse to flaw equally strongly in asoutterly direction. With an approximalely four month larval period, this may resull in extensive larval dispersal. Larvae hatching off northem Calilormia could theoreti- cally move as far north as British Columbia before currents reverse, Similarly, larvae hatch- 368 MEMOIRS OF THE QUEENSLAND MUSEUM 132° 126° RECRUITMENT PATTERNS OF DUNGENESS CRABS 7 WEST WIND DRIFT CENTRAL PACIFIC GYRE » — ro 2 TRANSITION ZONE a %, ¥¢ 3 1 COASTAL DOWNWELLING COASTAL UPWELLING 180° wi70° W 160" W 150° W 140° W 130° W 120° W 110° Ww 100° Ww FIG. 2. Approximate areas of oceanic domains and prevailing current directions in the northeast Pacific Ocean (modified from Ware and McFarlane, 1989). ing near the southern boundary of the Coastal Downwelling Domain could move to its north- ern boundary, while larvae hatching in the north- ern part of the Coastal Upwelling Domain could move into the Coastal Downwelling Domain, entirely because of passive transport. The con- sequence is that considerable mixing of progeny hatched at different sites probably occurs, making it impossible to clearly identify the parent population of juveniles that recruit at any particular location. As discussed by Jamieson (1986a), the extent to which a local population may contribute to local recruitment is unknown, but it appears with available data to be slight. It is illegal to harvest female Dungeness crab in Alaska, Washington, Oregon and California. Although this can legally be done in British Columbia if females exceed the minimum legal size (MLS) of 155 mm CW (= 165 mm, spine- to-spine carapace width), in practice, few are harvested because of poor market demand, since meat yield is less, and there is a general lack of sufficiently large female crab. The size limit for males, although not known to be based on any documented biological data, presumably allows successful mating to regularly occur since in most locations many female crab caught during the winter carry extruded, fertilised eggs (Jamie- 369 son and Armstrong, unpubl.). Jamieson (1986a) discussed in detail the available data supporting assumptions relating to crab fecundity, and con- cluded that if maximising reproductive potential is an identified goal, then insufficient data are presently available to establish what relative level of progeny production is being achieved. Nevertheless, although commercial landings have varied substantially over time (Fig. 3), de- tailed surveys of larval occurrence (Jamieson and Phillips, 1988; Jamieson et al., 1989; Jami- eson, unpubl.) have consistently found wide- spread high levels of larval abundance over the continental shelf off Vancouver Island and Washington, and in Georgia Strait in the five years studied to date. Annual settlement of larvae has varied substantially during this period (Jami- eson et al., 1989), suggesting that factors other than overall larval production are the major de- terminants in establishing year-class strengths. LARVAL SETTLEMENT Some Dungeness crab larvae occur at great distances offshore and while this no doubt facil- itates and/or is the result of species dispersal, there is always the risk of larval wastage in that many larvae may never return successfully to geographic areas favourable to juvenile survival. It has not been established how far offshore most larvae which do settle and survive have actually gone, but the relative lack of early-stage mega- lopae, in abundance, in close proximity to shore in outer coast areas, at least off British Columbia and Washington (Jamieson et al., 1989; Jamie- son, unpubl.), does suggests that movement in at least the kilometre scale can be expected. As- sumed aspects relating to this have been dis- cussed in detail by Jamieson ef al. (1989), and they, along with Jamieson and Phillips (1988), have demonstrated that juvenile recruitment pat- terns off the outer coast of Vancouver Island, British Columbia, are substantially different from that off Washington, Oregon and Cal- ifornia (Fig. 3). Outflow from rivers emptying into the GS—PS complex is predominantly through surface out- flow in Juan de Fuca Strait, and this outflow, the VICC, subsequently moves northward adjacent to the coast of Vancouver Island. Crab mega- lopae are virtually absent in this current and are concentrated on its seaward boundary (Jamieson and Phillips, 1988; Jamieson et al., 1989). It thus apparently acts as a barrier to the movement of plankton to shore (Thomson et al., 1989), and FIG. 1. Prevailing surface circulation off the British Columbia—Washington coast. A, winter. B, summer. Broken arrows indicate uncertain currents. Numbers give speeds (cms) (modified from Thomson, 1981). 370 ALASKA 5 YS BRITISH COLUMBIA uw a a as 7.073075 77 79 BF 0S BS AF BD 9D mt Arnenacine : PUGET SOUND WASHINGTON LANDINGS (1073) CALIFORNIA ‘h 7R 40 BD He 77 ot Bk BA BT OG Ot WS4 3 SH AO 57 Sy Bt ec Mm we DSS Ql te Be Ow PN Py Ty ot Shoo nl SEASON FIG. 3. Dungeness crab landings by political jurisdic- tion off western North America. recent study by Jamieson and Thomson (un- publ.) indicates that megalopae are being con- centrated in an area of upwelling and/or seaward surface current movement of relatively low velocity (1-5 cm sec’') between the VICC and the SBC (Fig. 4). Shoreward movement of sur- face waters is associated with southerly winds (Fig. 5) but unless sufficiently intense or pro- longed, such movement is only to the seaward boundary of the VICC. The presence of the VICC seems to direct most up-welled water off- shore, while because of the shallow depth of the nearshore portion of the continental shelf, no shoreward movement beneath the VICC is possible. The only apparent opportunity for sub- stantial movement to the shore is when the VICC temporarily breaks down because of cessation of the surface outflow in Juan de Fuca Strait, which is typically associated with sustained, strong southerly winds. This is accompanied by a rise in mean coastal sea level, enhanced wind and convective mixing of surface waters and the cessation of upwelling — events similar to those which occur during and after the Fall Transition (Thomson ef al., 1989). From a crab recruitment, MEMOIRS OF THE QUEENSLAND MUSEUM major recruitment on the west coast of Vancou- ver Island is thus only possible when appropriate meteorological events occur when megalopae ate present and ready to settle, namely May and June (Jamieson and Phillips, 1988). This does not always occur, and since 1983, major crab settlements at Tofino, British Columbia, were only observed in 1983 and 1989 (Smith and Jamieson, 1989a: Jamieson, unpubl.). Little settlement occurred from 1985 to 1987, while there was only limited settlement in 1988. South of Cape Flattery, located at the southern, seaward end of Juan de Fuca Strait, the absence of a ‘barrier’ current adjacent to the coast means that settlement is not physically impeded by nearshore currents, although years of excep- Line G, June 1989 Abundance (per 10 square meters) Depth (m) 7000 600 —— C. mogleter ‘eb [= Depth 7500 N wa 10 J F ‘i 4,300 +k : eee, ‘ / 4200 - “ DA gate fee = = 100 or 0.01 —L —— — —L —L_ oO Q 10 20 30 40 50 60 Distance offshore (km) Line E, June 1989 nba putenass (per 10 square meters) Depth (m) Bo —— C, magiater = paptn /\_ }s00 ws \ / S400 Pfs _— \ Ma (306 \ Zz i \ a 7 200 O1e \ E \ 44100 ae V 0.07 [ ie — " “ 0 10 20 30 40 50 60 Distance otfshore (km) FIG. 4, Abundance of Dungeness crab megalopae in across-shelf transects in relation to depth. The north- flowing Vancouver Island Coastal Current is mostly shoreward of 100 m depth, with the south-flowing Shelf-Break Current on the seaward side- RECRUITMENT PATTERNS OF DUNGENESS CRABS 371 a LV ij = SRITISH os05s/16 5 Neal 5/16 : a f | COLUMBIA eee ® % E. * ak Vancouver ‘ a 4 | {sland “ay & A a ene, hy He Th FE yds é. ¢ fy 3 MAP re TOFINOY Yo, INSERT Lace . Hm Js A sanbebre SS a hs &, de o309/13 rv BARKLEY 0512/13 SOUND 0400/18 roy \6 rh ~~ -—— ~ ‘5 y =. 7, 2202/13 es \ \ yi} ~ 14 14° 100m St ey ‘ y= 200m a 5/13 it ° oy rae ) S458 j % : @®> € ‘- j “| \ A \ \_- ae } ts ir ~L ¢ af” ' eZ Pa i 1 a lt } i j a \ t / \. ) ‘ ny yi Ww : - ‘ i) \o 20 30 Km ye i 200m a ¢ t ae" \, . 48° JUNE 1986 f ; a aal ? | \26" r26° 4 FIG. 5. Tracks of 9 drifters deployed along a transect off Tofino, British Columbia, on June, 1986. Marks along each track indicate the position of each drifter at noon on the day (the adjacent 2-digit number) indicated. Four-digit numbers refer to the hour the drifter was deployed and/or retrieved (from Jamieson et al., 1989). tional settlement are also typically sporadic. The temporal pattern of settlement along the Ameri- can coast has shown an annual variability in magnitude of about ten-fold, with no obvious similarity to that off Vancouver Island. Major landings have occurred about every 9-10 y (Fig. 3) and causative mechanisms have been hy- pothesised and discussed extensively (Jamieson, 1986a; Methot, 1989; Botsford e7 al., 1989). A satisfactory explanation has yet to be fully estab- lished. While larvae have been observed in abun- dance over most of the continental shelf, some data suggest (R.A. McConnaughey, Univ. Washington, Seattle, WA, pers. comm.) that in years of major settlement off Washington, most larvae may never move far from shore. This, coupled with that area’s extensive favourable habitat, increases larval survival at settlement. There have been no studies of relative larval distribution and abundance off Alaska. Annual commercial landings (Fig. 3) do not show the same pattern evident off British Columbia or 372 further south, but this may be because, like the crab fishery in British Columbia (Jamieson, 1985), regional landings are the composite of a number of distinct regional fisheries (Koeneman, 1985; Kimker, 1985; Merritt, 1985; Eaton, 1985). Recruitment patterns in each re- gion may be largely disconnected, giving no clear pattern for the region as a whole. Larval settlement patterns in the GS—PS com- plex are different from those along the outer coast. Megalopae settle in abundance mostly later in the year (August-September), are smaller in size, and show some minor, although perhaps significant, morphological differences (DeBrosse et al., 1990). Recent studies of meg- alopal spatial and vertical distribution (Jamieson and Phillips, unpubl.) in Georgia Strait indicate that in July, megalopae are found in high abun- dance throughout the Strait but that their vertical distribution during daylight seems to differ from that found off the outer coast (Fig. 6). In the Strait, megalopae appear to descend to depths of about 150 m while offshore, they are seldom found in quantity below about 40 m (Jamieson etal., 1989). While megalopae have been caught below 100 m on the outer coast (Jamieson, unpub.data), they have been late intermoult stage, suggesting they may have been in the process of settling. Dungeness crab megalopae have been caught as deep as 273 m in coastal inlets in epibenthic sled tows (Jamieson and Sloan, 1985), a depth where they are unlikely to survive as juveniles. This difference in megalopal diel migration behaviour has interesting consequences, partic- ularly if zoea from the two regions show similar differences as well. Since summer water temperatures below about 50 m in most of the Strait are 7-8°C (Thomson, 1981) [temperatures on the outer coast at 25-50 m depth are about 12-14°C (Thomson e¢ al., 1989)] and daylight in July is about twice as long as darkness, growth rate would be reduced, thereby probably extend- ing the larval period and possibly resulting in their smaller size at settlement. It also could result in stock isolation, since the surface water of Juan de Fuca Strait, the main connection be- tween the GS—PS complex and the Pacific Ocean, flows predominantly seaward (Fig. 7) while water below about 80-100 m flows pre- dominantly shoreward (Thomson, 1981). Geor- gia Strait megalopae, which may spend most of their time at depth, would thus tend to be retained within the GS—PS complex while outer coast megalopae, which are mostly near the surface, would generally be prevented from entering the Strait. Sustained southerly winds can, though, temporarily stop the outflow of surface water in MEMOIRS OF THE QUEENSLAND MUSEUM Megalopal Day Depth Distribution Georgia Strait, July 19, 1989 Percent N = 143 70 60 | | f= 207 10 l " T a : —— 100-120 120-140 140-160 160-180 180-200 Depth (m) | —<—— 80-100 Maximum depth = about 400 m Megalopal Day Depth Distribution Outer coast, May and June, 1987 Percent ——_ N= 175 | 0-12 12-25 0-25 Depth (m) Maximum depth + >400 m FIG. 6. Daytime depth distributions of megalopae off the outer coast (modified from Jamieson et al,, 1989) and Georgia Strait. Data collected with Tucker trawls in 1987 and 1989, respectively. Juan de Fuca Strait and the penetration of outer coast water (Fig. 8), sometimes containing meg- alopae (P. Dinnel and D. Armstrong, unpubl.), has been documented (Thomson, 1981; Thom- son etal., 1989). However, for reasons described later, this is mostly on the American side of the Juan de Fuca Strait and relatively few outer coast megalopae would seem likely to penetrate into the Canadian waters of Georgia Strait. JUVENILE SURVIVAL UPWELLING DOMAIN: Megalopae settle to the benthos and metamorphose to first instar juve- nile crabs primarily between May and June along the coast from Northern California through Washington State (Botsford er al., 1989). Most studies of juvenile crab populations in this area have been descriptive portrayals of distribution and abundance, growth and size-at-instar RECRUITMENT PATTERNS OF DUNGENESS CRABS DEPTH ima Heed slronger (har gee Gialanes gerne suet iim) FIG, 7. Average direction of water flow in cross-sec- tion of Juan de Fuca Strait from Pillar Point (USA) to Port Rentrew (Canada), Shaded is a seaward flow, no shading is a landward flow (from Thomson, 1981). (Cleaver, 1949; Poole, 1967). There have been few quantitative surveys that provided estimates of mortality or indices of year-class strength. but those done indicate that considerable differences in survival occur within a region, depending on both abiotic and biotic factors. It is important to briefly discuss these factors. in considering how recruitment is mediated. Although larvae may occur in abundance off- shore, juveniles for the most part seem to survive only in nearshore locations, in water generally 373 shallower than 40 m (Gotshall, 1978; Carrasco et al., 1985). Estimated density increases ap- proximately 20- to 50-fold as depth decreases from 41-70 m ta 16-40 m (Carrasco ef al, 1985: MeConnaughey and Armstrong, unpubl), Even inside of the 40 m isobath, density of 0+—0+ crab fluctuates appreciably because of substrate lype. IL is highest on well sorted sand and lowest on gravel-cobble (Fig. 9), Trawl samples off Grays Harbor, Washington, in [985 showed 0+ crab densities as high as 30,000 crab/ha on sand, compared to only about 200/ha on gravel. Post- settlement crab growth on the outer coast fram June through September is typically relatively slow, und young-of-the-year are only usually about third instar (13 mm CW) by September (Fig, 10; Gunderson et al., 1990). This Is due in large part to bottom water temperatures of less than 10°C in this upwelling system, As a con- sequence of small size, crab mortality is high, since they remain susceptible to many predators (Reilly, 1983) through the winter, Even numeri- cally Strong year-classes at settlement, such as that of 1985 (Gunderson e¢ al,, 1990), can have their abundance depleted sufficiently through their first winter to become unexceptional il recruitment to the fishery, Quantitative data of sufficient 0* 0+ y-class FIG. 8. Drawings based on infrared satellite images of sea-surface temperatures, showing a sequence of warm-water intrusion (heavy stippling) into Juan de Fuca Strait trom the Pacific Ocean in September, 1979. Intrusion was confined {o the southern half of the Strait and reached a maximum of 135 km from the entrance. Four days after the cessation of the causative southwest Winds, the seaward estuarine ¢irculalian was reestablished and the intrusion began ta he udvected our of the Strait (from Thomson, 1981). 124 20 MEMOIRS OF THE QUEENSLAND MUSEUM 124 10wW Jettles —— 46 50N 12410Ww FIG. 9, Dungeness crab density (number ha’') offshore of Grays Harbor, WA, June 1985. survival over sequential years to construct in- dices of year-class strength and determine spawner-recruit relationships are non-existent. Gotshall (1978) found no correlation between an index of 0+ crab abundance and commercial landings 3.5 y later, based on cursory coastal and estuarine surveys in northern California. How- ever, Warner (1987) measured 0+ crab density in fall trawl surveys off northern California from 1972 through 1985 and noted that a 20-fold greater density for the 1972 year-class sub- sequently resulted in a near-record commercial fishery in 1976 (11,300 t). Tasto (1983) and Reilly (1983), who estimated the abundance of benthic juveniles and larvae in central Cal- ifornia, respectively, both observed relatively strong year-classes in 1975 and 1977, which were consistent with an increase in commercial landings for California in 1978-80 (Methot, 1989; PMFC, 1989). The most comprehensive study of 0+ Dunge- ness crab recruitment and survival has been done along the southern Washington coast between 1983 to 1989 (Armstrong and Gunderson, 1985; Gunderson et al., 1990), While they found that high interannual variability in estimated abun- dance of 0+ crab did not equate well to the strength of future fisheries, measures of 1* y-old crabs did. The high abundance of 1+ crab in 1985 (1984 year-class; Fig. 11) led to a record high fishery in excess of 10,000 t in 1987/88 and 1988/89 (Fig, 3). Unique to the 1984 year-class was unusually rapid growth of the coastal cohort (Armstrong and Gunderson, 1985), which re- 50 45 MEAN CARAPACE WIDTH 40 8 MONTH FIG. 10. Comparison of 0°+0+ Dungeness crab growth during their first summer inside an estuary (Grays Harbor, GH) and on the outer coast in near- shore waters near the estuary (NS). Numbers indicate mean bottom water temperature (°C.); bar = 1 SE) (from Armstrong and Gunderson ,1985). RECRUITMENT PATTERNS OF DUNGENESS CRABS PORILATION So * AMI SAT AM an AW lhe hehe Auge mua ‘gee iges ior iver FIG. 11, Population estimates for (1 and 17 -e 1+ Dungeness crab by month and year on the aulet coast and adjacent estuaries aff Washington, Estuarine data for 1983-84 are for Grays Harbor only, but include Willapa Bay for 1985-87 (from Gunderson eral, 1990), sulted in a mean size, by fall, of about 22 min CW, Gunderson et af, (1990) speculated that the more rapid growth of this year-class increased survival over fall and winter and, in turn, a strong 1+ cohort in 1985 (Fig. 11). The cause of more rapid growth in 1984 seemed to be a combination of carly settlement and unusually warm bottom water temperatures in May and June, 1984, com- pared to other years during the study. Another aspect of settlement along the open coast in the Upwelling Domain is direct recruit- meant of juveniles to coastal estuaries (Fig. 12). Settlement there can be high in both intertidal and subtidal areas, although in the subtidal, mor- tality is relatively high and newly settled crab quickly disappear (Dumbauld and Armstrong, 1987; Gunderson et al., 1990). Optimal habitat in the intertidal has a large quantity of bivalve shell, notably of cultured oyster (Crassostrea gigas) or wild softshell clam (Mya arenaria) (Armstrong and Gunderson, 1985; Dumbauld and Armstrong, 1987). Estuarine ctab also bene- fit from higher temperatures and accelerated growth (Fig. 10). By September, estuarine 0+ crab are approximately 335 mim CW, in contrast to the approximately 13 mm CW of outer coast juveniles. During the summer, intertidal crab gradually move to the subtidal, where they are now able to avoid most predators by virtue of their greater size (Reilly, 1983). However, despite high intertidal estuarine abundances of U+ 1+ crab abundance, annual 1* y-old subtidal estuarine populations. are fairly constant and fluctuate only about two-fold (Fig. 11; Gunder- son er al,, 1990). This had led to speculation that estuaries provide a relatively stable recruitment source lo the fishery, representing a significant Proportion of the long-term average landing in coastal fisheries. Contrary to original hypotheses of Armstrong and Gunderson (1 1985), estuaries may thus not be the source of particularly strong year-classes that cause peaks in cycles of fisher- ies landings (Fig. 3). Such peaks instead seem to be the result of high survival of 0+ crab that settle and recruit directly in outer coast areas (Gunder- son ef al,, 1990). DOWNWELLING DOMAIN: As previously noted, this region is topographically quite differ- ent from most of the Upwelling Domain region, General life history and fishery information on the species has been summarised by Koenemar (1985) for southeast Alaska. There is no reason to assume that aspects of life history and habitat requirements are any different for Dungeness crab in this area, but the timing of seasonal life cycle events is different, Settlement of larvae is later and typically occurs in August and Septem- ber. Although fisheries landings do not show cycles of the same magnitude as reported along the coast from Washington to California, sub- stantial fluctuations in catch probably reflect variability in yeur-class size, attributable to the same suite of biotic and abiotic factors hypothe- sised to affect the species clsewhere in its range (Botsford et al., 1989). The apeewelling fea- tures of this area, as previously described, may serve to retain larvae nearshore rather than en- courage lony distance transport in the Alaska Current. Larvae may thus be produced and re- tained in a smaller geographical scale and pro- geny may recruit to areas near where they were hatched. No systematic, quantitative long time serics of data exist for juvenile Dungeness crab recruitment and survival in this Domain, GEORGIA STRAIT/PUGET SouND: As noted earlier, oceanographic features in the inland sea of the GS-PS complex, which extends across the border between Canada and the United States, lead to unusual conditions that may result in maintenance of a separate stock distinct fram that on the outer coast, Based on timing of settle- ment and size of first instar juveniles, P. Dinnel and D, Armstrong (unpubl.) have defined at least two coharts of 04 crab recruiting to Puget Sound in May through September. The first cohort scttles in May and June and juveniles are ap- proximately 7-8 mm CW, comparable in size with outer coast crab juveniles (Gunderson ef al., 1990). This outer coast cohort is identical in size to cohort ‘a’ reported by Orensanz and Gallueci (1988). Coastal zoeae or megalopae apparently enter the GS-PS rh i through the Strait of Juan de Fuca, probably either in surface waiters when surface outflow temporarily ceases (Fig. 376 COASTAL on “3 GRAYS HARBOR, NEARSHORE : oF ¥ Roider \ fumme: Orowenc/ OF tele FIG. 12. Schematic of generalized movement and distribution of megalopae, 0+ and 1+ y-old juvenile crabs between the nearshore coast and Grays Harbor estuary. 8), as discussed earlier, or at depth in the com- pensating inward flow of more dense water. Be- cause of the across-Strait tilt in the boundary line separating net seaward flow at the surface and net landward flow in the lower layer (Fig. 7) due to the combined effects of the Coriolis force and channel curvature (Thomson, 1981), outflow favours the Canadian side and inflow the Amer- ican side. This explains why most settlement of outer coast crabs in the Strait and GS-PS has been observed in American waters. The second cohort identified by P. Dinnel and D. Armstrong (unpubl.) setties in late July and August and is substantially smaller, with a first instar size of 1425 1625 182.5 Carapace Width (notch-to-notch) 422.5 202.5 FIG. 13, Commercial catch size distributions of Dungeness crab, showing the reduction in relative proportion of large crabs as fishing has intensified over time. The narrow vertical bar indicates the minimum legal size limil, modified to show the notch-to-notch measurement. Hecate Strait data modified from Butler (1960); remaining data mod- ified from Smith and Jamieson (in press). RECRUITMENT PATTERNS OF DUNGENESS CRABS characterised by sand and small cobble, often with eelgrass (Zostera marina) or overlying mats of algae such as Ulva sp. At a number of inter- tidal locations throughout Puget Sound, Dinnel et al. (1987) reported high densities of 0+ crab in cobble-sand, with densities highest if macro- phytes were present (Dinnel ef al., 1986). Pre- dictably, refuge availability is an important element determining the carrying capacity of an area, but in contrast to the outer coast where bivalve shell is important (Armstrong and Gunderson, 1985), algae and eelgrass provide most cover in the GS—PS complex. As measured by trends in the fishery, overall recruitment and survival of juvenile stages appears to be more constant and stable within the GS—PS complex compared to the outer coast, and is probably limited in magnitude to a great extent by availa- bility of appropriate refuge habitat for early ju- venile instars at settlement. PRE-RECRUIT SURVIVAL Pre-recruits are defined here as the size cohort that will recruit to the exploitable cohort in the next subsequent year, and for Dungeness crab, this implies male crab in the size interval of about 130-159 mm CW (Smith and Jamieson, 1989b). The conventional assumption is that since male crab greater than 140 mm show evidence of previous matings by abrasion marks on their chelipeds (Butler, 1960; Smith and Jamieson, in press), current minimum size limits (155-159 mm CW, depending on jurisdiction) should pro- tect many crab from capture for at least one breeding season prior to their recruitment to the exploitable size range. The rationale and data used to justify existing size limits were never documented, but in the early 1900s when size limits were first introduced, it is hypothesised that most crab populations were less heavily exploited than at present and that a relatively large proportion of crab significantly exceeded the minimum size limit adopted. In 1954, the mean size of crab sampled by Butler (1960) in Hecate Strait, the location of the largest fishery at that time, was about 173 mm CW, with many crab exceeding 190 mm CW (Fig. 13), Crab this size are seldom caught today in any significant fishery in British Columbia (Fig. 13), although large crab are caught on the outer coast of Wash- ington [mean = about 175 mm CW (S. Barry, Washington State Dept. Fish., Montesano, WA, pers. comm.)] and even larger crab are caught in Alaska. Merritt (1985) reported that the mean CW of commercial crab caught at Bluff Point, Cook Inlet, AK, from 1973-75 ranged from 190-200 mm, but that the very large crab (230+ mm CW) caught when the fishery first began 377 LEGAL SIZE Male =¥ instars Removed by fishing FREQUENCY => T re a T al 90 110 130 150 170 190 CARAPACE WIDTH (mm) FIG. 14. Diagrammatic depiction of a male crab instar size distribution in relation to the minimum legal size limit, and the effect of fishing removal on the ap- parent instar composition of a size frequency dis- tribution, Two instars from Clayoquot Sound, 1985-86, are shown: adjacent u = 129 mm CW (+12 mm CW) and u = 156mm CW (+13 mm CW) instars (from Smith and Jamieson, 1989b). there in 1973 had disappeared. Crab landed in Kachemak Bay, adjacent to Bluff Point and which has been exploited for most of the century, averaged 15% smaller than Bluff Point crabs between 1978-83. In an intensive study of the Tofino, British Columbia, crab fishery, Smith and Jamieson (1989a, b) reported that the recruiting instar size distribution was nearly halved by the minimum legal size (MLS) (Fig. 14). Forty-two percent of this cohort were pre-recruits, and hence unavail- able to the commercial fishery that year. What was surprising, though, was that there was con- siderable evidence (Smith and Jamieson, 1989a) that these pre-recruits had a high natural mortal- ity (M=2.9-4.5), with less than 10% ultimately surviving to legal size. Thus, about 40% of this recruiting cohort apparently never recruited. It is not known if this was a phenomenon unique to the relatively small geographic area involved (about 60 km*) and/or that particular time period (1985-86). Further study, both at Tofino and elsewhere, is currently under way, but because of a lack of settlement at Tofino in recent years and logistic difficulties in conduct- ing an appropriate study in a larger geographic area, these results have not been confirmed else- where to date. Smith and Jamieson (1989a) sug- gested this apparentlyy high mortality might be a result of having recruits being removed from the population in this year-round fishery vir- tually as fast as they recruit (F=5.1-6.9); only 9-16% of recruits are expected to survive more than 90 days. Continuous trapping and release of pre-recrults While fishing for recruits. (current escape port size is not optimal; Jamieson, un- publ.) may have increased their mortality stb- stantially, or there may be some, as yet undetermined, biological explanation. A final consideration 1s the growth history of the recruiting cohort. In the Tofino instance de- scribed above, the MLS divided the recruiting cohort almost equally, but this may not always occur. In some years, mean instar sizes may be such that the MLS falls between distinct, adja- cenl instars, rather than over one instar specifi- cally, resulting in almost the entire pre-recruit jnstar recruiting with its next moult, Any scenario between the above two extremes may occur, resulting in up to a two-fold difference in recruitment of year-classes of similar absolute abundance, This may mostly explain the large average size of recruited crab in the outer coast Washington fishery (175 mm CW) relative to that in the Tofino fishery (about 165 mm CW: Smith and Jamicson, 1989a). SUMMARY The prediction of relative year-class strength at recruitment to the fishery for Dungeness crab, and probably for most species, is nota trivial matter. Limited mobility, pronounced spatial differences in abundance, and a variable en- vironment result in sufficient unpredictability that future estimation of year-class abundance af Dungeness crab to a fishery can only be made with acceptable accuracy from 1+ y-olds. Female abundance, in the absence of any fishery for them and little data on their occurrence be- cause of the use of escape ports, is unavailable. The ultimate settlement location of larval pro- duction ts also unknown. Consequently, tradi- tional stock-recruitment relationships are effectively meaningless for management and have not been determined for this species. Re- search emphasis is currently focusing on dcter- mining and describing the critical environmental conditions (currents, temperature, winds, reluge availability), behaviour (larval distribution in the water column), and population dynamics (growth rate, survival and causes of mortality) in coastal areas having significant regional fisher ies. LITERATURE CITED ARMSTRONG, D.A. AND GUNDERSON, D.R. 1985. The role of estuaries in Dungefess crab early life history: A case study in Grays Harbor, Washington. Proceedings of the Symposium on MEMOIRS OF THE QUEENSLAND MUSEUM Dungeness Crab Biology and Management. Sea Grant Report 85-3: 145-170, BOTSFORD, L.. ARMSTRONG, D. AND SHENKER, J. 1989, Oceanographic influences onthe dynamics of commercially fished populs- tions, chapter | 1, 3) 1-365. In M. R. Landry and B. M. Hickey (eds) ‘Coastal oceanography of the Pacific Northwest’. (Elsevier Scientific Publish- ing: Amsterdam), BUTLER. T.H. 1960. Maturity and breeding of the Pacific edible crab, Cancer magister Dana, Jour- nal of Fisheries Research Board of Canada (7(5)) 641-646, CAPUTI, N, AND BROWN, R. 1986. Relavionship between indices of juvenile abundance and re- cruilment in the western rock lobster (Panielirus cygntus) fishery. Canadian Journal of Fisheries and Aquatic Selences. 43; 2131-2139 CARRASCO, K.R., ARMSTRONG, D.A., GUNDERSON, D.R. AND ROGERS, C, 1985. Abundance and growth of Cancer mugister voung-of-the-year in the nearshore environ- ment, Proceeding of the Symposium on Dunge- ness Crab Biology and Management. Sea Grant Report, 85-3: 273-286. CLEAVER, F.C, 1949. Preliminary results of the coastal crab (Cancer mapister) investigation. Stale of Washington, Department of Fisheries, Biological Bulletin 49-A: 48-82, COBB, LS. AND CADDY, J.F.1989. The population biology of decapods, chapler 15, 327-374, In JF. Caddy (ed,) "Marine invertebrate fisheries: their assessment and management’, (John Wiley and Sons} New York). DEBROSSE, G., SULKIN, 8. AND JAMIESON, GS. 1990). Intraspecific variability in selected morphological traits in megalopae of three sym- patric species of the genus Cancer (Brachyura, Cancridae), Journal of Crustacean Biology. 10(2): 315-329. DINNEL, P., ARMSTRONG, D. AND MCMILLAN, R, 1986, Dungeness crab, Cancer mugisler, dis- tribution, recruitment, growth, and habitat use in Lummi Bay, Washington, University of Wash- ington, Schoul Fisheries Report Number FRI- UW-8612. 6Ip. DINNEL, P., MCMILLAN, R., ARMSTRONG, D., WAINWRIGHT, T. AND WHILEY, A. 1987. Padilla Bay Dungeness crab, Cancer magister, habitat study. University of Washington, School Fisheries Report Number FRI-LIW-8704, 78p. DODIMEAD, A.J.. FAVORITE, F. AND HIRANO, T.. 1963, Salmon of the North Pacific Ocean — Part Il, Review of oceanography of the subarctic RECRUITMENT PATTERNS OF DUNGENESS CRABS Pacific region. International North Pacitic Fish- erjes Commission Bulletin 13: 1-195, DUMBAULD, B.R. AND ARMSTRONG, D.A, 1987. Potential mitigation of juvenile Dunge- ness crab loss during dredging through enhance- ment of intertidal shell habitat in Grays Harbor, Washington. University of Washington. School Fisheries Report Number FRI-UW 87/4. 64p. EATON, M.F. 1985. Kodiak Island commervial Dungeness, Cancer magisier. fishery. Proceed- ings of the Symposium on Dungeness Crab Bi- ology and Management. Sea Grant Report 85-3: 97-118. FREELAND, H.J., CRAWFORD, W.R, AND THOMSON, R.E. 1984, Currents along the Pacific coast of Canada. Atmosphere-Oceun 22: 151-172, GOTSHALL, D, W. 1978. Relative abundance siudies of Dungeness crab, Cancer magister, in northern California. California Department of Fish and Game 64: 24-37, GUNDERSON, D. R.. ARMSTRONG. D.A.. SHI. -BING, AND McCONNAUGHEY. R.A. 1990). Patlerns of estuarine use by juvenile Eng- lish sole (Parophrys verulus) and Dungeness crab (Cancer magister), Estuaries 13; 59-71. HART, J.F.L. 1982. Crabs and their relalives of British Columbia. British Columbia Provincial Museum Handbook 40: 1-267. HATFIELD, S. BE, 1983. Intermalt staging and dis- tribution of Dungeness crab, Cuncer mugisier, megalopae. 85-96. In P. W. Wild and R. N. Tasto (eds) “Life history, environment. and mariculture studies of the Dungeness crab, Cancer magister, with emphasis on the central California fishery resource’. Californta Depari- ment of Fish and Game, Fish Bulletin 172. HICKEY, B.M, 1979, The Californias Current system — Hypotheses and facts. Progress in Oceano- graphy 8: 191-279. 1989. Patterns and processes of circulation over the Washington continental shelf and slope, 41—- 115. In M.R. Landry and B.M. Hickey (eds) “Coastal oceanography of Washington and Oregon’. (Elsevier Scientific Publishing Com- pany: Amsterdam). INCZE, L. ARMSTRONG, D.. AND SMITH, S. 1987. Abundance of larval tanner crabs (Chionoecetes spp.) in relalion to adult females and regional oceanography of the southeastern Bering Sea, Canadian Journal of Fisheries and Aquatic Sciences 44: 1143-1156. JAMIESON, G.S, 1985, The Dungeness crab (Cancer magister) fisheries of British Columbia, Pro- ceedings of the Symposium on Dungeness Crab tet ~ “we Biology and Management, Sea Grant Rep 85(3); 37-60. 1986a, Management and recruitment — the impli- cation of fluctuations in abundance in select crab populations. Canadian Journal of Fisheries und Aquatic Sciences 43: 2085-2098. 1986b. A perspective on invertebrate fisheries man- agement — the British Columbia experience 57-74. In G. S. Jamieson and N, Bourne (eds) “North Pacific workshop on stock assessment and management of invertebrates’. Canadian Special Publication of Fisheries and Aquatic Sciences 92, JAMIESON, G.S, AND PHILLIPS, A.C. 1988. Qe- currence of Cancer crah (C. magister and C. oregonensis) mMegalopae off the west coast of Vancouver Island, British Columbia, Fishery Bulleun 86(3); 525-542. JAMIESON, G.S., PHILLIPS, A.C. AND HUG- GETT, W.S. 1989. Effects of ocean variability on the abundance of Dungeness crab megalopie. 305-325, In R.J. Beamish and G.A. McFarlane (eds) ' Effects ofocean variabilily ontecruitment and an evaluation of parameters used in stock assessment models’, Canadian Special Publica- lion of Fisheries and Aquatic Sciences 108, JAMIESON, G.S. AND SLOAN, N.A., 1985. King crabs in British Columbia. Proceedings of the International Symposium on King Crabs. Sea Grant Rep 88( | 2): 49-62. JENSEN, G.C. AND ARMSTRONG, DA. 1987. Range extensions of some northeastern Pacific Decapoda, Crustaceana $2(2): 215-217. KIMKER, A. 1985. Overview of ihe Prince William Sound management area Dungeness crab lish- ery. Proceedings of the Symposium on Dunge- ness Crub Biology and Management.. Sea Grant Report $5(3): 77-84. KOENEMAN, T.M. 1955. A brief review of the com- mercial fisheries for Cancer magister in south- east Alaska and Yakutat waters, with emphasis on Tecent seasons. Proceedings of the Sym- posiom on Dungeness Crab Biology and Man- agement. Sea Grant Report 83(3): 61-76. LIPCIUS, R, AND VANENGEL, W, 1990. Blue crab population dynamics in Chesapeake Bay: varia- lion in abundance (York River, 1972-1988) and stock-recruit functions. Bulletin af Marine Science 46: 180-194. LOUGH, R, G. 1976, Larval dynamics of the Dunge- ness crab, Cancer magister, off the central Oregon coast, 1970-71, Fisheries Bulletin 74; 353-375. MERRITT. M.F. 1983_ The lower Cook Inlet Dunge- ness crab fishery from 1964-1983. Proceedings 380 of the Symposium on Dungeness Crab Biology and Management, Lowell Wakefield Fisheries Symposium Series. Sea Grunt Report 85(3): 85— 96, METHOT, R. D. 1989, Management of a cyclic resource! the Dungeness crab fisheries of the Pacific coast of North America, 205-223. In J. F. Caddy (ed.) ‘Marine invertebrate fisher- ies! their assessment and management’. (John Wiley and Sons: New York), NICHOLS, J. AND THOMPSON, B. 1988, Quan- litalive sampling of crustacean larvae and its se in Stock size estimation of commercially exploiled species. 157-175. In A. Fincham and P. Rainbow (eds) “Aspects of decapod crustacean biology’. (Clarendon Press; Lon- don) 375p. NICHOLS, J,, BENNETT, D., SYMONDS, D. AND R, GRAINGER, R, 1987, Estimation of the stock size of adult Nephrops nurvegicus (L.) from larvae surveys in (he western Irish Sea in 1982, Journal of Natural History 21: 1433-1450. ORENSANZ, J. AND GALLUCCT, V. 1988. Com- parative study of postlarval life-history sched- ules in four sympatric species of Cancer (Decapoda: Brachyura: Cancridae). Journal of Crustacean Biology 8; 187-220. PACIFIC MARINE FISHERIES COMMISSION (PMFC). 1989, Dungeness crab fishery, 16. In 41st Annual Report, Pacilic Marine Fisheries Commission, (Portland: Oregon). PARRISH, R.H., NELSON, CS. AND BAKUN, A. 1981. Transport mechanisms and reproductive success of fishes in the California Current, Bio- logical Oceanographer 1(2): 175-203 PHILLIPS, B.F. 1986, Prediction of commercial catches of the western rock lobster Panulirus cygnus, Canadian Journal of Fisheries and Aquatics Sciences 43: 2126-2130). PHILLIPS, B.F. AND BROWN, R. 1989, The West Australian rock lobster fishery: research for management. 205-223, In J, F, Caddy (ed,) “Marine invertebrate fisheries; their assessment and management’. (John Wiley und Sons; New York), POOLE, R.L. 1966. A description of laboratary- reared zoea of Cancer magisier Danu and meg- alopae taken under natural conditions, (Decupoda Brachyura), Crustaceana 11; 83-97, 1967, Preliminary results of the age and grawth study of the market crab (Cancer magister) in California; The age and growth of Cancer magister in Bodega Bay, 553-567, In Sym- posivm an Crustacea, Ernukulam, India. 1945. MEMOIRS OF THE QUEENSLAND MUSEUM Proceedings (Part 2) Marine Biological Associa- tion, (Mandapam Camp: India), REILLY. P.N. 1983. Dynamics of Dungeness crab, Cancer magister larvae off central and north- ern California, 57-84, In P. W. Wild and R. N. Tasto (eds) ‘Life history, environment, and mariculture studies of the Dungeness crab, Cancer magister, with emphasis on the central California fishery resource’. California De- partment of Fish and Game, Fish Bulletin £72. SMITH, B.D. AND JAMIESON, G.S. 1989a. Exploi- taion und mortality of male Dungeness crabs (Cancer magister) near Tofino, British Colum- bia. Canadian Journal of Fisheries and Aquatic Sciences 46; 1609-1614. 1989b. Growth of male and female Dungeness crabs near Tofino, British Columbia. Transac- lions of the American Fisheries Society 118: 556-563. IN PRESS. Possible consequences of intense fish- ing for malé Dungeness crab on the molting and size distribution of females. Transactions of the American Fisheries Society, SGULE, M. AND TASTO, R.N. 1983. Stock identi- fication studies on the Dungeness crab, Cancer magister. 39-42. In P. W. Wild and R. N. Tasto (eds) ‘Life history, environment, and maricul- ture studies of the Dungeness crab, Cancer mugister, with emphasis on the central Cal- ifornia fishery resource’, California Department of Fish and Game, Fish Bulletin 172. TANG, Q. 1985. Modification of the Ricker stock recruitment model to account for environmen- tally induced variation in recruitment with par- ticular reference to the blue crab fishery in Chesapeake Bay. Fisheries Research 3; 13-21. TASTO, RN. 1983, Juvenile Dungeness crab, Cancer magister, studies in the San Francisco wreas. 135-154, In P. W. Wild and R. N. Tusto (eds) “Life history, environment, and mariculture stu- dies of the Dungeness crab, Cancer magister, with emphusis.on the central California fishery resource’. California Department of Fish and Gume, Fish Bulleun 172. THOMSON, R.E. 1981. Oceanography of the British Columbia coast. Canadian Special Publication of Fisheries and Aquatic Sciences 56; 1-291, THOMSON, R.E., HICKEY, B.H. AND LEBLOND, P.H. 1989. The Vancouver Island Coastal Cur- rent: fisheries barrier and conduit, 245-296, In R.J. Beamish and G.A. McFarlane (eds) ‘Effects of Ocean variabuily on recruitment and an eval- uation of parameters used in stock assessment models’, Canadian Special Publication of Fish- eries und Aquatic Sciences 108, RECRUITMENT PATTERNS OF DUNGENESS CRABS 381 WARE, D.M. AND MCFARLANE, G.A. 1989. Fish- assessment models’. Canadian Special Publica- eries production domains in the northeast Pacific tion Fisheries and Aquatic Sciences 108. Ocean. 359-379. In R.J. Beamish andG.A.McFar- WARNER, R. W. 1987. Age and growth of male Dunge- lane (eds) ‘Effects of ocean variability on recruit- ness crabs, Cancer magister, in northern Cal- ment and an evaluation of parameters used in stock ifornia. California Fish and Game 73: 4-20. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 382 UNUSUALLY RAPID GROWTH OF COASTAL 0+ DUNGENESS CRAB MAY LEAD TO STRONG FISHERIES Dungeness crab, Cancer magister, is the primary crustacean fishery along the west coast of the United States from northern California through Washington, and is charac- terised by cyclic landings with a periodicity of 9 to 10 years (Botsford et al., 1989), Despite numerous hypotheses to suggest a suite of biotic and abiotic factors as explanations for such cycles, no cause-and-effect relationship has been demonstrated as responsible for high or low year class abun- dance. Although larval production, transport, and settlement to nearshore areas are assumed to be critical for high juvenile abundance, year class strength is often not determined until the 1+ ageclass since mortality of early benthic instars is very high. In previous hypotheses, Armstrong and Gunderson (1985) believed that estuarine recruitment of juveniles was essential to production of a strong year class because growth is more rapid in these systems than along the colder (upwel- ling) open coast, and estimated abundance of 1+ juveniles is usually greater in estuaries compared to the coast. Since 1983 we have measured timing of settlement, growth rates, movement, and relative abundance of juvenile Dungeness crabs along the southern Washington coast in a stratified survey program intended to contrast population dynamics across several habitats within the estuaries of Grays Harbor and Willapa Bay and along the nearshore (inside 70m) coast. During this time we have measured at least two very strong year classes as Ist instar, 0+, crab; one of which had very low subsequent survival and produced an average fishery, and one that produced a record fishery 4 years later. Megalopae settle along the nearshore coast and in estuar- ies, and mortality is generally rapid in both systems. Esti- mates of 0+ juveniles within the survey areas shown by Gunderson et al. (1990) have varied by at least 14 times, and in most years initial summer survival seems to be highest in estuarine intertidal shell habitat. As a consequence of estuarine settlement, 1+ abundance is typically high the following year and this cohort is joined by siblings that immigrate to the estuary from the open coast, thereby decreasing the summer abundance of juveniles in colder coastal waters. Summer estuarine abundance has varied by only about 2 times between 6 to 12 million crabs in a system like Grays Harbor. Year class strength as reflected in the fishery was discern- ible during the period of our study. Six of the worst commer- cial years on record occurred between 1980 and 1987 (1,400-1,800 t), but some of the largest landings for Wash- ington state were in 1988 (7,500 t) and 1989 (10,000 t) which corresponds to a 3.5 and 4.5 year lag back to the 1984 year class (YC) that entered the fishery over a two year period. Reasons for this strong YC are not based on extraordinary events in the estuaries where 1+ abundance was consistent MEMOIRS OF THE QUEENSLAND MUSEUM with values from all other years. Rather, the coastal cohort of the 1984 YC was exceptionally strong and survived well for two apparent reasons. Firstly, the YC settled in strength early that year in May whereas other YC's typically do not fully recruit until late June to early July. The effect of early settlement was essentially a longer growing season. Sec- ondly, bottom water temperatures in May and June were about 1.5°C warmer than six year monthly averages. As a result, 0+ crab of the 1984 YC were about 22-25mm carapace width (CW) by September compared to a range of 12-14mm CW in most years, Substantially larger size by the end of summer protected the 1984 YC from continued high predation that usually decimates a coastal 0+ population by the following spring. Measured as 1+ abundance in spring the year after settle- ment, the 1984 YC ranged in abundance from 29-100 million juveniles along the coast compared to 1-10 million in other years. Thus coastal fisheries of low to moderate yield may be largely based on fairly stable estuarine production of ju- veniles, but very large fishery peaks that characterise Dunge- ness crab could result from auspicious coastal conditions and early settlement that, in this case, led to accelerated growth of coastal 0+ juveniles in 1984. Related to this observation is the perspective that strong onshore larval abundance and subsequent settlement do not often equate to a strong YC since 0+ mortality is extremely high. Larval retention and/or transport onshore is only a first-stage ingredient for a strong YC that is also based on survival of 0+ juveniles. Acknowledgements This work was supported by a series of grants from Wash- ington Sea Grant (NA 86AA-D-SG044) and the U.S. Army Corps of Engineers. We express our thanks to R. McCon- naughey and R. Palacios for help with analyses of these data, and to numerous students who helped in the field. Literature Cited Armstrong, D. and Gunderson, D. 1985. The role of estuaries in Dungeness crab early life history: A case study in Grays Harbor, Washington. Proc. Symp. Dungeness Crab Biology and Management, Sea Grant Report No. 85(3): 145-170. Botsford, L., Armstrong, D. and Shenker, J. 1989. Oceano- graphic influences on the dynamics of commercially fished populations, 511-565. In M.R. Landry and B.M. Hickey (eds) ‘Coastal oceanography of the Pacific Northwest’. (Elsevier: Amsterdam). Gunderson, D., Armstrong, D., Shi, Y. and McConnaughey, R. 1990. Patterns of estuarine use by juvenile English sole (Parophrys vetulus) and Dungeness crab (Cancer magister). Estuaries 13: 59-71. David A. Armstrong and Donald R. Gunderson, School of Fisheries WH-10, University of Washington, Seattle WA 98195, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM ASPECTS OF THE BIOLOGY OF THE HAIR CRAB, ERIMACRUS ISENBECKII, IN THE EASTERN BERING SEA (CRUSTACEA; DECAPODA: ATELECYCLIDAE) The hair crab, Erimacruy isenbeckii, is a medium- sized brachyuran in the family Atelecyclidae. The development of an United States fishery for hair crab in 1979, and the substantial decline of the eastern Bering Sea (EBS) population trom 1481 to 1984 prompted an analysis of hair crab data collected by the National Marine Fisheries Service (NMFS) during trawl surveys in the summers of 1979-1984, and in February 1983 and 1985. Pertinent Japanese literature on the worldwide distribution, reproduction, and moulting of hair crab is summarised. In the eastern Bering Sea, Erimacrus isenbeckti is distributed from the north shore of the Alaska Peninsula to the Pribilof Istands, and north to St. Matthew Island, It also oecurs along the Aleutian Archipelago. In the West Pacific, it is distributed along the east coast of Korea. both coasts of Japan and Hokkaido, and along the Kurile Islands to the Kamtchatka Peninsula (Rathbun, 1930: Vinogradoy, 1947), According to NMFS surveys, [he estimated popula- tion in the eastern Bering Sea was about 23 million crabs (rom 1979 to 1981, bul declined sharply to 4.4 million by 1984 (Olio ef al,, 1985), The majority (67%) of the popu- lauion occurred in the Pribilof Islands area, Male crabs occurred ala mean temperature of 3.4°C and depth of 66 m, Whereas females occurred al a mean of 2.4°C and 64 m. There was no significant difference in mean depths be- tween malas and females, but there was a significant dilfer- ence in mean temperatures at which male and female hair crab were found, Some reproductive information was col- lected from females, which comprised only 8% of the total survey catch. Ovigerous females were 65-87 mm in carapace length and carried from 34,000-—160,000 egys. Females’ gonopores were open, closed with a protei- naceous plug of male origin, or closed With a swollen membrane similar to an arthrodial membrane. depending on reproductive stale of the female. Moulling was much more apparent during the February 1983 cruise than the other cruises; 30% of the females and 20% of the males were either softshell or in the process of moulting. The mean length of males was 96 mm and the mean weight 383 was about 714¢. The mean size of females was much smaller than for mules; they averaged 66 mm in length and 197 g in weight. Hair crab have been fished around Japan and Korea for more than 60 yrs (Kawakami, 1934). The United Stales fishery began in 1979 and occurred incidental to the Bering Sea tanner crab fishery during the months of March through June. The Pribilof area contributed 94-98% of the catch (Griffin and Dunaway, 1985), which was taken with commercial king and tanner crab pots. The decline of the Bering Sea hair crab population coincided with the substantial declines of king and tanner crabs. These declines may have resulted from changes in the environment, increased predation, increased incidence of disease, or vulnerability to fishing pressure. Additional information on maturity, growth, and mortalily is impor- tant for a more complete Understanding of the biology of the hair crab. Literature Cited Griffin. K. and Dunaway. D. 1985. Bering Sea area shell- fish management report to Alaska Board of Fisher- ies, 179-245. In ‘Westward region shellfish report to the Alaska Board of Fisheries’. Kawakami, S., 1934, Survey forhair crab, Ten-day Report, Hokkaido Fisheries Experimental Laboratory. 238/259: |-16, Otto. R.S., Stevens, B.G.. MacIntosh, R.A.. Stahl-Johnson, K.L. and Wilson, S.J. 1985. United ‘States crab re- search in the eastern Bering Sea during 1984, Inter- national North Pacific Fisheries Commission, Annual Report 1984: 47-59, Rathbun, M.J., 1930, The cancroid crabs of America of the families Euryalidae, Portunidae, Atelecyclidae, Can- cridae and Xanthidae. United States National Museum Bulletin 152: 1-609. Vinogradov. L.G., 1947, Decupod crustaceans of the Ok- hotsk Sea. Izv. Tikhookean. Naukno-Issled. Inst. Rybn, Khoz. Okeanogr., XX V_ 100 p. [Translation]. Therese M. Armetta, Washington Dept. of F.isheries, 1000 Point Whitney Rd, Brinnon, Washington 98320, USA, Bradley G. Stevens, Alaska Fisheries and Science Center, Kodiak, Alaska 99615, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum THE IMPACT OF STAGHORN SCULPIN PREDATION ON NEWLY SETTLED DUNGENESS CRAB During laie spring/eatly summer, vasy numbers of Dunge- ness crab (Cancer magister) megalopae reach estuaries and settle on inlertidal flats, and during the next two months the crab population is rapidly culled by predation and cannibal- ism. Crab without appropriate refuge hablrar are highly vulnerable to predation by fish and birds and accordingly survival of young crab is highest in shell and eelgrass beds, Staghorn sculpin (Leptocortus armutus) known to be gener- alist, Opportunistic predators wilh large gapes. have high estuarine abundance, and are distribuied (hroaughoul estuaries as crabs seitle and moult to Ist instar. The objective of this study Was (O assess the potential impuct due to slighorn seulpin predation on newly settling Dungeness crab in the Washington coastal estuary of Grays Harbor. Staghorn sculpin and Dungeness crab population dynam- ies have heen followed by monthly trawl] surveys from April io September in 1983 through 1989. Young sculpin are found in the upper reaches of the subtidal channels and crecks, and migrate to deeper channels of the bay as they grow. Sculpins sumpled by our gear ranged in size from 60) to 231} mm TL, and all sculpin greater than or equal jo 80 nym TL were found tu be capable of consuming newly settled crabs which com- prised similar proportions of the diet of Iwo size groups of sculpio in our samples. The summer diet of staghorn sculpin composition was assessed by a series of 6 trawling trips in April through August, 1989 Stomach contents of sculpin trom these monthly collections were analysed by a modified Index of Relative Importance (Stevens eral., 1942). The sculpin's diet consisted of amphipads (46%), cranganid shrimp (24%), and small fish (12%) in April and Ca/lianusse sp, (45%) and nercid polychaetes (37%) in May betore crab setilement, In early June as crab became available, sculpin switched 10 nereid polychaetes (60%) and Dungeness crab (23%) as their primary food. In July and August, Callianasya and Upogebia sp., (wo species of mud shrimp, and C. magister were the three major items of diet, By pooling the results of all stomach content analyses from April to August, it was deler- mined that C. magister farmed 9% of the total summer diel of staghom sculpin in Grays Harbor, It should be noted that the IRI index is a composite of frequency of occurrence, numerical and gravimetric percentages and thus a conscrva- ilve measure of dietary importance in this case. Staghorn sculpin are opportunistic feeders. This is shown hy shifts in monthly diet that reflect prey availability, These fish have relatively high food requirements for fapid estuarine growih during warm summer months when waler temperatures reach 14~16°C. Percent wut fullness (bv visual assessment) was routinely high (>50% to distended) anu MEMOIRS OF THE QUEENSLAND MUSEUM mean put contents Were calculated at 7% of dry fish body weight, Interannual variability in sculpin populations was examined from 1983 to 1988 and peak summer populations ranged irom | to over 3 million seulpin, with a six year mean estimated to be 2 million fish. To assess the potential impact of sculpin predajion on crabs, energetic requirements were used lo derive an estimate and then tield data were used to substantiate the parameters. An average size sculpin of 120 mm TL (20.49 wet wt, 4.1 g dry wt) would consume 7% of its body weight per day (0,3 g dry wi) asa daily ration, If 10% of the total summer diet is Dungeness crab, then sculpin would consume 0,03 g crab dry weight per day. Gutermuth and Armstrong (1989) calculated the dry weights of Dungeness crab instars, Thus the daily raion of erab is equivalent to either 2 first instars, | second instar or O.5 third instars, This pattern and frequency were substantiated by examining the number and stage of crab consumed by sculpin from carly June to late July. As the instar sizeé increased the number of instars eaten per fish decreased. Two scenarios of sculpin impact look into.account variation in crab settlement period, crab moult frequency, proportion of daily ration composed of specific crab instars, and numbers of resident sculpin. Extremes in the different scenarios predicted staghorn sculpins could consume he- bween 158 and 180 million newly settled Dungeness crab during June and July. Armstrong ef al. (1987) have estimated (hal the average estuarine population of newly settled Dunge- ness crab is about 400 million which is reduced ta between 20 and 40 million juvenile crab by the end of the summer, Thus, of the 360 million crab lost during summer, staghorn sculpin predation aceounts for approximately 44 to 50% of the loss. Literature Cited Armstrong, D., Wainwright, T., Orensanz, J., Dinnel, P. and Dumbauld, B. 1967. Model of dredging impact on Dungeness crab in Grays Harbor, Washington, Univer- sily of Washington, School of Fisheries Report No. FRI-UW-8702. 167p. Gulermuth, F. and Armstrong, D. 1989. Temperature-de- pendent metabolic response of juvenile Dungeness crab Cancer magister Dana: Ecological implications for estuarine and coastal populations. Journal of Experimen- tal Marine Biology and Ecology 126; 135-144. Stevens, B., Armstrong, D. and Cusimano, R, (982, Feeding habits of the Dungeness.crab Cancer magister as deter- mined by the index of relative importance, Marine Bl- ology 72: 135-145, Janet L. Armstrong, David A. Armstrong, and Paula. Dinnel, School of Fisheries, WH-10, University of Washington, Seatile, WA 98195, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 38 SOME BIOLOGICAL ASPECTS OF THE GIANT ISOPOD, BATHYNOMUS GIGANTEUS (A. MILNE-EDWARDS) (ISOPODA: CIROL- ANIDAE), OFF THE YUCATAN PENINSULA Specimens of the giant isopod, Barhyvnomus giganteus (A. Milne-Edwards), were collected on the continental slope off the Yucatan Peninsula, Mexico, in October 1985 (74 isopods). February 1986 (70), August 1986 (64), August 1989 (163) and February 1990 (1280), The isopods were collected with traps baited with skipjack tuna and large carangids, Depth of collection ranged from 350 to 730 m. In the deepest station, only mancas and juveniles were obtained. Size distribution ranged from 4.4 cm to 36.5 cm total length. A 36.5 em male is the largest specimen of this species so far recorded. Male- female ratio varied in each collecting date, from 0.8:1 to 1.7:1. Mature males and females were obtained in every collecting date. Length-weight and length-width relation- ships were obtained. Specimens collected in August 198Y and February 1990 were studied in more detail, In August, 35% of the males had appendices masculinae, and 14% of the females showed fully developed oostegiles, In February. these percentages were 50 and 45, respectively. Both the smallest mature male and female measured 21 cm, No ovig- erous females were caught in any cruise. An ovarian develop- ment scale was designed, ranging from stage | (quiescent ovaries) to stage 5 (spent ovaries with ovociles in resorption). Tn August, a large percentage of females showed ovaries in intermediate stages 2 and 3, while in February, the ovaries of most of the females were in stages | and 4. These results suggest a differential distribution of life stages on the bollom. hn An exponential relationship between body length (BL) and body weight (BW) was found (Log. BW.=-1.43 (BL) + 2.96; n = 515, r = 0.998). Although males with appendices masculinae and females with developed oostegites were found from every collecting date, the analysis of ovarian development indicates that in August most females are pre- paring for reproduction, while in February most of this reproduction has taken place. The large number of mancas (554) collected in February also support this idea. In gul content analysis, the following groups were identi- fied: fish, cephalopods, decapods, isopods, sponges, echino- derms, nematodes and tunicates. No differences were found in the diet composition between sexes. B. giganteus is re- ported as a scavenger, but these results show that it also feeds on some sessile organisms on the bottom, A large female was found in the stomach of a tiger shark, Galeocerdo cuvierii. In regard to epizoans, the cirriped Octolasmis aymonini geryonophyla was found in a large percentage of isopods from every cruise. In February 1990, the gastropod Mitrella rushit was found in large quantities inside the oostegites of a number of females, but also on the coxal plates and pleopods of some males. This is the first record of this association, but their relationship is not clear. Epizoans were more abundant on females than on males which suggests that they have a lower moult rate than males. P. Briones-Fourzan and E. Lozano, Institute Ciencias del Mar y Limnologia, Estacion ‘Puerto Morelos’, Universidad Nacional Autonoma de México. Ap. Postal 1152, Canctin, O.R., 77500 México, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum GROWTH AND REPRODUCTION OF TWO SPECIES OF SPIDER CRAB (BRACHYURA: MAJIDAE} Brachyuran crabs, and decapod Crustacea generally. display @ ereal diversity of growth-réproductive patterns (Hartnoll. 1985). The Majidae are more constrained thun most other brachyuran groups, as the females are limited to a Single mature instar (Hannoll. 1963, 1985), The processes of growth and reproduction are therefore temporally separate. These species are nol, however, fully semelparous as females may lay several epge batches in the terminal instar. This study considers the female life history of two majids, Ayas courcratus and Inachus dorsettensis. Reproduction in the field and growth mn the labora- lory have been studied in relation to the Known phenology of their life-cycles, A life history strategy model currently applied to a different species is described also, to which the results af this study are to be applied. Animals were collected at sites where the two species co- exist in the Irish Sea, 54° N. The offshore water temperature there is at.a minimum between February and March and at a maximum between August and September. The two species have contrasling life histones. H. courctatus females start to mature their ovaries in January, prior to the terminal moult which occurs mainly between May and July, Mating and epg laying follows immediately. After 9-11 months, the following March to April, eggs are hatched and the females which survive then lay a second batch. |. dorsettensiy females mature their ovaries only after the terminal moull, which occurs between July and September. After a short delay for ovarian maturation the first egg batch is laid in autumn, Ege development time is relanvely short, allowing a second batch 10 be laid in early spring. Egg development is not synchronised with (he seasons in this species, Fecundity of the females was assessed using a dry method. In H. coarctatus a strong relationship was found between ege number and the cube of carapace Jength. /. dorsetrensis had a double fecundity curve, Samples taken in the autumn, when most animals would have been carrying their first batch ofegys, gave a shallow curve. In the spring, when the animals would have been carrying their second or subsequent batch, 4 signifi- cantly si¢eper curve was obtained. It Would appear theretore that fecundity is low for the first batch of eggs, despite the animal delaying ovarian maturation until the final and largest instar. The growth experiment was performed in the laboralory aver 500 days, with the temperature mimicking thal of the sea through the seasons. The results, in (he form of the percentage moult increment and inlermoult period, were analysed in rela- MEMOIRS OF THE QUEENSLAND MUSEUM tion to the size of the animal and the temperature, treating juveniles and animals moulting to maturity separately where appropriate, In H., coarctatus. the mean percentage increment was srgnif- icantly smaller for maturity moult than for juvenile moults. This may be related to the early diversion of resources to reproduc- tion in this Species, Percentage increment showed a significant nogalive correlation with temperature, but only for juvenile moult, Intermoult period was positively related to carapace length and negatively correlated wilh temperature. Tn direct contrast, 1. dorsettensis had a greater percentage increment at the maturity moult than at its juvenile moults. This may be tentatively interpreted as a strategy for maximum body size in the final instar. in which to develop its ovaries, The maturity moult was undergone al a significantly higher temperature (han the juvenile moults, a result which agrees well with the known phenology of this species, Intermoult period was found to be negatively related to temperature but unrelated to carapace length. These results will be applied to the model of Hartnoll and Gould (1988). At present this model describes. the life history of a crab species which conlinues moulling after puberty, It is aimed to predict how lifetime egg production varies with the precocity of reproduction and lifespan, both measured as the number of instars. A second aim is lo observe the change in optimal strategy, wilh respect Lo lifetime egg production, when the mortalily assumptions are varied. Application of the spider crab dala to the model will allow a comparison of predicted optima with jhe observed natural life history and the investiga- lion of the effect of mortality on life history strajegy. Acknowledgements The author was supported by a Natural Environment Research Council studentship and is supervised by Dr R.G. Hartnoll, Literature Cited Harinoll, R.G. 1963. The biology of Manx spider crabs. Proceedings Zoological Society London 141 - 423-496. 1985. Growth, sexual maturity and reproductive outpul, 101- 128, In A.M. Wenner (ed.) ~ Crustacean growth: Factors in adult growth’. Crustacean Issues 3. (A.A, Balkema: Rotlerdam). Hannoll, R.G. and Gould, P. 1988. Brachyuran life: history strategies and the optimisation of egg production. Sym- posium Zoological Society Landon 59; 1-9. Andrew D. Bryant, Part Erin Marine Laboratary, University of Liverpool, Isle af Man, UR. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM ROLE OF FILTER-FEEDING CRUSTACEAN ZOOPLANKTON IN DUTCH LAKES OF VARYING DEPTH AND TROPHY Most freshwater lakes in The Netherlands are man-made. small (area 50-200 ha). shallow (mean depth 1-2 m) and highly eutrophic. The major symptoms of the eutrophicanon are: 1) high standing crop of seston (phytoplankton and detritus) (10-20 mg DW.L |) comprised mainly of filamen- tous blue-green algae; 2) high chlorophyll a levels (100- 300ugL"'); and 3) poor under-water light climate (Secchi-disc transparency, 30-50 cm). The mésotroptiec lakes, which are relatively less common are. on the other hand, deep and exhibit summer stratificalion; they have much lower algal and detrital concentrations. and the light pene- trates to deeper layers, Recently, allempts have been made ta restore some of the eutrophic lakes (Loosdrechl Lukes) by reducing the external phosphorus loading (Van Liere et al., 1990). In many other smaller lakes biomanipulation has been attempted as a lake rehabilitation measure (Gulati, 1990a, b). These tesiuration measures offered a good opportunity to follow the course of changes in the structure and grazing of crustacean zooplankton. Results and Discussion There are major differences between the two trophic cate- gories of these Jakes in the composition, size structure and grazing activities of the crustacean zooplankton. In the shal- low, eutrophic category larger-bodied crustacean filter feeders. wiz. Daphnia species (>1.5 mm). ave generally scarce, or even absent; instead, the smatler-bodied. filler- feeding crustaceans, (Bosmina longirostris, B. coregoni. D. cucullata and Chydorus sphaericus) are abundant, besides 3-5 species of cyclopoid copepods. Lis puzzling. however, that one Daphnia species, D. hyalina, which invariably coex- ists with D. cucuifata in both the eutrophic lakes and me- sotrophic lakes, is absent in several other eutrophic lakes (Gulati, 1990b). The calanoid copepod Ewdiapromus gracilis 18 an important indicator of trophic status, being sparse or absent in eutrophic lakes. The limnetic zooplankton of (he eutrophic Jakes is dominated by rotifers which, with their mean-densities ofc. 4000 ind.’ outnumber the crustaceans by 9 to 1. The size structure of crustacean Community also differs: in the mesotrophic lakes the mean crusiucean size is larger (3-11 ug C.ind’’) than in the eutrophic lakes (0.65 ug Cind"'). Biomass relationships between the crustaceans and their sestonic food (< 150 jim) indicates a Monod type of relationship with an initial part of the curve in which the zooplankton responds linearly to the seston increase lo about 2mg C.L". observed in the mesorrophic and biomanipulated 387 lakes. Anseston levels of 3-4 mg C LL the zooplankton mass (0.4 mg C,L"') reaches a saturation level. At higher seston levels (4-10 me C. chy, the food is dominated by blue-green algae. so that zooplankton mass tends to decrease rather than increase, possibly due to the inhibitory effects of the food. The structural differences between the crustaceans in these lakes are attributable to differences in the intensity of the size-selective predation or on the larger-bodied crustaceans by planktivorous fish. These fishes. especially bream (Abramis brama),and other young-of-lhe-year planktivorous fish, are far more abundant in the eutrophic lakes than in the mesotrophic and biomanipulated lakes. Experimental bi- omanipulation, i.¢. artificial reduction in planktivorous fish, of alternatively increase in piscivorous fish. in some of the smaller eutrophic waters has led to the appearance of and dramatic increases in large-bodied Daphnia species. These changes generally go hand in hand with corresponding differ- ences in the grazing pressure of the tiler-feeders. The specific filtering rates (filtering rates per unit body weight. mg zoop. C) in the deep mesotrophic lakes (1-3.5 mg zoop. C.L') are 219 5 limes higher than in the eutrophic lakes, The crustacean zooplankton js thus an important causal factor in the phytoplankton mortality in deeper lakes. In the eutrophic lakes, on the contrary. the seston standing crop is high, dominated by filamentous blue-greens which are poorly edible, The smaller-sized crustacean zooplankton which dominate in the eutrophic lakes is much less effective in grazing down the food than the larger-bodied species in the mesotrophic lakes. To eliminate the daily phytoplankton primary production in the eutrophic lakes (e.g. Lake Breukeleveen.in the Loosdrecht area) about 325 ind.L.d"! of the crustacean grazers are required, compared with waly about one-tenth of this number needed to remove the daily production in the mesatrophic and biomanipulated lakes. Literature Cited ‘Gulati. R.D. 1990a, Zooplankton structure in the Loosdrecht lakes in relation (o trophic Slaltus and recent restoration measures, Hydrobiologia 191; 173-188, 199()b. Structure and grazing respanses of zooplankton com- munity (0 biomanipulation of some Dutch water bodies. Hydrobjologia 19%; 200-201; Van Liere, L., Gulati, R-D. Wortelboer, P.G_ and Lammens, E.H.R.R. 1990. Phosphorus dynamics following restora- tion meusures in the Loosdreche lakes, Hydrobjologia 19: R7-95, R.D. Gulati, Limnological Institute, Rijksstraawee 6, 363] AC Nieuwersluis, The Netherlands. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 398 NATURAL DIET OF CALLINECTES ORNATUS (BRACHYURA; PORTUNIDAE) IN BERMLDA Foregut contents of 56 specimens of Callinectes arnatus (8,8-51.8 mm carapace length) collected trom Mulley Bay, Bermuda in 1981 and (988 were examined. Foreguis which were = half full (91,1%) contained more prey items per gut (X = 4.67) than did guts = half full (X = 2.73). Dictary analysis was based on two methods; (1) the index of relative importance (IRI), which combined frequency of occurrence (FO), percentage of total blomass (GC), and percentage ot lolal numbers consumed (NC). and (2) weighted points (PTS), which combined FO and estimated relative volumes of each prey item. No signiticant differences were revealed in relative proportions of foregur contents beiween males and females, or between adull and juvenile crabs. This crab is an OpportuMisic predator of slawly moving benthic macroinvertebrates, specifically gastropod malluses. Pier was related in prey avallabliiy, Modulus moduli, a cerithiacean gastropod that grazes algae and Tralassia, dom- inated the diet, accounted for 21.1% of the rorl IRL Two other cerithiaccans collectively tanked socund (19.96) of loll IRI). All species were common in Mullet Bay. Car- bonate substrate was (he mosl (frequently occurring category (51.79%) and ranked third in [RI (17.2% of total). Whele MEMOIRS OF THE QLEENSLAND MUSEUM many studies of crustacean diet relegated such ennties 1 a A-NutfiHOnal status, Other papers documented the presence of diverse microscopic and meiohenthic organisms In coral sand substrates, Because the biomass cun be relutively high in such substrutes, they should be regarded as a potentially important food souree, and considered part of the diel. Plant milteridl, crustaceans, nereld polychaetes, fish, and bivalve Molluses ranked fourth though eighth in IRL The PTS index is better suited for foods consisting of uw high proportion of sott tissue, FO ls appropriate for most foods, but tends 1 elevale the importance of unidentifiable material, sand, and small animals occurring frequently, but in smal! amounts. Errors die to accumulation of material that Is digested of cleared slowly oveurs in both methods. While ao one quan- lilulive method ts ideal for assessment of dictary analysis in Hrachyurans, the (RI value has 4 greal deal of merit, Because IRI Is based on three other indexes, itis possible ky determine the relative impact that each component Index has wn the total IRI for the dietary items, and because the PTS method has been Widely accepted, i is fecomimended that future dietary studies of brachyorans be designed to incorporate all indexes. PLA. Maefner, de, Deparrment of Biology, Rochester Jastitute of Tecknolegy, Rachester, NY, USA. THE LIFE HISTORIES OF THE TASMANIAN FRESHWATER CRAYFISHES OF THE GENUS ASTACOPSIS (DECAPODA: PARASTACIDAE) The life histories of the two poorly understoud members of the Tasmanian endemic freshwater crayfish genus Asta- copsis wore studied in their natural habitats. A. gould, the world's largest freshwater crayfish, and therefore (reshwuter crustaceyn, is cupable of reaching very large size (3 lo 4 kg) and is restricted to the rivers of the north of Tasmania while the smaller A, franklin? (up to 1 kp) is Widesproud in rivers and Jakes throughout the siale (Swain ev al,, 1982), Both species are generally associated with swill and cuol riverine or highland lacustrine habitats. Male and female seasonal reproductive and moulting cycles, malting, spawning and larval development, were investiguled through intensive monthly sampling and mark-récapiure pro- gramme from Seplember 1985 to May 1987 (Hamp, 1990) A portion of each caich was preserved for subsequent gonad analysis in the laboratory Results. Matore females of A, gouldi mate and spawn in April May. eggs are carried over winter, hatch in January and young stay aached unl late into the tollowing summer (March-April), After the release of their broods. females overwinter, then moult in mid-summer (January-February | and mate and spawn again in autumn, bvo yours after their previous mating. Similarly, A, franklinel mate and spawn in April-May, eggs are carried over winter, hatch in January, and young stay attached until well into the follawing autumn (April-May). Aduli femules of Asracapyis therefore exhibit i biennial breeding and moulting cycle, This sirategy results in bwo distinct female reproductive groups: |. reproductive, or (hose moulling. mating and spawning in 4 given summer and, 2. non-reproductive, or those incubating young and larvae ina given summer, These iwo groups cin be vasily separated Gn the basis of ovary development, presence of Cggs or young, moult stage and the condition of secondary sexual characters such 4s glair glands and ponopore and pleupodal setation. Representatives of the two reproductive groups occurred in collections hroughou) the duration of the study. In males of both species, sperm Was found within (he vasa deferentia from February a May Sperm tubes began forming in February, their number peaking in early May and then decreasing through the winter, Unlike females, males appear to breed every year. The gonads of reproducing females and males therelore show synchronous eyelic development with peak development occurring just prior to the mating season. The postembryonic development in Aste- copsts cansisis of four morphologically distinct larval stages and appears to be significantly different from other para- slicids as well as astacids/cambarids The development sequence is considered lo be primitive in having retained some of the ancestral marine larval ehyracters in particular the four developmental stages, and early differentiation of swimming appendages in the form of # fall fan, Literslore Cited Harr, P. 1990, ‘The comparative reproductive bidlegy of the Tasmanian freshwater craylishes Ayiacapsis wouldi Clark, Astacopsts frankliui Grey and Parastacoides tasmanicus Clark (Decapoda: Parastacidac)” Unpub- lisned Ph_Ty. thesis, Department of Zoology, University of Tasmania, Swain, R., Richardson, A.M,M. and Hortle, M. 1982, Revision of the Tasmaninn genus of freshwater crayfish Astacopsis Huxley (Decapoda: Puraslucidae). Austratian Joumal Marine and Freshwarer Research 33; 69-709, Premek amr, Department of Zoology, University af Tasmania, GP.Q. Box 252C, Mobart Tasmania 7001, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM IMMIGRATION OF METAPENAEUS STEBBINGI, M.AFFINIS AND M. MONOCEROS JUVENILES IN THE CREEKS AND BACK- WATERS NEAR KARACHI Metapenaeus stebbingi, M. affinis and M, monoceros inhabit the northern Arabian Sea and contribute significantly to the Pakistani fishery. The immigration and life cycles of these species were studied in four localities: Korangi Creek, Bham- bore Sandspit and Hab Delta during 1979. These are all muddy. mangrove areas near Karachi City, with a temperature range of 16°-33°C . Salinities were generally high during winter (December—January) and spring (37-39 ppt) due to the pro- longed dry season. Lower salinities (29-30 ppt) in summer were caused by southwest monsoon rains and in winter due to the occasional northeast monsoon. The growth rates in the four species were determined by rearing these in the laboratory so as to know their age when caught. M. stebbingi were caught round the year in Korangi Creek with a peak from July to September and secondary peaks during February—March and November (early winter), a July peak in Hab Delta and a November peak at Sandspit. In general larger 10-14 mm C.L. individuals were abundant during winter and smaller 3-9 mm during spring and summer, Recruitment gener- ally occurred during late summer (July—October) and early winter (November-December). Juveniles of this species are abundant in areas where high salinity prevails, like Korangi Creek and Mekran coasts, but are insignificant in areas where there is great variations (0-40 ppt) as in the Indus Delta (Hassan, 1989). The species spawns throughout the year with a peak during May-July. Peaks of abundance in M. affinis occur during summer al the four localities, with highest in Korangi Creek and lowest at Sandspit. Larger 8-12 mm were more frequent during winter (January-February) and late summer (September—October), and smaller 3-7 mm during spring (April) and summer. This species in less abundant in areas where high salinity prevails (30-36 ppt) but recorded in very large numbers further south in the Indus Delta where there are great variations in salinity (0-40 ppt, Hassan 1989). The species spawns throughout the year with peaks during February—March and recruitment generally oc- curring from April to July. M. monoceros juveniles were present in the study area in smaller numbers than other species at the four localities, and only during April to October, with a peak during May—June. The species spawns from January to July with recruitment occurring during summer. It is typically abundant off the coast of Pakistan (Golobov and Grobov, 1969; Zupanovic, 1971). It seems that juveniles of this species prefer low or moderate salinities as George (1971) reported great abundance in low saline estuaries and paddy-fields in India. A temporal partitioning is apparent between M. affinis, M. monoceros and M. stebbingi related to spawning cycles. In the former the spawning is in spring and in the latter summer. This is similar to M. endeavaouri and M. dalli in Dugong River (Coles and Long, 1985) and to M. bennetae and M. macleayi in Moreton Bay (Young, 1978; Dall, 1958). 389 Life Cycle Metapenaeus spawn at sea and enter the creeks and back- waters when 15—20 days old and 1 mm C.L. They continue to move to and fro with tidal currents and generally settle at one month old and 3 mm C.L. (Hassan, 1983, 1987b, 1989). Ju- veniles grow for about 4 months before migrating back to sea at 12-16 mm. Sub-adults spend about a month in the deeper waters of the same locality, or shallower shelf, and attain 20 mm. They continue to grow and mature as they spread into deeper waters and spawn when 7 months old (20-30 mm). However, the bulk of the cohort spawn at 30-35 mm C.L., when 10-12 months old (Zupanovic, 1971; Garcia, 1985). Acknowledgements I express my deep sense of gratitude to Dr M. Ahmad, Dr F.R. Harden Jones, Dr D.I. Williamson and Dr A.B. Williams for comments and suggestions. Literature Cited Coles, R.G, and Long, W.J.L. 1985. Juvenile prawn biology and the distribution of seagrass prawn nursery grounds in the southeastern Gulf of Carpentaria. Second Australian National Prawn Seminar: 55-60. Dall, W. 1958. Observation on the biology of the greentail prawn, Metapenaeus mastersii (Haswell) (Crustacea Decapoda;Penaeidae), Australian Journal Marine Fresh- waler Research 9(1): 111-134. Garcia, S, 1985. Reproduction, stock assessment models and population parameters in exploited penaeid shrimp populations. Second Australian National Prawn Semi- nar: 139-158. Gorge, M.J. 1970. Synopsis of biological data on the penaeid prawn M. monoceros (Fabricius). FAO Fishery Report 57 (4): 1539-1557. Gololobov, J.A. and Grobov, A.G. 1969. The fishery inves- tigations of Azcher NIRO in the northern part of the Arabian Sea. (Pakistan): I & II, 252p. Mimeo. Hassan, H. 1983. ‘Distribution and abundance of penaeid larvae in the coastal waters of Pakistan’. Ph.D. thesis, CEMB, University of Karachi. 288p. 1987. Distribution and abundance of penaeid larvae on the shelf adacent to Korangi Creek and Manora Channel. Proceeding 7th Pakistan Congress of Zoology: 193-197. 1989. Distribution and abundance of penaeid juveniles on Mekran and Sind coasts. Pakistan Journal of Zoology 21(2): 147-152. Young, P.C. 1978. Moreton Bay, Queensland: A nursery area for juvenile penaeid prawns. Australian Journal Marine Freshwater Research 29: 55-57. Zupanovic, S, 1971. Shrimp explorations off the coast of west Pakistan. Report FAO/Marine Fisheries Department. 88p. Habib-ul-Hassan, Institute of Marine Sciences, University of Karachi, Karachi-32, Pakistan. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 390 GREGARIOUS SETTLEMENT BY PORCELAIN CRABS, PETROLISTHES (ANOMURA; PORCELLANIDAE) The planktonic larvae of many marine invertebrates setile in response (0 Specific cues (Meadows and Campbell, 1972: Scheltema, 1974), but the means by which postlarvae at de- capod Crustacea identify and select appropriate hubjtals ure largely unknown. A series of Held and laboratory experiments were conducted to examine settlement patterns by megalopae of the porceiain crabs Petrolisthes cinetipes and P. eriomerus. which often display distinct, non-overlapping imiertidal dis- tributions when they co-oceur. The adult vertical distributions are due to abiotic factors, sensitivity to thermal stress during aerial exposure confines P. eriamerus to the low intertidal. while the distribution of P. cinetipes is correlated with substrate composition (Jensen, 190). These patterns are maintained in part through gregarious settlement by megalopae of both spe- cies; megalopac were induced to settle in response to caged conspecific adults transplanted above or below their normal range (Jensen, 1989), Subsequent ipvestigalions have focused on the means by which conspecific adults. afe located, and possible post-settlement benefits of associating with adults, Ina field experiment, adult P. eriomterus were contined to chambers placed beneath concrete patio blocks. These cham- bers were screened in. a manner thal prevented either tactile or visual contact by megalopae, while similar chambers without crabs served as controls. Significantly more megalopue oc- curred on the (reatment blocks as compared to interspersed controls, suggesting that a waterborne cuc ts inyolved. Laboratory observations revealed thal contact with adults iniliales a sequence of behavioural and morphological changes including a. loss of forward swimming behaviour. changes in color, and degeneration of the pleopnds, all fea- tures consistent with ensuing metamorphosis lo first instar. Petralisthes cinctipes megalopaé (obtained by holding zoeae caught in plankton tows) placed individually in containers with adults completely settled within 24 days while those in control eatments without adults continued to swim strongly for 2 weeks; in some individuals lhe swimming response persisted for as long as 3 weeks (Fig. 1). This Supgests an extended period of competency io seltle, an important consideration since upon moulling froma zoea into the megalopa stage an individual could be anywhere from tens of metres to tens of kilometres from share, After settle- ment, juveniles continue fo remain intimately associated with conspecific adults for at least a year, hiding beneath (hem or between their legs. Clustering wilh adults probably reduces predalion by interlidal fishes, as. the megalopae of these species are relatively slow moving and do not demonstrate other defensive tactics such as burying in the substrate. Ina laboratory experiment, juveniles with conspecific adults suffered significantly less predation compared 10 those with adult congeners or in controls with no adults. There are indications that two species of porcellanids of the genus Pachycheles also behave in o similar manner (Jen- son, 1990), and while adul-mediated setllement inihese MEMOIRS OF THE QUEENSLAND MUSEUM mean seconds swimming/minute o 5 10 1§ 20 2s DAYS FIG, L. Mean swimming times (seconds/minute, 1 sd) for P- cinetipes megalopae confined with adults (treatment) or held alone (control). filler-feeding speécies is admittedly a special case, gregarious settlement could be widespread among deposit-feeding or her- hivorous decapods. Species that are likely candidates should mee} 3 criteria (hal are compatible with this ype of selective seulement: |) adults and juveniles occur together; 2) they should have relatively specialised habitat requirements; and 3) a minimal tisk of cannibalism. Gregarious settlement could be advantageous even among potentially cannibalis- lic species, provided the benefits of proper habitat selec- lion outweigh the risks, or settling postlarvae are too small to elicit alfack, IL is unknown to what extent the benefits of such close association with adult populations may be offset by increased intraspecific competition. This study provides evidence of a settlement competency pedod for porcellanid megalopae, and subsequent benefits of gregarious settlement. More importantly, it demonstrates seitlement in response to a specific cue, a widespread phenom- enon in other invertebrate larvae bul nol previously demon- strated for decapod crustaceans. Literature Cited Jensen, G.C, 1989. Gregarious settlement by megalopae of the porcelain crabs Pefrealisthes cinctipes (Randall) and P, erfomerus Stimpson, Journal of Experimental Marine Biology and Ecology 131; 223-23), 1990. ‘Intertidal zonation of parcelain crabs: resource partitioning and the role of selective selement’- Disser- lation. University of Washinglan, 11 1p, Meadows, P,S, and J.f. Campbell, 1972. Habitat selection by aquatic invertebrates. Advances in Marine Biology 10; 271-382, Schellema, R, 1974, Biological interactions delermining larval setilement of marine invertebrates. Thalassia Jugoslqvica 10; 263-296, Gregory C, Jensen, Seheol of Fisheries WH-10, University of Washington, Seaitle, WA 98195, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM VERTICAL MIGRATION OF THE EDIBLE CRAB, CANCER PAGURUS (CRUSTACEA: DECAPODA: BRACHYURA), ON ROCKY SHORES OF THE SOUTH COAST OF NORWAY Crustacean foraging activity in the intertidal zone during high tides, and sheltering in subtidal areas during low tides, has been noted on numerous occasions by many authors. Besides the study by Robles e¢ al. (1989) on diel variation of intertidal foraging by Cancer productus L. in British Colum- bia, Canada, there exist only a few quantitative studies of temporal variations of such habits (Robles er a/., 1989). It has been known for many years that Cancer pagurus L. (the only commercial crab in Norway) makes diurnal vertical movements on rocky shores of the Norwegian Skagerrak coast during the summer and early autumn ( Nordgaard, 1912; Bjerkan, 1927; Dannevig and Gundersen, 1982). Ac- cording to Dannevig and Gundersen, many crabs move to shore level at night to forage, and angling for crabs with flash light and scoop net on summer nights has a long tradition, This kind of cyclical movement of C. pagurus has not been teported from other parts of the crab’s range, from the Mediterranean to northern Norway (Christiansen, 1969), nor tas aclose study of this activity been previously undertaken. Here we describe skin-diving surveys of cyclical movements of C. pagurus during the night, and throughout the year, on tocky shores on the Norwegian Skagerrak coast. Study Area and Results The study area was a small unsheltered rocky islet between Grimstad and Lillesand c.150m from the mainland (58°16'19"N, 8°32°33"E) The islet is c. 290 m in perimeter, and a maximum of 100 m across. The whole field area covered c. 3700 m’, bounded in depth by the upper limit of Laminaria digitata (Hudson) (3-5 m), and the water line. The common mussel, Mytilus edulis L., occupied a broad zone in the study area. The survey reported here was carried out between March and December 1980. Temperature, salinity, water level, height of waves, directions of current and wind, and light conditions were recorded during all surveys. The difference in tide at the study area is 17 cm. No crabs were seen on the first night-survey (30 March), nor were any individuals observed at night on the two next surveys (1 and 3 May). On 24 May, and until the last survey on 11 December, crabs were observed on all 30 nights of survey. Onall surveys, crabs were observed eating M. edulis, and random examinations showed that the crab stomachs usually were filled with fragments of the mussel, A maxi- mum of 237 crabs were counted during a survey on 22 June, In contrast only 1 crab was observed during the night survey on 7 August. This low number may be due to the moulting and mating processes which occur at this time of the year. 391 In late August surveys were carried out every fourth hour throughout 24 hours. Only 2-3 crabs were observed during day time, whereas the highest number, 91 crabs, was counted between two and three hours after sunset. Surveys were also carried out during the daytime on 9 different days, but only O to 4 crabs were observed on these surveys. Carapace width throughout the investigation period varied between 50-190 mm for females and 50-200 mm for males, with the highest number between 130-150. mm and 120-140 mm, respectively. Females were regarded as sexually mature at 130 mm, but females with eggs were never observed in the study area. According to the literature (Edwards, 1979; Dan- nevig and Gundersen, 1982) crabs with a carapace width of 115 mm should be about 5 years old, and older individuals may be up to 300 mm in carapace width. Tagging of crabs was done while swimming in the field area. Of 542 tagged crabs, 136 (25%) were recaptured from 1 to 7 times at the islet or within a 0.5 km radius, during the study period. In addition, 44 crabs (8.1%) were found be- tween 0.5 and 28 km from the islet. Two of these had earlier been recaptured at the islet. The last recapture of a long-dis- tance migrant crab was two years after tagging. The percent- age of recaptured individuals at the islet was highest for males, whereas a higher percentage of females was recap- tured more than 0.5 km from the islet. That females of C. pagurus make extensive migrations has previously been mentioned by several authors (Edwards, 1979), Literature Cited Bjerkan, P, 1927. Undersokelser over krabben (Cancer pagurus). Aarsberetning vedkommende Norges Fisker- ier for 1926: 141-162. Christiansen, M.E. 1969. ‘Crustacea Decapoda Brachyura. Marine invertebrates of Scandinavia 2’. (Universitets- forlaget: Oslo). 143p. Dannevig, G. and Gundersen, K.R. 1982. Taskekrabben. 230-234. In R. Frislid and A. Semb-Johansson (eds) “Norges dyr, Vol. 4: Virvellose dyr’. (J.W. Cappelens Forlag A/S: Oslo). Edwards, E. 1979, ‘The edible crab and its fishery in British waters’. (Fishing News Books Ltd: Farnham, Surrey, England), 142p. Nordgaard, 0. 1912. Faunistiske og biologiske iaktagelser ved den biologiske station i Bergen. Det Kongelige norske Videnskabers Selskabs Skrifter 1911 (6): 1-58. Robles, C., Sweetnam, D.A. and Dittman, D. 1989. Diel variation of intertidal foraging by Cancer productus L. in British Columbia. Journal of Natural History 23: 1041-1049, Kjell Karlsson and Marit E. Christiansen, Zoological Museum, University of Oslo, N-0562 Oslo 5, Norway. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum SPATIAL STRUCTURE IN A STONE CRAB POPULATION (BRACHYURA:XANTHIDAE) AND THE INTERPLAY WITH RESOURCE MOSAICS For large, motile, den-dwelling decapuds (e.g, clawed and spiny lobsters) habitat should be considered a mosaic of resource patches. Patchiness affects access lu resources which, in turn, affects mating patterns wilhin populations (Emlen and Oring, 1977), For some small brachyurans, patchiness of refuge or premium burrowing sites factors into male mating success (Christy, 1983; Diesel, 1986; Abele ef al., 1986), We asked if population structure of commercially important stone crabs would vary with refuge patchiness sufficiently to exclude alternative mating Strategies as de- fined by Christy (1987). Methods Refuge spatial patterns were manipulated as a splil-plot experimental design for a population of hybrid stone crabs (Menippe mercenaria x M. adina) in the northeastern Gulf of Mexico. Six interspersed treatment plots each contained 36 prefabricated Teel modules in either a widely spaced (60m), uniform pattern, a closely spaced (2m) uniform pal- tern, or an intermediate, mixed pattern, ic. G widely spaced clusters, each with 6 closely spaced modules. In September and October, 1987, 12 randomly selected modules were non-desiructively sampled on each plot. In late August and early October, 1987, one black of treatment plots was ¢xhau- slively bul non-destructively sampled (n = 36 modules/plot). That sume block was exhaustively sumpled monthly trom August 1988 through July 1989. Data foreach crab included specific den Jocation, tag identification, sex, carapace width, and phenotypic index according to Bert and Harrison (1988) Summary of Results Phenotypically, this hybrid population most closely re- sembled M, shercentaria, In 1987, widely spaced modules harboured more crabs than did closely spaced modules or those in an intermediate, mixed pallern, Widely spaced an mixed modules also tended to harbour larger males und females, although differences were not significant for every sampling period, Sex ratios did not differ among lreatments, yel widely spaced modyles harboured more mated pairs than expected from the distribution of males among plois Crabs left the study site during late summer und fal] 1988 as Octopus vulgaris invaded plots, Treatment elects re- emerged tollowing spring 1989 recolonisation by adult crabs. Crabs tagged in 1989 were not long-term den residents, bur resightings were preater than expected by chance on the wide plot. Females were tesighted more often than males. Only 5 of 100 tagged males were resighted, three resighted justonce, and two large males (122 mm and 10 mm CW) found repeatedly in different wide-plot modules with different females. Discussivn Differences in. crab abundance may be explained by difver- ential prey depletion on soft-boltom as a function of refuge spacing and distance from refuge (Lindberg ef a/,, in press, Frazer and Lindberg, unpubl.). Refuge value apparently MEMOIRS OF THE QUEENSLAND MUSEUM Changes with access to prey, and the resultant mosaic thon influences residency patierns by size and sex. Low site fidelity by males compared to females and mul- tiple male occupancy of modules (Wilber, 1989a; and herein) precludes 4 resoutce-centred male mating strategy. Pro- tracted mate guarding (Wilber, 1989b) also impugns an encounter-raic-competition male strategy. The greater per cupila mating success of males on wide plots, and resightings of few large males amidst numerous females is consistent with ether a female-centred, patrol-and-de fend stralegy ora search-and-defend strategy influenced by patterns of food and refuge. Acknowledgements This. work was funded by the Florida Sea Grant College Program, U.S. Department of Commerce, grants NAROAA- D-00038 and NAS6AA-D-SGO68. Literature Cited Abele. L.G., Campanella, P_J. and Salmon, M. 1986, Natural history and soctal organization of the semiterrestrial grapsid crab Pachygrapsus transversus (Gibbes), Jour- nal of Experimental Marine Bivlogy and Beolowy 104: 153-170. Bert. TM, and Harrison, R.G, 1988, Hybridization in West- ern Atlantic stone crabs (Genus Menippe): evolutionary history and ecological context influence species interac- tions. Evolution 42: 528-544, Christy, J,H, 1983, Female choice in the resource-defense mating system of (he sand fiddler crab, Vea pugilator. Behavioral Ecology and Sociobiology 12; 169-180, 1987. Competitive mating, mate choice and mating associa- tions of brachyuran crabs, Bulletin of Marine Science 44: 177-191. Diesel, R. 1986, Optimal mate searching strategy In the symbiotic spider crab /nachus phalangium (Decapoda), Ethology 72; 311-238. Emlen,S,T. and Oring, L,W, 1977. Ecology, sexual selection and the evolution of mating sysiems. Sejence 197; 215- 333, Lindberg, W.J., Prazer, T.K. und Stanton, G.R. In Press. Population effects ot refuge dispersion for adult stone crabs (Xanthidae, Mvnippe), Marine Eulogy Progress ‘Series. Wilber, D, H, 19899, Reproductive biology and distribution of stone crabs (Xanthidac, Menippe') in the hybrid zone on the northeastern Gulf of Mexico. Marine Ecalogy Progress Series 52; 235-244, 1989b. The influence of sexual selection and predation on the mating and postcopulatory guarding behavior of stone crabs (Xanthidac, Menippe), Behavioral Ecology and Sociobiology 24; 445-451. Wid. Lindberg and T.K. Frazer, Department of Fisheries and Aquaculture, University of Florida, Gainesville, Florida USA. G.R. Stanton, Florida Stee University Marine Lubaralery, Tallahassee, Florida USA, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 393 SPATIAL AND TEMPORAL DISPERSAL AND RECRUITMENT PATTERNS OF DECAPOD CRUSTACEA IN THE NORTHWESTERN ATLANTIC Larval dispersal and postlarval recruitment are Vital proc- esses affecting the maintenance of ecologically and economi- cally significant populations of decapod crustaceans. Vertical posilioning of larvae and postlaryae in the water column plays a major role in the particular strategies of tetention or expulsion with immigration that are employed. The present study was undertaken to investigate variations in vertical distribution of prejuvenile decupod crustaceans according to temporal (diel), spatial (estuarine, transitional, Oceanic), ontogenetic (larval siages, postlarvae) and various environmental factors (light, temperature, salinity, wind, tidal cycles). Furthermore, effects of vertical positioning on dispersal and recruitment were examined. Three stations were established for the present study; York River mouth (estuarine) (37°12'N, 76°16 W): Chesapeake Bay mouth (transitional) (36"S8'N, 76°07'W); Chesapeake Light Tower (offshore) (35°54°N, 75°43°W). Each station was occupied for a continuous 72 hour period in late summer aver six tidal cycles. Quantitative plankton samples were collected every three hours from the following depths: Neus- ton (0.1 m), Im, 3m, 6m, epibenthos (11=13 m). A total of 375 samples were obtained (125 from cach station), Non-par- ametric methods of statistical analysis. were used. except where normality was nol criticul. Collectively, 4] decapod species, 160 developmental stiyzes and an estimated 6,000,000 specimens were obtained. A large majority of the total careh (86%) came from the oflshore location, True crabs (Brachyura) accounted for 53% of the species, 50% of the stages and 92% af the specimens. Anois rans. thalassinideans and shtimps were also found. Cullinectes supidus (87% of the total), Uco spp. (39) and Priiaa clive toplerana (2%) were the most commonly collected species. OF the 160 developmental stages, 56 Were present in sufficient quantities for data analysis (Maris. 1986), Fifteen different distributional groups were farmed based oy siatis- lical comparisons of abundances wiih depth Results indicated that proximity to the estuary greatly affects vertical positioning. Overall day-night mean depths (m) for collective specimens were: estuarine, 5.96 4,24; Iransitional, 7.49-—3.19: offshore, 1.86-1.41. Light was prov posed as the major factor governing distribution, with (empera- ture, salinity and tidal cycles having no signitican effects, Six dispersul-recruitment palierns were established fur collected genera based on temporal and spatial distributions: totained estuarine (Neopanope, Palaemonetes, Panapeus), retained estuarine-transitional (Callianassa, Pinnixa, Pin- sotheres, Upogebia), retained transitional-n¢arshore (Eucer- amus, Hevapanopeus, Pagurus), retained offshore (Emerita, Lidinia, Ovalipes), expelled with estuarine spawning (L’ca) and expelled with transitional spawning (Callinectes). Vertical positioning greauly influences larval dispersal and posilarval recruitment of decapod crustaceans. Certain estuarine and transitional species accomplish retention by con- sistently maintaining a vertical location near the bottom, while some vertically migrate over short intermediate distances, pre- sumably to the depth of no net motion. Others maintain constant intermediate depths, while various species vertically migrate over long distances, Offshore, individuals are typically retained an the continental shell by maintaining shallow-intermediate depths. Larval abundance correlations with ebb Uides (promoting flushing) and flood tides (promoting retention) in small inlets have béen presented by Cronin and Forward (1982), Lambert and Epifanio (1982), and Brookins and Epifanio (1985). In the present study, the general lack of correlation between tidal influence and vertical distribution possibly indicates that different mechanisms are in effect in large systems as compared to small inlets. Even though tidal effects were found to be minimal, larvae likely utilise the net flow patierns of the bilayered systent for movement. Transport mechanisms Lypically consist of near bottom estuarine concentrations with upper layer affinities maintained offshore. Acknowledgements fam grateful for technical advice from John R. McCo- naugha, Anthony J. Provenzano, Ir,, David L. Feigenbaurn, und Michael H. Prager (Old Dominion University) and Charles FE. Epifanio (University of Delaware) The crew of the R/V Linwood Helton and numerous volunteers are givon much appreciation for field collecting. Literature Cited Brookins, K.G, and Epifanio, C.E. 1985, Abundance ot brachyuran larvae in asmall coustal inlet oversix con- secutive tidal cycles. Estuaries 8: 60-67. Cronin, T.W, and Forward, R.B. 1982, Tidslly timed be- havior: their effects on Jarval distributions in estuaries. 505-520. In V. Kennedy (ed.) "Estuarine comparisons’. (Academic Press: New York). Lamberl, R. and Epifanio, CE. 1982, A comparison of dispersal strategies in two genera of brachyuran crabs in a secondary estuary. Estuaries 5: 182-188. Manis, R.C_ 1986. ‘Patterns of diurnal vertical distribution and dijspersal-recruitment mechanisms of decapod crustacean larvae and postlarvae in the Chesapeake Buy, Virginia and adjacent offshore waters”, Ph.D. Disserta» tion, Old Dominion University, Norfolk, Virginia, 222p. (University Microfilms International Publication Nu. RO-1 7863) Robert C. Maris, Department of Biology, Mansfield University of Pennsylvania. Mansfield, PA 16933, OSA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum AGE STRUCTURE OF ANTARCTIC KRILL (EUPHAUSIA SUPERBA) POPULATIONS AS DETERMINED BY AGE-PIGMENT ANALYSIS AND BY SIZE-FREQLUENCY ANALYSIS Morphometric measurements and size frequency analysis have conventionally been used to assess the age structure of crustacean populations. Certain crustaceans have, however, not proven amenable to such analyses. For example, labora- tory studies have shown that the Antarctic krill Fuphausna superba can live for 7~8 years (Ikeda and Thomas. 1987), a life-span far in excess of that predicted from morphometric delerminations. Furthermore, this species may decrease [n size during periods of low food availability (Ikeda and Dixon, 1982) thus obscuring the relationship between measurements of body size and age. In tesponse lo these problems, an age-determination technique was developed for E. superba which was based on the measurement of levels of ape-piz- ments (FAPs) in the animals (Ettershank, 1983, 19844, b, 1985). Early work on FAPs held promise (Ettershank, 1983, 1984a, 1985) but subsequent studies demonstrated methodo- logical problems (Nicol, 1987), Studies examining FAPs in other organisms have yielded equivocal resulis (Hill and Radtke, 1988; Hirche and Anger, 1987) but the utility of this technique for aging populations of the species for which it was originally proposed — Euphausid superba — is yet to be proven. A population of juvenile &. superba was maintained wader constant laboratory conditions. A sample of the populmion was removed al the start of the experjment and the animals were frozen individually in liquid nitrogen. The surviving animals from the original populanon were frozen in liquid nilrogen one year later. The two sets of samples were uni- lysed for FAPs (Ettershank, 1984b) and the mean fluores- cence peak heights af the two groups were compared, The resulls of the fluorescence technique were compared with those of a more conventional weight-frequency analysis. The mean fluorescence (expressed as telative fluorescence or as weight specific relative fluorescence) of the year 2 TABLE 1. The mean values and predicted mean values for the weight specific telative fluorescence and the dry weight of the animals in each sample. ees fh; ee Se Fluorescence 133.286 213.873 Mean wt. specific | 10.625 (9.53) 21.10 (20.42) fluorescence Mean dry weight | 13.286(19.34) number of samples | 37 Comparison between mean weight specific Muores- cence in year | and year 2: t=-7.586, 58 df, p< 0.0001, Comparison between mean dry weight in year | and year 2:1 = 2.522, 58 df, p = 0,014, Values in brackets are predicted means from Mac- donald-Pitcher analyses of combined year 1 and year 2 dala sets. 9.926 (9.65) 23 MEMOIRS OF THE QUEENSLAND MUSEUM Sfoup Wassignificantly preater than that of the year 1 group. fo contrast, the mean weight of the individuals in the popu- lation decreased significantly over the course of the year (Table 1), The weight and relative fluorescence dala were pooled, simulating the normal field situation af 4 series ot frequency data from which peaks must be discerned, In this instance the number of year classes and the mean peak heights were known 50 the resul!s from the frequency anu- lyses could be compared to the expected (real) case. An analysis of the weight specific relative fluorescence dala by the Macdonald-Pitcher method yielded a best til for two modal peaks, the means of which were nol significantly different to the knawn means for the two year classes. The weightefrequency analysis also yielded a best fil for two peaks bul in this case the correspondence between the means of the predicted and known weight graups was nat so precise oF accurate. These results show that under laboratory conditions it is possible to separate year groups of £. superba by FAP quanti- fication and that the secumulation rate over a period of one year 15 Brear enough that the vear groups can be discriminated even when the data are pooled, We have alsn shown thal FAPs can be used to demonstrate vear group separation and predict which group {s older when size-frequency analysis gives the wrong answer, Literature Cited Ettershank. G. 1983, Age structure and cyclical annual size Change in the Antarctic krill, Euphausia superba Dana. Polar Biology 2(3): 189-193. 19844, A new approach to the assessment of longevity in the Antarctic krill Euphausia superba. Journal of Crustacean Biology 4: (Special Issue |) 295-305. 1984, Biomass Handbook 2, 1-14, 1985, Population age structure in males and juveniles of the Antarctic krill Euphausia superba Dana. Polar Biology 4(4): 199-201, Hill, K.T. and Radike, R.L. 1988. Gerontological studies of the Damsellish Dascyllus afbisella, Bulletin of Marine Science 42(3); 424-434. Hirche, HJ. and Anger, K. 1987, The accumulation of age pigments during larval development of the spider crab, Hyas arancus (Decapoda,Majidae). Comparative Blochemistry and Physiology 88B(3); 777-782, Skeda, T. and Dixon, P. 1982. Body shrinkage as a possible ovet-winteting mechanism of the Antarctic krill, Euphasia superba Dana. Journal of Experimental Marine Biology and Ecology 62(2): 143-151. Tkeda, T, and Thomas, P.G, 1987. Longevity of the Antarctic krill (Euphausia superba Dana) based on a |aboratory experiment. Praceedings of the National Institute of Polar Research Symposium on Polar Biology t; 56~62. Nicol, S, 1987. Some limitations on the use of the lipofuscin ageing lechnique. Marine Biolagy 93(4): 609-614. Stephen Nical, Martin Stolp and Graham W. Hosie, Antarctic Division, Channel Highway, Kingston, Tasmania 7050, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM 39 ESTIMATION OF GROWTH PARAMETERS OF THE VELVET SWIMMING CRAB (LIOGCARCINUS PUBER) (BRACHYURA: PORTUNIDAE) AT PLYMOUTH. S.W. ENGLAND. Liocarcinus puber (L.) (formerly Macropipus puber) is a focally abundant portunid crab cm rocky coasts of Western Europe. Recent overfishing in Spain and continued demand has allowed an export fishery to develop trom the UK being centered in N.W, Scotland. Anecdotal information suggests that there may be significant variations in the grawth format between Spain and N.W. Scotland, however management patameters for the UK fishery have been based largely on data from Spain. Approximately 4,000 specimens were sampled by hand from the intertidal, and via SCUBA, nearshore sub-littoral areas, trom November 1985 to December 1987, Size frequency analysis from monthly samples readily described the growth of juveniles, attaining a mean mode! size of 40-415 mm Carapace Width atan age of 1 y. Sexual malurity occurs atc ly (=46,5, = 40.6 estimated from allometric growth of chela and abdomen) (Norman, 1989), Adult modes shawed no cleat definition into year classes. Examination of moult stages of adults from monthly samples showed a marked peak in early post-moult crabs (soft and paper-shell stages) in June/July for males and in August for females and a smaller peak in autumn. Laboratory fearing under simulated natural conditions, showed similar moult periodicity, with large adults { >60 mm, >50) mm CW) moulting annually, males in June and females in July/August, whilst smaller adults moulted al corresponding times 10 100 | -1) 80 x 4) E 60 = 4 3 Fy ® 40 E Ms tT © 20 1 2 3 4 Age (Years) FIG. i. Von Bortalanffy growth curves for female Liocarcinus puber from 1) Spain (Gonzalez Gurriaran, 1985) and 2), 3) and 4) this siudy, ELEFAN, probability paper technique and laboratory rearing respectively. Arrows demark size at 1 year ald. nw larger adults and again between September and December. Male growth curve showed close agreement with other methods, whilst females showed reduced growth from >55 mm CW (Fig. 1); this probably being due to increased reproductive effort, ELEFAN (Pauly, 1987), a programme which fils a con+ tinuous growth curve to monthly size frequency data via a leas! Squares Optimisation process Showed clear oplimisa- uon of parameters, but low agreement between actual and eslimated parameters due to the discontinuous nature of crustacean growth as well as the natutal variation within the sample. The probability paper technique (Cassie, 1954) due to the difficulty in distinguishing moult classes from year classes and requirement of subjective assessment, was felt to be Jess robust than other methods. Estimates for the growth constant (K) between the three methods ranged from, for male 0.28 to 0.34, and female 0.35 to 0.45, and for the asymptotic length (Lx), for male 107 to 114, and female 91 Io 98. Size frequently analysis from Spain (Gonzalez Gurri- atdn, 1985) gave higher estimates of K ( 0.65, 0.67), but comparative Lx ( = 109, = 96). In both studies age of sexual malurily is approx. ] year, but al correspondingly different sizes (Fig. 1). The validity of this difference in sive of sexual maturity is further endorsed by measure- ments from allometeic growth, the size of smallest oviger- ous female and size al which 50% of sample have mature ovaries, for each, estimates from Spain are consistently larger. by approx, 10) mm, than for Plymouth (Gonzalez Gurriaran, 1985; Norman, 1959). Acknowledgements The authors gracefully acknowledge Polytechnic South West for the award of Research Assistantship. Literature Cited Cassie, R.M. 1954. Some uses of probability: paper in the analysis of size frequency distributions. Australian Jour- nal of Marine and Freshwater Research 5: 513-522. Gonzalez Guriaran, E. 1985, Crecimento de la nécora Mac- ropipus puber (L.) (Decapoda, Brachyura) en la Ria de Arosa (Galicia, N.W. Espamia), y primeros datos sobre la dindmica de la pobalacion. Boletin del Instituto Espanol Oceanogratia 2(1): 33-S1- Norman, C.P. 1989. “Ecology of the velvet swimming crab Liocarcinus puber (1..) (Brachyura; Portunidae)’. PhD, Thesis. Polytéchnic South West, United Kingdom. 247p. Pauly, D. 1987. A review of the ELEFAN system for the analysis of length-frequency methods of study of the growth, mortality and recruitment in fish and aquatic invertebrates. 7-34, In D. Pauly and G-R. Morgan (eds) “Length-based methods in fisheries research’. ICLARM Conference Proceedings 13. C.P. Norman, Department of Aquatic Biosciences, Tokyo University of Fisheries, 4-5-7, Konan, Minato-ku, Takyo 108, Japan, M.B. Jones, Department of Biological Sciences, Polytechnic South West, Drake Circus, Plymouth, Devon, England PL4 &AA, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 396 SPAWNING BEHAVIOUR OF SERGIA LUCENS (HANSEN) (DECAPODA: SERGESTIDAE) The ‘Sakura-ebi’ Sergia lucens (Hansen) has provided the base of an historic fishery in Suruga Bay, on the south coast of Honshu, since 1894. Today, the annual catch totals 2500 to 3000 metric tons, more than US$20 million in landed value. Research on the shrimp is well advanced (Omori. 1969; Omori et al., 1973). Sergia lucens completes its life cycle in Suruga Bay. Spawning occurs al J year of age, from June to the middle of November. One female produces about 2000 eggs. The eggs are primarily spawned near the mouth of the riversal the head part and the western part of the bay. The eggs are planktonic. and are distributed mostly at depths ranging from 20-50 m, where the temperature is higher than 18°C, which js the lower limit of the optimal iemperature range (18°—25°C) for spawn- ing and larval development (Omori, 1971; Omori and Jo. 1989), Eggs hatch into nauplii afler 24~36 hrs under normal environmental temperature conditions. The larvae attain a length of 20-25 mm and recruit ta the fishery at 3-4 months old. The fishery is based on a species with a lifespan of only 1,5 years, and the tecruitment is instrumental in determining year-class strength. Tn 1985 and 1986, frequent sampling of the 0-50 m water column by vertical tow net was conducted al 2 stanons at the head of the bay torJuly, August and Seplember. In addilion, samples were obtained once a month from Juné to October at 8 stations in the entire bay. The abundance and distribution of eggs and larvae were analysed in relation to possible causes of the temporal and spatial yariations, Daily fluctuation in egg abundance was considerable. The coefficient of variation in July varied from 81—269°% (Bishop etal., 1989), In 1985 spawning occurred from the beginning of July, whereas in 1986 it occurred after the middle of July. In August when the seasonal thermocline js particularly marked and the optimum temperature zone narrow, spawning, was reduced, The possibility of a second peak of spawning was sug- gested in September 1985. In 1986 spawning activity did nat recover al the head of the bay, as the principal spawning area seemed to have shifted from the head to the western part. Under favourable conditions, 5, lucens may produce two broods in one season with a considerable interval between. Many external and internal factors may be involved in the spawning activity of §, /ucens. Among (hem, temperature MEMOIRS OF THE QUEENSLAND MUSEUM seems to be the most important. The start of heavy spawning is roughly associated with the warming of the surface water {o 24°C and vertical oscillation of the 18°C-isotherm depth. The temperature around 40 m rapidly increases to 18°C, 3-7 days before the spawning peaks. Temperature at 20-50 m depth affects the abundance and growth of the larvae, whereas food is abundant and would not have great a effect. Correlations between spawning and Junar period were not significant. In general, the potential size of stock for the following year is largely affected by the production and survival of eggs and larvae during the early spawning season. There is a positive rélation (r<0.01) between year-class strength and yearly average width of the optimum tempera- ture Zone from June through to August al the head of the bay (Nakamura, 1982), Literature Cited Bishop. G.H., Omori, M., and Muranaka, F, 1989. Temporal and spatial variations in the spawning activity of the micronektonic shrimp, Sergia fucens (Hansen) in Suruga Bay, Japan. Journal of the Oceanographic Society of Japan 45: 243-250. Nakamura, V, 1982. Oceanographic feature of Suruga Bay from view point.of fisheries oceanography. Bulletin of the Shizuoka Prefectural Fisheries Experiment Sta- tion(Spec. No.) 17: 1-153. [In Japanese). Omori, M, 1969, The biology of a sergeslid shrimp Sergesles lucens Hansen, Bulletin of the Ocean Research Institute, University of Tokyo 4: 1-83. 1971. Preliminary rearing experiments on the laryae of Sergestes lucens (Penaeidea, Nalantia, Decapoda), Marine Biology 9: 228-234. Omori, M., and Jo, 5.-f. 1989. Plankton sampling system wilh a new submersible voriex pump and its use to estimate small-scale vertical distribution of eggs and larvae of Sergia lucens. Bulletin of Plankton Society Japan 36: 19-26, Omori, M., Konagaya, T., and Noya, K. 1973. History and present status of the fishery of Sergestes lucens (Penaeldea, Decapoda, Crustacea) in Suruga Bay, Japan. Journal du Conseil, Permanent Intemational pour’ Ex- ploration de la Mer 35; 61-77. M, Omori, Tokyo University of Fisheries, Tokyo, Japan, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM CATASTROPHIC MORTALITY BREEDING TROPICAL ROCK LOBSTERS In Augusi-September cach year many 3—4 year old Sub- adul Ponulirus ornatus emigrate from Torres Strait. notth- eastern Australia, into the Gull of Papua; some migrate as far as Yule Island al the eastern side of the guilt, appearing in breeding condition on shallow coastal teefs by mid- January (Moore and MacFarlane, 1984: MacFarlane and Moore, 1986; Bell ef a/,, 1987), There is a seasonal artisinal fishery for these breeding lobsters, but it lasts only a few months. The breeding lobsters are in poor condition anu IL has been hypothesised that they inVest so much energy in the migration and in reproduction that death is inevitable (Trendail and Prescott, 1989). However, the population could also decline as a result of fishing pressure or emigra- tion from the fishing grounds. These alternative explana- lions of the annual decline of the breeding population were investigated in carly 1989. OF Methods In order to distinguish between the three hypotteses was necessary to estimate natural and fishing mortality, and immigration and emigration rales. A variety of methods were used to estimate these parameters; (a) tangle nels were deployed in deep water adjacent to the coastal reels to reveal the extent of mavements on and off the reets, (b) the caich and effort of the fishery were analysed to indicate trends in abundance, (c) lobsters were tagged and their recapture rite was monitored lo provide an estimate of populalion size und Joss rates, and (d) the water content of samples of digestive gland was measured to show trends in physiological condi- ton. Results and Discussion The Yule Island fishery followed a typical pattern over the period January—March 1989, with two major peaks in evtch following monsoonal storms before warning through March. The sex ratio of the first peak was close to unity whereas prior to this the calch consisted mostly of males and the second peak comprised almost entirely females. The tangle nets caught lobsters in two pulses in synchrony with the January and February full moons. However, these pulses were considered not to indicate emigration because (i) catch rates from the reef top peaked immediately afler- wards, (ii) Several animals lagged from the nets were caueht later by the fishery. and (tii) through March, when the caich of the fishery declined rapidly, n0 associated movement of lobsters off the coastal reefs was revealed by the nets. Instead, the pulses were interpreted as lunar hatching excur- sions as they comprised almost entirely females with cvi- dence of recently hatched broods. Analysis both of the tagging and catch data indicated extraordinarily high total loss rates (Z = 10-12) campared with lobsters in Torres Strait (Z< 1); indeed. of the 2U.UHU— 30,000 Jabsters estimated ta be presen at the beginning of the study more than 95% disappeared during the Inllowing few months. The tag return rate was high indicating that 397 fishing pressure was responsible for much of the decline (F = 3-4), but \henatural mortality rate over (he period was even higher (M = 7-8) possibly as a result of the stress of migration and breeding. This interpretation is supported by trends in the water content of the digestive gland, The water content (60% in healthy lobsters) increased steadily to 80% by early March after which it declined slightly; this apparent recovery may have resulted from animals with the highest water content dying ala faster rate. The degree of deterioration was greater in females and lhe recovery was more marked im the very few males remaining in the fishery al this time, Prior to (his physiological recovery, recently moulted lobsters were very rare. However, in the final weeks of the fishery nearly all males caught had moulted recently and their mortality rate had reduced to an unmeasurable level. In cantrast, maulting Was not observed in females and their mortality rate re- mained very high throughout the study, TLis clear thal lobsters breeding on coastal reefs near Yule Island do not survive to breed again in subsequent years. This raises the question of the generality of this phenome- fon among other breeding populations at P. ornatas that have been discovered recently in deep water adjacent to jhe far northern Great Barrier Reef of Australia. Acknowledgements We wish to thank she fishermen of Yule Island and staff of Yule Lobster Enterprises for their co-operation, and the crew of the FRY Kulasi, Por Moresby, for their assistance and support jn the field. This research was funded by the Common wealth Department of Industries and Energy, and the PNG Department of Fishenes and Marine Resources_ Literature Cited Bell, R.S,. Channells, P.W.. MacFarlane, J,W.. Moore, R. and Phillips, BF. 1987, Movements and breeding of the omate rock labster. Panulirus ornates, in Torres Strait and jhe northeast coast of Queensland. Australian Jour- nal of Marine and Freshwater Research 38; 197-210. MacFarlane, LW. and Moore, R. 1986. Reproduction of the omate rock lobster, Panvliruy ornatus (Fabricius), in Papua New Guinea. Australian Journal of Marine and Freshwiler Research 37: 55-65, Moore, R. and MacFarlane, JW. 1984 Migration of the orale tock lobster, Panwliras ornarus (Fabricius), in Papua New Guinea. Australian Journal of Marine and Freshwater Research 35: 197-212, Trendail, J.T. and Prescott. J.H. 1989, Severe physiological stress associated with the annual breeding emigration of Panulirns ornatus in the Torres Strait, Marine Ecology Progress Series 58: 29-39. C.R. Pitcher, D.M. Dennis, T.D. Skewes, CSIRO Marine Laboratories, P.O. Box 120, Cleveland, Queensland 4163, Australia, JH. Prescou, Department of Fisheries and Marine Resources, Konedobu, Port Moresby, PNG, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 398 REPLENISHMENT OF CRUSTACEAN ASSOCIATES OF CORAL ISOLATES IN THE CENTRAL REGION OF THE GREAT BARRIER REEF Mast coral reef habilats support a rich fauna of crustacesn associates (Bruce, 1976), These associations range from the use of corals as one of a range of habitats (Coles, 1980) through to obligate species feeding on coral mucus (Knud- sen, 1967). Although previous ecological studies have re- vealed local and regional variations in species composition and abundance of coral dwelling crustaceans (Abele. 1976) there have been few aliempts to quantify distributions, abun- dances and species replenishment systematically atany scale. The present study was a four year survey of the crustacean fauna associated with live and dead Pocillopora verrucosa. The crustaceans were sampled systematically (rom isolated corals placed al coral reel’s located on a transect spanning the width of the continental shelf in the central region of the Great Barrier Reef. The location of the reels and thesampling methods used are described in detail in Preston and Doherty (1990). The results of this study demonstrated pronounced cross- shelf patterns in the species composition and abundance of crustaceans that colonised cleared corals. These patterns persisted (hroughout the four year study. Among the microcrustaceans copepods were the dominant taxa found on live and dead corals in the mid-shelf and outer shelf reefs. Tanaids and cumaceans were more dominant on the inner shelf reef particularly on back reef sites. The toral abundance of microctustaceans was significantly greater on the mid-shelf than on the inner or outer shelf. Live and dead corals from the mid-shelf reefs yielded significantly greater numbers of agile shrimps than those located al the inneror outer shelf reets. On all reefs the shrimp fauna on live corals was dominated by a single species; Pertclimenes amymone. However, monthly comparisons of community structure and faunal similarity revealed regional variation in spécies replenishment following disturbance of live corals. By contrast, the agile shrimp associates of dead corals showed a more even distribution of individuals among species and a more regular pattern of regional species re- plenishment, Destructive sampling at the end of the survey revealed that live corals on all reefs supported a common group of seden- tary macrofaunal associales. However, there were signifi- cantly fewer of these associates on the inner shelf reef. On dead corals there were similar numbers of sedentary macro- faunal associates at all locations bul pronounced cross-shelf patterns in species composition. MEMOIRS OF THE QUEENSLAND MUSEUM The results of this study suggest that the amount of space available is not necessarily a limiting resource for crustaceans that have formed an association with living corals. Nor is it the case for free-living species that inhabit dead corals. Consistently lower yields of agile shrimps and microcrustaceans from standard sized units of live and dead corals at the inner and outer shel reefs compared with the mid-shell reefs indicate that the former sustain relatively depatiperatée populations of these crustacean associates. Rela- tively low rates of replenishment by recruitment or migration apparently maintain this cross-shelf pattern, Regional variation in replenishment of live corals by ob+ ligate species probably reflects the regional population den- sily of the host corals. In order to establish if a similar link exists between the distribution and abundance of free-living Species and concurrent patterns of particular habitats we need to know more abou! the connection between these species and their habitars. Acknowledgements This study was funded by an Australian Marine Science and Technologies grant. J am grateful to P.J, Doherty for initiating this study and for providing the samples, I thank the captain and crew of the ‘MV Harry Messel’ and the many volunteer divers that assisted in the field work. A.J, Bruce and P, Davie provided valuable assistance in taxonomy, Literature cited Abele, L.G. 1976, Comparative species richness in fluctuat- ing, and constant environments: Coral-associated de- capod crustaceans, Science 192; 461-463. Bruce, A.J. 1972. Shrimps and prawns of coral reefs, with special reference to commencalism. 37-94, In A.O, Jones and R, Endean (eds) ‘ Biology and geology of coral reefs’, Vol. TIT, Biology, 2. (Academic Press: New York). Coles, $.L. 1980. Species diversity of decapods. associated with living and dead coral Pocillapora meandrina. Marine Ecology Progress Series 2281-291, Knudsen, J.W. 1976. Trapezia and Tetralia (Decapoda, Brachyura, Xanthidae) as obligate ectoparisites of pocil- loporid and acroparid corals, Pacific Science 21: 51-57. Preston, N.P_and Doherty, PJ. 1990, Cross-shelf pattems in the community structure of coral dwelling Crustacea in the central region of the Great Barrier Reef. 1: Agile shrimps. Marine Ecology Progress Series 66: 47-61. N,P, Preston, CSIRO Marine Laboratories, Cleveland, Queensland 4163, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM REPRODUCTIVE BEHAVIOUR OF CARDISOMA CARNIFEX (HERBST, 1794) (BRACHYURA; GECARCINIDAE) AT LIZARD ISLAND, GREAT BARRIER REEF The land crab. Cardisama carnifex, was first Tound at Lizard Island by Peter Davie of the Queensland Museum in June 1987, The closest previous record was Murray Island in the Torres Strait (Turkay, 1974). The populations studied were located in Watson's Bay and Mermaid Cove on Lizard Island (14°40'S, 145°27°B). The Watson's Bay study site included two afcas of approximately 400 sq m with over 300 obviously active burrows, The Mermaid Cove sile is smaller comprising 300 sg m and 200 burrows, The burrows were located on the edge of the man- proves. near the high-water mark ina community of grasses dominated by the sallwater couch, Sporobolus virginicus. Reproductive behaviour and periodicity were studied be- «ween October 1987 and June 1990, The female crabs spawned by migrating from their burrows to the ocean. In Watson's Bay they migrated from their burrows on the landward edge of the mangroves, over a 5m high spinifex covered sand dune to the ocean or followed Ferrier’s Creek to its mouth. The crabs entered the sea and swam a maximum of 15m trom shore to depths of 0.1—3m, Hatching was induced when the ege laden abdomen was submerged and the temale flicked her abdomen. The egg cases immediately ruptured und the zoea swam free. Each 300-400y crab teleased between 350,000 and 450,000 eggs. Egg mass was related to body weight. Evidence from captures of berried females, tracks on the beach at Watson's Bay and Mermaid Cove, and observations of spawning, indicated that spawning was highly seasonal and tied to lunar phase on Lizard Island. In October 1988 tracks from 10.crabs were observed on the beach al Watson's Bay indicating that in at leas) some years spawning may begin as early as October (the austral spring). No berried females or tracks were observed in November in any of the sludy years. Spawning migrations occurred primarily three nights before full and new moons in December 1989 and January 1990, Spawning migrations were observed on 11-13 December 1989 (approximately 30 crabs per night at Mer- maid Cove; 20 crabs per night at Watson's Bay) and $-10 January 1990 (approximately 20 crabs at Mermaid Cove; 30 crabs at Watson's Bay). both periods occurred during the see days prior lo full moon, No migrating males were observed, Also tracks from 60-70 spawning crabs were observed on 12 December 1989 in Watson's Bay and ftom 25-30 crabs al Mermyid Beach, Tracks from approximately 50 crabs were observed on the strand line.on the new moon on 29 January 1989, There was no evidence of spawning in February 1991), An ovigerous female was captured by the burrows on December 1989, The undifferentiated yolky eggs developed into zoea and hatched in 13 days, The timing of zuen release coincided with the December spawning migration. Vision plays an important cole in the migration, Crabs that had just released eggs were captured, Some crabs eyes were 39Y covered blocking vision; the eyes of others were left unob- structed, When released the visually impaired crabs were disorientated. Non visually impaired crabs would immedi- alcly move up the beach and seek cover. Migrating crabs would stop if a lightor large shadowy object was near them. A sample of the migrating crabs were caught and tagged by etching the carapace with a hacksaw. Alihough Cardi- soma puanhund is known to spawn several times.in a season (Lutz and Austin, 1983), none of the tagged spawning fernales were recuptured during subsequent spawning migra- lions. During the 2.3/4 year study a total of nine copulations were observed — six between October to January and two during the last week of May. Three female crabs collected in late May/early June were dissected. Two of these were post copulatory, In all three, the brown ovaries were undeveloped and weighed 0.7, 0.9 and i.4g. The period between copulation and spawning in Scyla serrala can extend up to 7 months under unfavourable con. ditions of temperature und nutrilion (DuPlessis, unpubl, it Heasman et al., 1985), tris possible that copulation in Car disoma carnifex occurs 1—S months prior to spawning, No precopulatory observations were made. Copulation occurred intermoult near burrows af temales, Copulailon occurred wilh crabs ventrally juxtaposed by the entrance Lo the female’s burrow There was litte movion, The female was not constrained by the male nor were there other males in the vicinily, Copulation terminated within 1-10 minutes after being spotted, The female quickly entered a burrow while the male slowly moved away, Literature Cited Heasman, M.P., Fielder, D.R. and Shepherd, R.K. 1985_ Mating and spawning in the muderab Seylla serrata (Forskal) (Decapoda: Pottunidae), in Moreton Bay, Queensland, Australian Journal of Marine and Fresh. water Research 36(6): 773-783. Kannupandi,'l., Khan, S.A., Thomas, M., Sundaramoorthy, S, and Natarajan, R. 19M(). Larvae of the land eren ‘Cardisoma carnifex (Herbst) (Brachyura: Gecarcinidae) teared in the laboralory. Indian Journal of Marine Science ¥, 271-277. Lutz, P.Land Austin, CB. 1983. Land crabs: a new resource potential. Proceedings of the Annual Gulf and Carribean Fisheries Institute 35: 6-16, Tirkay, M. 1974, Die Gecarcinidae Asiens und Ozeaniens (Crustacea; Decapoda), Seckenbergiana Biologica 55(a6), 223-259, Nu Galan, BL. Kojis, Lizard Island Research Stanton P.M.B. 37, Cairns, Queensland 4871, Australia, K, Diele, Jttiin-Maexmilians Universitdl, Wurzburg, Gerrnerry. U, Meischaer, Kiel University, Kiel, Germany, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 40p FOOD AND DILKNAL BEHAVIOUR OF DEEPWATER PRAWNS Penaeldean and caridean prawns provide most of the emustacedn catch ino demersal trawl fishery for prawns and scampi on (he North West Slope of Australia. The main penaeidean prawns are Arvishaeamarphy foliacea, Arixteus Wrilis, Hullporaides sibogae and Plesiapenaeus edwardsi- wnus, and |he main curidean prawns are Aeferoearpus si- hagae and Hy weodmasoni. Calch rates of all six prowe species are greater during the day than al night. Foregut contents in trawl-caught prawns were analysed, and broad ielary groups used to Indicate the habitats in which the prawns were feeding. Prey groups Considered 10 indicule midwater feeding included siphonoplinres, chactog- naths, heleropods and pteropads: prey groups indical ing ben- ihic feeding ineludecl sponges, polychaetes, bivalves and echinoderms. In all prawn species, (he majorily of the foregut contents consisted pf decapod crustaceans ynd fish, most of which was unidentifiable or was not classifidble as neces- sarily having a miclwarer ar demersal origin. Significant quamites of foramniterons and squid were also ingested MEMOIRS OF THE QUEENSLAND MUSEUM Aristeus virilis, Haliporaides sibagae and Plestenenacus edwardstanus, Which ate mainly benthic or demersal anl- mats, had mean catch rates between 1.4 and 2,0 limes greater during, the day than at night. Aristeeomerpha Joliacea and Metwroacarpus sibagae, which ate both midwater and demer- sal animals, and Heterecarpus woodmaseni, which ale mainly micdwater animals, had mean catch rates between 2.6 and 163 times higher during the day than al night, Decreased catch races of these species probably reflect nocturnal migra- iron inte midwater, Catch rates of A, foliacea peaked wround mid-day, suggesting thata substantial proportion of Lhe popu- lation may still be in midwater during daylight hours, Catch rates of Hererocurpus sthogae and A. weedmaseni varied lie during daylight hours but changed rapidly around dawn and dusk, suggesting shar their diummal! behaviour is strongly dependent on ambien) light tevets. Studies on midwater populaiians are proposed to determine ihe importance of midwater feeding in the djumally migratory prawn species. S.F. Rainer, CSIRO Murine Labormories, P.O Box 20, North Beach, Western Australia 6020, Aaxtralia- MICROPROCESSORS AND FIELD INSTRUMENTATION FOR CRUSTACEAN BIOLOGY Micropower microprocessors are making possible the galhering of data, and its transmission, from siluatians where direct Observation is either Impossible or would influence the phenomena under study. This paper proposes two examples of field instrumentation, desigaed around microprocessors, which will address otherwise refractory questions in two areas of crustacean biology: larval transport/recruiiment, and behavioural-physiological ecology, The highest mortality in life cycles of marine Crustacea occurs during planktonic larval stage, yel litle is understood about the phenomena that control mortality, transport. dis- persion, and especially eventual recruitment. Experimental testing of hypotheses is made difficult by the minute size of the dispersing larval slages, Sampling of cither the larvae themselves, or of the current regimes they would encounter as they migrate vertically, ul the relevant spatial scale, is prohibitive. The Lagrangian approach requires intensive sampling trom many vessels, with subsequent sorling of high numbers of plankton samples, the Eulerian approach demands unreasonable numbers of current meters. To experimentally test theories of larval transport and recruitment, we ure developing 4 microprocessor-coutrolled Lagrangian drifter that behaves like a larva but can be tracked remotcly, A buoyancy adjustar under microprocessor contral will allow the device lo mimic larval behaviour, relevant to the species under study, in response to lime, depth and other environmental cues, e.g. temperature, light, salinity, Initially these buoys will be programmed to mimic larvac of Rhdhro- panopeus harrisil and Callinectes sapidus, based on be- lraviours observed in laboratory and field, and used to examine how those behaviours contribute to retention in estuaries (FR, Ageristi) or export to Continental shelf waters with subsequent re-invasion of estuaries (C, sapidus), A similar approach is applicable to replenishment af benthic Taunas on tsolated Istands. The devices could also be pro- grammed with hypothetical behaviours to examine the can- sequences of such behaviours for (ransport in Virious Hajural nyvdropraphic regimes. Another difficult area for study is the physivlogical and behavioural ecolugy of species inhabiiing estuaries, Direct observation by divers is difficult and often impossible be- cause the subjects are highly mobile, and tive under very turbid conditions. Laboratory observations cannot be relied upon tv provide relevant behavioral data, particularly for species that range over spatial scales orders of magnitude larger than the laboratory can accommodate. To relay complex behavioural data (rom unrestrained an- imals in natural environments, we have designed microproces- syr-based multichannel Ultrasonic blotelemetry transmitters. The devices monitor up to eight different phenomena (¢.g.. musele potentials, limb positions), At any change of input stale, he microprocessor awakens and transmits the current State of its inputs, thus marking the beginning and end of an oventalany input. The information is encoded either as pulse width, or as a frequency-shifl-keyed (FSK) serial data word, All ultrasonic frequencies are synthesised by the micro- processor, which alsw drives the piczoclectric transducer directly. Power consumption is held to levels supportable with Small bulléries by operating the microprocessor with low duty eyeles, putting it into ‘sleep’ (power down) mode when idle. The initial application of these transmitters will be to explore predator-prey and predator-predalor interac- tions among C, sepidus and prey patches of small clams in Chesapeake Bay. Acknowledgements This research is being supported by grants OCE 8900060 and OCE 9002168 from (he U.S. National Science Founda- tion. TG. Waleatt and DL. Woleun, Marine, Earth und Atmospheric Sciences, Nort: Caroline State University, Ralvigh, NC 27695, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM SIZE AND ASSORTATIVE MATING IN THE SHORE CRAB, CARCINUS MAENAS Mating in the common shore crab, Carcintus maenas, can only occur when the female has recently moulted, Males find females about to moult by free search, and guard them until they moult. When mating occurs, they will subsequently guard the female until her new carapace hardens. Males will compete aggressively aver receptive females, and itis pener- ally assurned that the larger, stronger males will be able to mate with the largest, and presumably, most fecund females. This would be expected to result in 3 homogamous mating pattern, which we, and others have observed in this species. This type of mating pattern is also seen in other brachyuran species. The behavioural hypothesis for homogamy rests on a number of assumptions; thal a large male will win a fight against a smaller male; that the males are capable of recog- nizing the relative size of a female, and that there are no other factors affecting a females desirability, e.g imminence of moult, and hence reduced guarding time: We tested each of these assumptions in the laboratory using artificial conflicts between chosen individuals. taken from mating pairs on the shore. Firstly, the largest male does not always win in a two male conflict. Out of 85 conflicts between two males over a single female, the smaller male won 36% of the time. Successful smaller males ranged from 2mm to 12mm smaller than their opponent. Similar results were found for groups of males with @ restricted number of females (smaller crabs were successful 38% of the time). Ina second set of experiments, one male crab was offered a choice of two females, one large (S0-S8mm carapace width), the other small (383mm). In 57 trials the malic chose the smaller female 49% of the time, Similar results were found for groups of males offered an excess of large and small females with 48% of the males mating with the smaller females. We found that the males did not appear to choose a female according to the imminence of her moult. Field collections showed that there was a slighi tendency for large males to be found paired with females further from their moult than small males. In the laboratory single males offered a choice be- tween two Females chose the female furthest from her moult approximately 50% of the lime. it would appear that large male Carcinus are incapable of discérning a relatively large female or one closer to her 401 moult, and may not win a fight to mate with her even if he did. A second possible explanation for the observed homa- gamy in the field is mechanical constraints. We collected over 500 mating pairs of crabs and in nu case was the female larger than the male, and usually al least 6mm smaller. During pre-copulatory guarding, the male carries the female under him. ft may be difficult or impossible for him to mave with a female which is larger than himself. After she has moulled and grown this problem will be exacerbated, which may explain why males lend to pair with females at least 6mm smaller. A second possible factor is thal very large males (carapace width > 70mm) rarely mate with females more than 35mm smaller than themselves. This may be due to difficulty in cither carrying, or in actually copUlating. We have developed a camputer model using the popula- tion results found on the shore. in which each male is paired atrandom with any female within the bounds described. No pairing if ihe female is within 6mm carapace width of the male of if she 1s mote than 35mm smaller than him. The resulting, simulated, population of mating pairs also showsa distinc! positive relationship between male and female size. which is very similar to the field population. Irseems likely, therefore, that homogamy, in this species, is a result of mainly mechanical constraints, and not conflict between males over (he ‘best’ females. This interpretion is supported by the field study. Over 50% of the mating females had moulted within two tidal cycles of capture, which may Suggest that if the males were capable of exercising choice they would haye very little time in which to do so. Further- more, in this location there are less females than males, and only a fraction of those will be moulting, and hence available lo male, al any one lime, Provided Uhal the available females ate sufficiently rare, im both lime and space, it would seem likely that the best strategy for an individual male, having found or won a receptive female, would he to remain with her and (o mate with her, There is clearly a trade-off between the increased reproductive success of mating with an opl- mally large female and the amount of time spent finding her, It would seem likely thal male Carcinus would only adopt a stralegy of picking and choosing females, if they were suffi- cienlly common (0 justify this, D.G, Reid, P. Abello and E. Naylor, School of Qcean Sciences, University College of North Wales, Bangor, Gwynedd, N. Wales, UK. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 402 LIFE HISTORY OF THE BEAR PRAWN, PENAEUS SEMISULCATUS, IN COASTAL WATERS OF SOUTHWEST TAIWAN To establish an effective system for prawn stock enhance- ment in Taiwan, the Tungkang Marine Laboratory selected the coastal waters along southwest Taiwan as an experimen- tal area and conducted a series of ecological studies on commercially important prawns from July 1982 to December 1987. This paper reviews the life history of the bear prawn, Penaeus. semisulcatus, in this area. A strategy for stock enhancement for this species is proposed. Distribution The prawns occurred mainly from November to March in waters between Fonbitou and Fangliao at depths of 20-40 m, and in July, between the estuary of Linpien River and Fan- gliao at depths of 20-30 m. Larger prawns in general oc- curred in deeper offshore waters (Su and Liao, 1984; Su, 1988). Reproduction The prawns seem to spawn throughout the year with a peak season from December to March. The main spawning ground lies in waters between Dapong Bay and the mouth of Linpien River at depths of 20-40 m (Su and Liao, 1984; Su, 1988). Emigration from Nursery Grounds The prawns emigrated from Dapong Bay to open coastal waters from July to December, mostly during the hew moon or full moon phase, 1-2 months after the rainy season. The mean carapace length of emigrating prawns ranged from 20.7-33.6 mm for females, and 20.4—29.6 mm for males. Early emigrants were usually the smaller ones which migrate mainly from June to August (Su and Liao, 1987). Food and Feeding Based on frequency of occurrence the food items were, in order of relative importance, crustaceans, molluscs, detritus and sand granules for prawns from Dapong Bay; and detritus, sand granules and crustaceans for prawns from the open coast. Volumetrically, the order was the same as that de- scribed above (Su, 1988). MAIN FISHING SEASON E w age “Bx wis cz zgcg 4 omeu- uw Be u ufi i= & w J FMAM JJ AS ON D J F SSS RAINY SEASON MEMOIRS OF THE QUEENSLAND MUSEUM Growth The growth rate was 3.21 mm in CL and 5.6 g in body weight per month for females, and 1.8 mm in CL and 3.14 g in body weight per month for males. Life History and Stock Enhancement By integrating the above information, the life history model of P. semisulcatus is summarised as shown in Fig. 1. For stock enhancement, it is recommended that: (1) post- larvae should be released into Dapong Bay from January to March to enhance the recruitment in the nursery life phase; (2) juveniles should be released into coastal waters to supple- ment the recruitment in the offshore life phase; and (3) juveniles should be released when they are 10-15 mm in CL, optimally during March to May, and ideally in the nearshore waters between Tungkang and Linpin. Acknowledgements Without Misses I.F. Chen, C.D. Jong and C.S. Chen it would have been impossible to complete this paper. The study was supported by grants from the National Science Council (NSC79-0409-B056a-01). Literature Cited Su, M.S. and Liao, I.C. 1984. Preliminary studies on the distribution and the stomach contents of some commer- cial prawns from the coast of Tungkang, Taiwan. 57-71. In L.C. Liao and R. Hirano (eds) ‘Proceedings of ROC- JAPAN symposium on mariculture’. TML Conference Proceedings, No. 1. Su, M.S. and Liao, I.-C, 1987. Ecological studies on commer- cially important prawns from the coastal waters of South- west Taiwan — II. Emigration of Penaeus semisulcatus from Dapong Bay. Journal of the Fisheries Society of Taiwan 14(1): 49-59. Su, M.S. 1988. Some ecological considerations for stock enhancement of commercially important prawns along the coastal waters of southwest Taiwan. Acta Oceano- graphica Taiwanica 19; 146-165. Mao-Sen Su, Tungkang Marine Laboratory, Taiwan Fisheries Research Institute, Tungkang, Pingtung 92804, Taiwan. Max. # Reproduction range Min.? Max. ——~ mean Min. Ss Main spawning Main recruitment Main immigration FIG. 1. Model of the life-history of P. semisulcatus in the coastal waters of southwest Taiwan. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM =03 PATHOLOGY AND FINE STRUCTURE OF AMESON SP... A MICROSPORIDIAN FROM THE BLUE SAND CRAB, PORTUNLUS PELAGICUS Microsporidian parasites of crabs were first described by Perez (1904) in the muscle and haemolymph tissues of the common shore crab, Carcinus maenas (L.). To date, only 11 microsporidians representing 6 genera have been reported or described from brachyuran crabs. The Tew reports of microsporidjan infections in crabs may ‘be a result of their low prevalence in host populations, the low abundance or crypticism of certain host populations, 8 lack of expertise in identifying the disease, and/or a lack of proper fixatives in field situations (Shields, pers. obs.). In 1989 the authors found a microsporidian parasite in the musculature of Portunus pelagicus. Characteristics of the parasite placed it firmly in the genus Ameson (di- plokaryotic meront, moniliform sporant, unikaryotic spore, isofilar polar tube, microtubules projecting from the exospore of the sporoblast und spore). Ameson sp. from P. pelagicus is the (wellth micrasporidian reparted from a brachyuran host; a full description is in prepata- tion (Shields, unpubl.). The prevalence of Ameson sp. in the observed population of P. pelagicus was approximately 3.0% (N ~ 205 crabs). The protozoan caused massive destruction of infected muscle which was flaccid, and had a milky appearance common jo this disease. Necralic muscles contained meronts, sporoblasts, and spores, Ameson 8p. spores were alsy found in the blood cells and the ovaries. The parasite was found jninicellularly in the sarcoplasm of host mus¢le cells. Microtubules found on the exaspare of sporoblasis anc spares were if close proximity to host mitochondria, and may be used to Lransport muirients into DAILY AND MONTHLY SETTLEMENT PATTERNS OF BRACHYURAN MEGALOPAE ON ARTIFICIAL SUBSTRATES Postlarval recruitment appears lo be a major factor that determines density of adult stocks for several crustacean species, If the population dynamics of marine species are driven by recruitment, then an understanding of rectuitment processes and associated spatial and temporal variability ts important if accurate predictions of population size are lo be achieved. The objectives of the present study were; 1) to compare the temporal patterns of postlarval brachyuran séttloment in a South Carolina estuaty with selilement pat- lems in Other estuaries thal are separated over a broad geo- graphic scale; and 2) to relate settlement peaks lo periodic (tunar, tidal, light phase) and chance (wind) events, Megalopae were collected every 5 days trom artificial substrates at asite in Charlesion Harbor, Sourh Carolina from July 1987 through October 1988. In 1989, daily samples were laken rom July through November al (he same site, a6 well asin the York Riverand Tangier Island, Virginia (by Robert Orth and Jacques Van Montfrans, Virginia Institute of Ma- tine Seicnee) and in Delaware Bay (Charles Eprtanio, Uni- versity of Delaware) as part of a regional settlement study. Atthe South Carolina site, 19 taxa settled on the artificial substrates, with Callinectes sapidus, Uca spp., and Paropeus éerbstii numerically dominating collectivas. Alihough mep- abapae were present year-round, except during March, the the cyioplasm of the parasite. Adjacent uninfected muscle was lurgely unaffected. Allempls were made lo maintain the life cycle of the microsporidian in the laboratory. Infected muscle tissues were macerated and mixed thoroughly in a mixture of ane part seawater lo two parts freshwater, The supernatant was injected directly inta the axilla of the fifth pereiopod of ¥ crabs (0.5 mL supernatant/crab). An additional 4 crabs were injected with the seawaler-freshwater solution as a conjyal Infected muscle was also fed to seven crabs that had been without food for 3 weeks, Crabs injected with spores developed acute disease in approximately 2) days. Spores were delected in injected crabs after 7 days. Crabs that were ted Infected tissues did not develop the disease. Ameson michaelis from Callineeses sapidus is transmitted via cannibalism of infected hasss (Overstreet, (978). The failure of this route of infection with Ameson sp. trom. P. pelagicus may have fequlled from (he poor quality of meut that was presented to experimental crabs. Literature Cited Overstreet, R.M, 1978, ‘Marine niatadies? Worms, germs, and othersymbionts (rom the northern Gulf of Moxica’. MASGP-78-02). Mississippi-Alabama Sea Grant Con- sovtium, Ocean Springs, MS Perey. C, (904, Sur une Microspariviv parasite du Carcinus maenas, Compre Renda Societe de Biologie, $7: 214— 215 J.D, Shields and FE Wood, Department of Parasitology, The University af Queensland, St Lucica. Queensland 4067, Australia. ereatés! settlement of blue crab occurred from Augus} through October. Settlement patterns were highly episodle and suggested a pulsed recruilment to the study area. Con- siderable variabilily in the magnitude of settlement was observed among years. Temperature and wind direction Were the only factors which related to increased number of mege- lopac, Megalopae were significantly more numerous at neeht and displayed a semi-lunar pattern of settlement wilh peak tumbers occurring on quarter moans. When the lomporal settlement patterns observed in 1989 were compared among siles, a coherent pattern of settlement on a broad spatial scale emerged, with a major peak in the first Week of September. What appears to be more variable And less. predictable than the timing of settlement is its magnitude, which differs considerubly among years und locations and has. implications for variability In fishery stock size among the regions. Data from the regional study suggest that large-scale climatic and hydrographic conditions may be influencing Settlement. The spatial and Lempordl dynamics associated with seulement events can provide insights into Factors structuring blue crab populations and may actually indicate limits wo year-class strength. flizabeth Wenner, Jeanne Boylan, and David Knott, Marine Resources Research liusninte, P.O, Box 12559, Charleston, SC, USA. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum a4 VARIATION IN TIE REPRODUCTIVE STATUS OF SWARMS OF ANTARCTIC KRILL, The swarming behaviour of Antarctic krill. Euphausie superba, is central to jis biology, The bialogical composition of adjacent kmll swarms expressed through characteristics such as mean length, sex-tatio and stages in the moult cycle of krill may be very different. e.g, Watkins 1986. In addition the size range of krill in swarms tity: be testriclud jn com- parison to the Jaca) population (Mar, 1962; Hamner, 1984; Watkins, 1986). Such observations have given rise to pro- posals for sorting mechanisms based on differential swim- ming or sinking rites (Mauchline, (980; Kile, 1981), Here we consider the malurily and size composition ot animals in 38 swarms to see if a size-related sorting mechanism could uccount for observed distribution of maturity stages. Results and Discussion Swarms were sampled with w large Longhurst! Hardy plankton recorder (Bone, 1986) during a 14 day period in February and March 1985 from an ares approx 50 km square between Elephant Island and King George tsland, The lene and sexua] maturity slage were measured on up to 100 krill from euch swarm (Murris.ef al, 1988). ‘The sex Composition af swarms was highly variable, male and female krill were found in all swarms bul the relative proportions in the individual swarms varied greatly (propor lion male 19-98%). The swarms were also either virtually all adullorcontajned a large pfoporhion of subadults. In only 11 swans was (he proportion of adults less than the population averuge (83%), revching a minimum of 37% in one swarm, The relative Crequency.of occurrence of the individual matu- Tily slages within the swarms varied considerably, The two adult male stages were found in all swarms, bul no single female maturity siage occurred in every swarm, There was also variation in the nuraber of maturity stages in a swarm: some swarms comained every maturily sutge while in others as few us [wo siages were present, Animals ot similar malu- rity often accurred together as indicated by the significant correlations hewween al) The immature maturity sages and also between the more mature adult stages. The difference between the length of the largest and small- est krill within each swarm varied greatly (11-30 mm: me- dian 15 nim). The size range in the swarms was significantly more resiricted (han would be expected if the distribuuion of size range was random (Kolmogoroy-Smirnov testp<0.0101), Mature krill Wend to be larger than immature krill although ihere is some wyidence of size regression afler spawning. In addition, the mean size of cach particular maturity stage varied between swarms. In some swarms the mean lengths of each maturily stage were longer Ihan average while in others they were shorter than average. Could these pallens of maturity Stage rise as a result of thissize-related sorting? Associated maturity stages were nol necessarily of a similar size. There was na correlation (t = 0.175; P20.1) between the size differance of each maturity slage and the degree of association hetween maturity stages. Thus, for éxample, subadult male krill (MS1, MS2and MS3) Were usually found together bul the mean sizes of these stages ranged from 42.646.4 mm. In contrast, subauull mule krill (M53) and adult male krill (MA2) were negatively associated but the difference between the mean size of these stages was MEMOIRS OF THE QUEENSLAND MUSEUM UO.) MM, tals seems Unlikely that differences In sex ratio at The swarms could be explained simply by size differences in the maturity stages because the size differences between the equivalent male and female maturity slages (e.g. MA2 and FA4) were usially small, although sometimes statistically sitnificaal, Passive sorting mechamisms based on size-dependem swimming or sinking speeds and differential prowth may explain the witer-swarm differences in krill size, however, they appewr to account for little of (he infer-swarm variation i sex and maturity stage, The very low numbers of maturing females found without ajtached spermatophores sugeests that mating, must oceur rapidly after each moult, Because of the very uneven numbers of males and females in many swarms itis likely therefore that active behavigural responses are Important in bringing male and female keill together to mate. Thus the swarms containing only mature males may be actively searching far aggregations of mature female krill. However, the actual mechanisms for producing the observed swarm distributions of reproductively active and inactive miulurity stages have still ta be determined, Literature Cited Bone, D.G, 1986, An LLHPR system for adult Antarctic krill (Euphausia superba). British Antarctic Survey Bulletin 73; 3147. Hamner, WOM. 184, Aspects of schooling of Euphausia superba. Journal of Crustacean Biology 4: 67-74. Kils, U. L981, Size dissociation in krill swarms. Kiecler Mecreslorschung Sonderhalt 5; 262-263, Marr, J.W.S. 1962. The natural history and geography of the Amaretic krill (Luphausia superba Dana). Discovery Report 32; 33-464, Mauchline, J. 1980, The biglogy of mysids and cuphausiids. Advances in Marine Biology 18; 1-681. Morris, DJ, Watkins, -L., Ricketts, C,, Buchholz, F. and Priddle, J. 1988. An assessment of the merits of length and weight measurements of Antarctic krill Euphausia superba. British Antarctic Survey Bulletin 79: 27-50. Watkins, J.L. 1986, Variations in the size of Antaretic krill, Exphausia superba Dana, in sinall swarms, Marine Ecolowy Progress Serjes 31; 67-73, JL, Watkins, British Antaretic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 DET, UK, DJ. Morris, Metocean Consultancy Lid, Hamilton House, Kings Road, Haslemere, Surrey GU27 204, UR. F. Buchitale, Instetat fiir Meereskunde an der Universitit Kiel, Dsternbrooker Weg 20, D2300 Kiel, Germany. C. Rickens, Department of Mathematics and Statisttes, Plymouth Polytectnic, Drake Cirews, Plymauth PLA SAA, UR. J, Priddle, British Antarede Survey, Natural Environment Rescarch Council, High Cross, Madingley Read, Cambridge C83 OET, UK, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMBOIRS OF THE QUEENSLAND MUSEUM THE RESPONSE OF MYSID SHRIMPS TO PHYTOPLANKTON DISTRIBUTION IN 4 HIGH ENERGY SURFZONE Visible accumulations of (he dialom, Amaulas ausrralis, are characteristic of the surfzone along the Sundays River beach, South Africa, Generally the beach is characterised by active rip systems separated by welded bars. Distom accu- mulations are relatively close inshore adjacent to Tips and these occur ata frequency of 2 per running kilometre of beach (Talbot and Bate, 1987). Atthe breakpoint 250-300 m trom the swashline, wave height ranges Irom 1-6 m, Median particle size of beach sand isc. 260 um. Tides are semi-di- urnal, subequal; with u maximum spring tide range of 2,1 m, Water temperatures range from 15-24". Despite this physically harsh environment, two species of mysids are commonly oncountered. In (he breaker-zone, the bentho-planktonic Gasirosaccus psammodytes occurs in num- bers of up 200m”, Behind the breakers, the gregarious Mesopodopsis slabbert has been recorded In numbers of up to 15,000 tm, During the dity, Gasrrosaccus psammodyies is confined to the white-water zone where it exhibits a well defined paitemn of intra-specitic zonation, Brooding fomales are significantly more abundant within 10-20 m of the swashline, while males and immatures become progressively more abundant further distant from the beach. Advantages which accrue to brooding females are mostly linked to Jess frequent disturbance fram the substrate ws a result of reduced wave turbulence. Ioter- alia, physical toss of larvae from te brood pouch is reduced, Gastrosaccus psammmodytes is a tidal migrant and the pattern of intra-specific zonation is maintained over the tidal eyele, Close inshore, mysids utilise a rich, bul localised phyto- plankton food source, Diurnally, alongshore abundance uf adult mysids was significantly greater in arcas of phytoplank- ton accumulations (adjacent (0 fips) on four of five occasions. when patches were visible (Chlorophyll-a concentration > 40-100 mg m* (Campbell, 1988)). Qn all occasions, adults were dominated by brooding females. Water currents mus! play a role in dictating mysid distribution, bul under rela- lively calm surf conditions, the distribution of adults is interpreted as a response fo the food concentration gradient, This allows maximisation of food intake as mysids (particu- larly brooding temales) undergo forays info the water column. As the energy state of the surfzone increases, walet currents feeding into tips must play a progressively more importun} role in determining mysid distribution. Alongshore distribution of immature mysids is often different lo the wdull pattern. Since swimming ability of juveniles is weaker com- pared to adults, threshold water Velocities would be less with respect lo the influence currents exert on dispersion patlerns, Although adults may respond ta 4 food concentration gradient, prevailing current velocities may be sufficient to act as The nain forcing function in determining distribution of immature mysids relative lo the tips (Wooldridge, [989), Although Anaulus australis accumulations are generally closely associated with rip currents, cells are continually being added to and eroded from parehes as a result of ware currents, Cells eroded frum paiches may be entriined in tips and transported seawards, Ip the cases of major nip activily, phytoplankton muy also be transponed behind the breaker line, Here, the lack of air-bubble formation (cell buoyancy is due 10 attachment to aif bubbles) results in the sinking of cells Which then secumulate near the bottom of the waler column. Re-entry into the breaker zone will occur if Wave energy increases, which effectively stirs up the bottom and advects cells shorewards as waves begin t6 break further offshore (Talbot and Bate, 1988), Anuulus anstralts also exhibits a well defined patrern of temporal variability. In the late alternoon, cells become psammophyllic, adhering to sand grains a8 4 result of und- lomical changes al the surface of the cell's frustule (Talbot ind Bate, 1928). Consequently, Anaiu/us disappears from the waier column aid is nol available to mysids foraging clase inshore after dark. The non-availability at night of phytoplankton in the inner surfzone results in a concomitant chadge in the feeding behaviour of Gastresaccus psammodyres. The brooding component of the population remains lishore where they become more carnivoruus, feeding in lhe shallows om planktonic and benthic organisms. The more pelagic covm- ponent of the mysid population migrates offshore where thoy exploit the aceumulaled (oud source behind the breakers, They remain planktonic tor the remainder of the night, re rurning to their inshore habitat at dawn. A second species of mysid, Mesepodapsis slabberi also Ulilises the accumulated food source behind the breakers ar night. Since itis a pelagic species, it seldom ventures intu the Whitewater zone where it would be vulnerable to the more lurbulen! conditions experienced there. Anaulus australis is therefore not available as a toad Source during the day. Instead, M, slabberi remains in deeper water during daylight where it is less visible 10 predators feeding in the water column. OF Sundays River beach, swarms ol this species are encauntered at about 15 m depth where (hey remain in clase proxiniity to reels, After durk, there is o general migration onshore where they remain until dawn feeding behind the breakers (Webh and Wooldridge, 199U), Literature Cited Campbell, EE. 1988. *The estimation Af phytomass ang primary praduction ofa surlvone’ Ph.D, thesty, Univer: sity of Port Elizabeth. 429p, Talbot, M.M.B. and Bate, G.C. 198%. The spatial dynaniies af surf diatom patches im a medium energy, cuspare beach. Bolanica Marina 30: 459-465, Talbot, M.M_B. and Bare, GC. 1988 The use Of false bun uncies by the surf distam Anaulas biroserans in the formation and decay of cell patches. Estuarine Coastal Shelf Science 2: 155-157, Webb, P, and Wooldridge, TH. 1990. Die! horizontal migra- live of Mesopodapsis siabbert (Crustacea: Mysidacea) in Algoa Bay, southern Africa, Murine Ecology Progress Series 62: 73-77 7 Wooldridge, TH, 1989. The sparial and temporal distribn- lon ot mys shrinips and phyloplanklon accumulations in a high energy surfanne. Vie Milieu 39; 127-133. TH, Wooldridge, Department of Zovlagy, Box 1600, University of Porr Elizabeth, Port Elizabeth 6000, Savill Africae MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 406 LIFE HISTORY AND BIOLOGY OF SACCULINA CARCINI (CIRRIPEDIA: RHIZOCEPHALA) PARASITISING LIOCAR- CINUS HOLSATUS (DECAPODA: BRACHYURA) Among the six Rhizocephala families, the Sacculinidae com- prise the largest number of species. Sacculina carcini has been reported to infect species of grapsid, xanthid and portunid crabs, the latter including Liocarcinus holsatus (Boschma, 1955). In this study, samples of Liocarcinus holsatus were obtained from a beam trawl (2m wide with a 19mm mesh net and a 9.5mm cod-end) at approximately monthly intervals from a depth of 3-20m around the Gower Peninsula, South Wales, U.K. (15°35’N, 04°07°W). Each trawl, at a speed of 3-4 knots, was of 20 to 30 minutes duration. All crabs were examined for infection by Sacculina carcini and some of the infected ones (>200) were tagged and maintained in recircu- lating seawater systems for observations on Sacculina growth and reproduction. Results and Discussion Of a total of 976 male and 1166 female crabs caught, 35.7% of the males and 38.6% of the females were infected by Sacculina carcini. Double and triple externae infections were low (<2%) and occurred mainly in males. The time and magnitude of peak abundance of the different stages of infection differed between years. However, the timing and sequence of the life history events of Sacculina was very much related to that of its host (Day, 1935; Heath, 1971; Liitzen, 1984). Externae started growing as early as February or March but the growth of these in the autumn cohort was slow when compared with those which emerged and grew in summer. Externae grew from emergence to 3mm in width in about a week but many did not grow beyond this size unless impreg- nated by male cyprids, and eventually died leaving a scar. Emergence of externae occurred without the host having to moult. Overall externae growth rate (temperature dependent) was 5.5 + 2.1 S.E. mm/month in the field and 8.3 + 1.7 mm/month in the laboratory. Eggs were present in the mantle cavity throughout the year but were most abundant in winter and again in summer. In the field, eggs began hatching in March or early April, reached a peak between June and August and stopped in late October or early November. In the laboratory, two broods of eggs (5-12 x 10° each), at an interval of about one month during April-October and four months during December—March, were produced. Both the eggs in the mantle cavity, and the nauplii produced, were of two size classes; the smaller being the females. The length of the internal phase of Sacculina infecting L. holsatus was MEMOIRS OF THE QUEENSLAND MUSEUM estimated to be between 5 and 12 months (x = 8.3 months) and the externae were estimated to live between 6 and 13 months (x = 8.0 months). Only adult crabs (= 20mm CW) could be classified as being highly feminised. These resembled females in their external morphology and behaviour (Choy, 1986). Apart from imposing metabolic stress upon the host, Sacculina impairs if not completely stops its growth and reproduction (Lawler and Shepard, 1978; Rubiliani, 1983). Infection by Sacculina decreased growth rates by up to 30% in males and 25% in females for each year of infection. During this period, egg production was reduced by up to 62%. For commercially important portunid crabs such as Necora, Ovalipes, Por- tunus, Scylla and Thalamita, infection by Sacculina can have a disastrous effect on the fishery. Weng (1987) has shown that the normal management practice of protecting smaller crabs can result in higher infection by Sacculina. Under these circumstances, management strategies will need to be mod- ified. Literature Cited Boschma, H. 1955. The described species of the family Sacculinidae. Zoologische Verhandelingen 27: 1-76. Choy, S.C. 1986. Priapion fraissei (Isopoda: Entoniscidae) infections in Liocarcinus holsatus (Crustacea: Por- tunidae) from the British Isles. Journal of Invertebrate Pathology 48: 127-128. Day, J.H. 1935. The life history of Sacculina. Quarterly Journal of Microscopical Science 77: 549-583. Heath, J.R. 1971. Seasonal changes in the population of Sacculina carcini Thompson (Crustacea: Rhizocephala) in Scotland. Journal of Experimental Marine Biology and Ecology 6: 15-22. Lawler, A.R. and Shepard, S.L. 1978. A bibliography of the Rhizocephala (Crustacea: Cirripedia). Gulf Research Re- port 6: 153-167. Liitzen, J. 1984. Growth, reproduction, and life span in Sac- culina carcini Thompson (Cirripedia: Rhizocephala) in the Isefjord, Denmark. Sarsia 69: 91-106. Rubiliani, C. 1983. Action of a rhizocephalan on the genital activity of host male crabs: characterization of a parasitic secretion inhibiting spermatogenesis. International Jour- nal of Invertebrate Reproduction 6; 137-147. Weng, H.T. 1987. The parasitic barnacle, Sacculina granifera Boschma, affecting the commercial sand crab, Portunus pelagicus(L.), in populations from two differ- ent environments in Queensland. Journal of Fish Dis- eases 10: 221-227. Satish C. Choy, Universiti Brunei Darussalam, Gadong 3186, BSB, Brunei Darussalam. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM DISTRIBUTIONAL ECOLOGY OF THE VELVET SWIMMING CRAB, NECORA PUBER (DECAPODA, BRACHYURA, PORTUNIDAE) Around the Gower Peninsula (South Wales, UK), Necora puber is found mainly on rocky or stony substrata extending trom the lower mid-shore down toa depth of about 20 metres below chart datum (Choy, 1988). Routine monthly samples of N, puber were taken between October, 1983 and Sepiem- ber, 1985 at Langland Bay (51°32'53"N, 4°)" )8"W) and between November, 1983 and April 1985 at Worms Head Sound, Rhossili (51°33'42"N, 4°18'16"W), both on the Gower Peninsula, In the intertidal zone, crabs were caught by hand while searching (for 15 minutes at cach station of stratified design, and corresponding lo different tidal heights} under boulders and rocks during differen! phases of the tidal and diumal. cycles. Sublittoral samples (ta a depth of 20m) were obtained by SCUBA or snorkelling. Results and Discussion Catch rate was positively correlated ty water temperature (P<0.05), The increase in the catch rate of crabs in the intertidal zone between March and November was a result of more newly séttled juveniles (<)0mm CW) and migrant adults (>40mm CW), Adult crabs did not remain in the littoral zone permanently (Choy, 1988). Crabs migrated on- shore either to feed or moult during these warmer months (Crothers, 1968); many adults were in mating pairs. Adult females were ovigerous mainly between January and March, but not. between September and November (Choy, 1988). During winter most of the crabs (especially the adults) were found in the sublittoral zone where the temperature and salinity were more slable. However, complete emigration to ihe sublitioral zone did not take place as some large crabs were still found on the shore even during the cold months, particularly during low tides which occurred in the mornings. Such a pattern has also been reported lorC. maenas (Naylor, 1962; Crothers, 1968). Higher catches were obtained at Rhossili than al Langland Bay (P<0.01). There was also a marked difference in the size composition of crabs from the two Jocalities: crabs from Langland Bay being larger (P<0.01). At Rhossili, newly settled juveniles appeared in mid-June and continued to do so until the end of July; there were also some in September. During July, August and September, densities of up to 30 juveniles m’' were recorded. There was a progression of the 2.5mm modal width from June until January when the crabs reached about 27mm CW. At Langland Bay, newly setiled juveniles (the carly crab instars) were never observed al- though the laler instars (7-15mm CW) were. Perhaps larval 407 settlement does not take place here as a result of silliness, the strength af tidal streams, unsuitable substratum orsome other unidentified factor. However, if settlement does occur, it is likely that the numbers are very low and the crabs escape detection or they are immediately precated on. Boulders at Rhossili Wére smaller than those al Langland Bay (P<(,U5) and the size of crabs found under the houlders was correlated to boulder size (P<1.05).. However, the shape of the boulders was also important: flat boulders sheltered mare crabs, especially when these boulders overlaid smaller ones. This pattially explains the difference in the size com- position of crabs found at Langland and ar Rhossill. V. puber was never found under otherwise suitable shelters which had decaying organic material or anoxic substrate under them, During summer, smaller crabs were more abundant in the Fucus zone (mid-littoral, LWN-EBLWN),; the large ones found here were mainly males that were moulling or were aboultomoull Very few crabs were found in this zone during winter. Qvigerous females and copulating pairs were found only in the Laminaria zone (lower littoral, LWS-ELWS), During winter, the size composition of crabs in the intertidal zone differed depending on the time of day of sampling and the tidal phase. Larger crabs (mainly males) were caught during low tides thal occurred during the morming. During the Summer large crabs Were caught at all low tides imrespec- tive ot when these tides occurred. During the warmer months, increased exploitation of crabs for bait and associated disturbances of the boulders resulted in Jower abundance of crabs in the intertidal zone. I was eslimated that three to four tidal cycles were required for replenishment of explaied stocks in this zone. Literature Cited Choy. S.C. 1986. Natural diets and feeding habits of Liocar- cinus puber and L, holsams (Crustacea: Decapoda; Por- tunidag). Marine Ecology Progress Series 31; 87-99, 1988. Reproductive biology of Liacercinus puber and L. halsa(us (Decapoda, Brachyura, Portunidae) from the Gower Peninsula, South Wales. Marine Ecology 9; 227- 24). Crathers, J.H. 1968. The biology of the shore crab Carcines maenas (L.). 2. The life of the adult crab. Field Studies 2: 579-614, Naylor, E. 1962. Seasonal changes ina population of Car- cinus macnas (L..) in the littoral zone. Journal of Animal Ecology 31; §01-609, Satish C. Choy, Universiti Brunei Darussalam, Gadong 3186, BSB, Brunei Darussalam. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 408 THE COMMUNITY ECOLOGY OF THE PARASITES AND SYMBIONTS OF PORTUNUS PELAGICUS: EVIDENCE FOR POSITIVE AND NEGATIVE INTERACTIONS Portunus pelagicus possessed a diverse community of parasites and symbionts. In 1989, over 200 crabs were dis- sected and examined [or parasites and symbionts. The com- mon symbiont fauna was comprised of 6 prolozoans [Operculariella sp., Lagenophrys sp.. Acineta sp. (ciliates), Thelohania sp., Ameson sp.(microsporidians), Nematopsis sp. (gregarine)}; 5 helminths [planocercoid turbellarian, Levinseniella sp. (metacercaria), Polypocephalus more- tonensis (cestode), telraphyllid cestode, Carcinonemertes mitsukurtt (nemertean)}; 4 crustaceans [Chaniosphaera indi- cus (copepod), Sacculina granifera, Octolasmis cor, Chelonibia sp. (cirripedes)], and 6—7 fouling organisms from other phyla, A few rare parasites were found (Puranophrys sp., Hematodinium sp.). The sand crab may possessed an interactive community of parasites and symbionts. There were |! pairs of interac- tions/associations between species measured by prevalence (X°) or by log-intensily (ANOVA on presence/absence, and linear regression). Three pairs of interactions were between protozoa and metazoa. Five pairs in the log-intensity data were reciprocals, i.¢. there were significant interactions be- tween both species. There were 3 negative associations (Car- cinonemertes vs Sacculina, Polypocephalus (a lecanicephalid) vs Levinseniella (a microphallid), and Octolasmis cor vs Operculariella sp.): the remaining, associations were pasi- live. Since association may not be a result of direct species interaction, methods to substantiate the significant associa- tions are being investigated. The rhizocephalan barnacle, Sacculina grantfera, had a marked effect on the assemblage of fouling species. Since sacculinised crabs do not moult, there was a notable increase in the diversity of foulmg species that live in the branchial MEMOIRS OF THE QUEENSLAND MUSEUM chamber and on the external surfaces of the host, The rhizo- cephalan also had negative effects on other symbionts, The ege predalor, Carcinonemertes mitsukurii (Nemertea), was commonly found on the gill lamellae of post-ovigerous female crabs (Prevalence ~ 53%). In the sacculinised female host, C. mitsukurii was absent. Further, roouets os S. granifera were observed in contact with recently dead P. moretonensis, and Levinseniella sp. The statistical analyses, however, showed no significanl association between the thizocephalan and these two helminths. Positive associations were numerous and may have re- sulted from prey finding abilities (planocercoid turbellarian vs branchial and external symbionts), host food preferences (P. moretonensis vs tetraphyllid cestode), or association with other host behaviours. * Here, 1 show that symbionts may interact within and between different microhabitats (guilds?) of the host. The host may mediate the interaction between certain species, especially those that are pathogenic, e.g. S, granifera vs C. mitsukurii, because these species do not overlap in their tespective host microhabitats but do overlap in their host resource use, ¢.g. reproductive products. Lastly, the commu- nity of parasites and symbionts in P. pelagicus did not fil the current definitions and models of communities and commu- nity interactions that predict few interactions between spe- cies in between guilds in ‘isolationist’ communities (Holmes and Price, 1986) Literature Cited Holmes, J.C. and Price, P.W. 1986. Communities of para- sites. 187-213. In D.J. Anderson and J. Kikkawa (eds) ‘Communily ecology: Pallern and process’. (Blackwell Scientific Publications: Oxford). J.D, Shields, Department of Parasitology, The University of Queensland, St Lucia, Queensland 4067, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum THE JAPANESE MARKET FOR CRUSTACEANS "VERRY SMITH, ANTHONY KINGSTON AND TONY BATTAGLENE Smith, P., Kingston, A. and Batlaglene, T. 1991 0901: The Japanese market forcrustaceans. Memoirs of the Queensland Museum 31: 409-419. Brisbane. ISSN 0079-8835. The Japanese food market is undergoing major changes. Some of the factors influencing these changes on the Japanese seafood market are examined. These include supply-side developments, such as the impact of the rapid development of aqua-culture-sourced products and the changing availability of seafood from capture fisheries. On the demand side, they include the increased “westernisation’ of Japanese culture, changes in the demographic characteristics of the population, increasing incomes and wealth and improve- ments in the availability of alternative products. Results of recent ABARE studies of Japanese seafood demand are drawn upon, with an emphasis on those results relevant to crustaceans. Price relationships between seafoods, and between seafoods and meats are discussed, as is the growth in consumption in different market segments. [] Japanese market, demand trends, prawn mitrket. Perry Smith, Anthony Kingston and Tony Battaglene, Fisheries Economics Research Section, Australian Bureau of Agricultural, and Resource Economics, Canberra, Australian Capital Territory 2600, Australia; 6 July, 1990. Japan's limited agricultural base and its pro- ximity to highly productive seas has resulted in its long recognised dependence on fisheries pro- ducts as a source of protein. The importance of fisheries products in the Japanese diet increased significantly in the 1950s and 1960s, In 1960 fisheries products supplied almost three-quarters of the total intake of animal protein in Japan (ABARE, 1988: 277). While consumption of all fisheries products has continued to increase, there have been major changes in the types of seafood consumed and in the factors influencing their consumption, The most apparent of these changes has been in crustacean consumption, which has increased from largely ceremonial and festivity use to more widespread general consumption, To examine these changes in the Japanese market for crustaceans and the factors behind them, it is useful to first examine the changing demand and supply relationships between fish- eries products and other foods before examining those factors specific to crustacean markets. SUPPLY DEVELOPMENTS DoMESTIC PRODUCTION Although fisheries products were an obvious source of protein for the Japanese people, it is only since the Second World War that fisheries products have been consumed in yery large quantities. Fisheries products were the main source of animal protein until the 1960s, as their domestic production could be expanded to meet nutritional needs without the country having to use scarce foreign currency reserves to purchase imports of other foods, As part of government efforts to improve di- etary standards, the fishing industry was cn- couraged to expand into offshore and distant water operations. It did so successfully, and these fisheries provided Japan with the majority of its fisheries products and were the main source of growth in landings during the 1960s. How- ever, in the 1970s twa ail price shocks forced a rationalisation of distant water fishing (ABARE, 1988; 273), Reduced access to foreign waters resulting from the introduction of the exclusive economic zone regime over the period 1977— 1980 reinforced this trend. Despite an increase in production levels be- tween 1970 and 1984 (Fig. 1), Japanese supplics of domestically landed fisheries products used directly for human consumption have remained relatively static. There have been significant changes in the catch composition, with an in- crease in (he importance of lower valued pelagic species landed from offshore fisheries (10-200 nautical miles from shore). Sardine catches were negligible in 1970 but represented 42% of total catches in 1986. These species have not gener- ally been used to meet consumer demand for fish, rather they have been used for processing — sardines into fishmeal, and others into fish- based consumer products such as surimi, Be- cause of the increasing importance of these 410 Figure 1: Total catch by fishery Marine culture 12 Bian water FIG. 1. Total catch by fishery. species, the amount of domestically caught fish used directly for food has remained static since 1975 (ABARE, 1988: 268). While representing only a very small com- ponent of total Japanese landings, production of crustaceans has shown a similar growth pattern, with output increasing during the late 1950s and the 1960s (Table 1) before stabilising at around 150 kt. Crab has been the main crustacean pro- duced by Japan. Since 1970, crab landings have varied around 90 kt, with gazami (blue crab) and king crab the most valuable species per unit weight. Japanese spiny lobster production has been stable at around 1.1 kt. Prawn catches have varied around 60 kt. The most valuable species of prawns caught in Japanese waters are the white prawn taisho ebi (Penaeus orientalis) and a black striped prawn, kuruma ebi (P. japonicus), the latter because of its ceremonial importance. MEMOIRS OF THE QUEENSLAND MUSEUM The other main crustaceans which are highly valued for traditional use are gazami, snow crabs and Japanese spiny lobster. There are limited prospects for increased domestic landings of crustaceans from capture fisheries. There has been considerable effort to increase domestic production through culturing of a number of crustacean species in Japan during the 1980s, and a culture industry has been established focussing on the market for live kuruma prawns (Fishery Journal, 1989). How- ever, while much of the culture technology adopted worldwide was developed in Japan, the results of crustacean culture in Japan have been less successful than elsewhere, while in contrast the Japanese aquaculture industry based on fish and mollusc species has prospered. FISHERIES TRADE With the rapid expansion in fishing operations, Japan was a net exporter of fisheries products until the mid-1970s. However, during the 1970s imports of fisheries products increased rapidly, their value increasing threefold between 1975 and 1979 to over US$4077m, while exports in- creased more slowly to around US$700m. Since 1977, Japan has been the largest single importer of fisheries products, accounting for over 25% of the total value of world imports. There was a number of demand and supply factors behind these changes. These included strong growth in demand for some high value products, due in part to increasing incomes and TABLE 1. Japanese landings of crustaceans (liveweight). 1965 Prawns — Freshwater — Kuruma — Northern — Other Lobster — Japanese spiny 1300 1 600 nas = Not available separately. Source: FAO (1989). 1970 1975 1980 6 840 3 831 1996 63 340 5 846 4816 3 853 6 020 1609 - 45 524 48 971 4229 2 807 1 823 56 24 187 21314 46 030 53 382 5 227 351 10 322 83 737 1500 1086 1065 1118 THE JAPANESE MARKET TABLE 2. Japanese imports of edible fisheries products 1970-84: Product weight. 1970) = 1980s 198T) = 1982) 1983) 1984 =: 1985 kr kt kL kt kt kt kt Fresh, chilled or frozen fish — Tuna 36.6 — Other fish 534.6 Total 91.2 108.4 1102 232.3 346.4 340.7 456.6 Fresh, chilled or frozen crustaceans und molluscs — Prawns 57.2 144.7 163.4 — Squid, cuttlefish, clams, abalone and oysters — Other crustaceans and molluscs é 68.5 71.7 Total 390.6 424.4 17,4 Processed fish, crustaceans and malluscs (salled, smoked or dried) — Fish and roes 9.4 45,0 49,1] 53.0 30.8 58.6 56.4 — Crustaceans and molluscs 12.4 18.8 20.6 20.8 20.9 30.0 36.0 Total 1. 63.8 69.7 73.8 51,7 88.6 92.4 951.6 (808) Total imports (976) (944) 1986 kt 58.3 46.6 104.9 963.6 1095.2 1237.8 1390.4 1614.7 (878) (1 146) (1071) Excludes seaweed. agar-agar, oilsiand fats, pearl, live fish and shellfish, preparations nol in airtight containers, corals. home aquarium fish, fingerlings for culture, caviar, sponges, shells, offal, wax and glue. nas = Not available separately. Note; Figures in parentheses indicate value in billion yen, Sources: JETRO (1981); Japan Tariff Association (1986). 411 in part ta their improved availability from over- seas sources, and reduced domestic industry competitiveness due to lower resource availabil- ity and the appreciation of the yen. Trade restrictions have also shaped Japanese fisheries trade, in two main ways. Firstly, there have been significant restrictions on imports of potential substitute products, such as beef (ABARE, 1988). Secondly, the types and quan- tities of fisheries products imported have been strongly influenced by quota and tariff restric- tions. Quotas. are imposed on four groups. of fisheries products (ABARE, 1988: 30) while tariffs apply to most fisheries. products. Tariffs applied to crustaceans range from 3% for frozen prawns to 6% for crabs. Higher tariffs are applied to processed products to encourage domestic processing of imported fisheries products. The rapid growth in imports of fisheries pro- ducts has had a major impact on Japanese markets over the 1980s. In 1970 imports sup- plied 5.3% of the 5.6 Mt total of fisheries pro- ducts used for food. By 1985 this. had grown to 22.4% of a total of 8.4 Mt. The main growth in the period 1970 to 1985 was in imports of fresh and frozen fish, which increased eightfold to 770 kt, Crustacean and molluse imports increased fivefold to 525 kt in the same period, The main single product in this category was prawns, im- ports of which increased from 57kt in 1970 to 1&5 kt in 1985 (Table 2). Imports of fisheries products have continued to rise strongly since 1985. Total imports of fisheries products have increased by 12% a year to 2661 kt in 1988, providing 30% of total sea- food consumed in Japan (MAFF, 1990: 38). Prawn imports have increased at an average an- nual rate of just under 10% a year, reaching 263 ktin 1989. Crab and lobster imports, while much lower, have also recorded strong growth over this time (Table 3). However, the total value of 412 TABLE 3. Japanese imports of crustaceans. Prawns — Live — Frozen Rock lobster — Frozen — Live nas = Not available separately. Source: National Marine Fisheries Service (1990). crustacean imports has risen only 2% a year over this period, to ¥400 million in 1989. PRAWN IMPORTS The rapid growth in supplies of imported prawns has dominated market prospects for crus- taceans since 1985 and is likely to continue to do so through the next decade. In 1960, imports of prawns were only 0.6 kt but in only 30 years this has grown to well in excess of 250kt. However, the recent strong growth in imports has been mainly due to significantly lower prices. Since 1985 the unit value of Japanese prawn imports has fallen by an average of 7% a year (Fig. 2). The growth in Japanese prawn supplies has been due to increased imports from three sources: @ aquaculture production; e increased commercial fishing for prawns for export in preference to domestic (often sub- sistence) consumption; and @ increased concentration of the world prawn trade on the Japanese and, to a lesser extent, the US market. Aquaculture has had a spectacular impact on world prawn supplies. Total cultured prawn pro- duction has grown from around 30kt in 1975 (2.3% of world supplies) to about 560kt in 1988 (26% of world supplies), an average annual growth rate of over 25%. Most of this growth in production has occurred in Asia, with large increases initially in Taiwan, China, Indonesia, the Philippines and, more recently, Thailand (Table 4). Japan has been the most important market for cultured prawns, for a range of reasons. These include the close proximity to the main prawn See tee [ooo | + | vo00 | + | vo00 | + | ¥000_| ies si 43 511] 212805] 306722] 245892] 334864] 258232] 327202 5s i 33 887| 33531] 44418] 37736] 60024] 53 456 8707} 21046 9249} 18513] 10737) 20796 nas nas nas nas nas nas MEMOIRS OF THE QUEENSLAND MUSEUM 40 a 1 626 56 802 53.786] 56269] 54691 11991} 22467] 12224 1908 6095 2.342 24 726 7739 culture growth areas in Asia, and the Japanese market acceptance of black tiger prawns (the main cultured species) because of its similarity to kuruma and brown tiger prawns. The strength of the yen against other currencies, particularly the US dollar, has also allowed export returns to be maintained at high levels while Japanese wholesale prices have fallen. Without this appre- ciation of the yen it is unlikely that the Japanese market would have been able to sustain these growth rates, The rapid growth in cultured prawn imports by Japan has had a number of important effects on the prawn market. These include major changes in the species composition and in the seasonality of supplies, and a major buildup in stock levels. CHANGES IN SPECIES COMPOSITION It is estimated that in 1989 Japan imported 118 kt of cultured prawns, some 45% of total prawn imports. Black tiger prawns were most impor- tant, with 86 kt, sourced mainly from: Indonesia (30.8 kt), Thailand (29.5 kt) and the Philippines Figure 2: Japanese imports of prawns 300 3000 Imports 250 2500 200 2000 150 1500 T ¥kg 1987 1988 “88-89 kt 1982 1983 783. .-84 ——— 1984 -85 1985 1986 [_ 86-87 FIG. 2. Japanese imports of prawns. THE JAPANESE MARKET 413 TABLE 4. Cultured shrimp production in Asia, 1975-1988. 1980 ki kt China Taiwan PC Indonesia Thailand Bangladesh India —M fA ASR owmooource Philippines Vietnam Re reso eSocoowouws p = Preliminary. Source: Ferdouse (1989). (16.5 kt), while the remaining 32.2 kt was of white prawns, mainly from China (Ferdouse, 1989). The development of aquaculture has caused a major change in the species composition of im- ports. The Japanese market was previously heavily segmented on the basis of particular species and sizes for specific uses. Tiger prawns were largely restricted to use in functions which required a red striped colour for presentation purposes. The increase in supplies has resulted in their more widespread use in a range of other outlets which were previously supplied by other, less favoured, prawn types and sizes which had less demanded characteristics. This has, in turn, placed pressure on suppliers. of other prawn types to try to maintain their own market posi- tion. Cultured prawns have also drastically altered the size composition of supplies on the Japanese market. While the large majority of cultured prawns were previously of medium and small counts, technological changes in feeding and breeding technologies used have allowed culture operations to increase the size of prawn pro- duced to take advantage of the higher prices for larger prawns. The consequence of this high grading is that price relativities between species and sizes have altered. SEASONALITY OF SUPPLIES The growth of cultured prawn supplies has drastically altered the seasonality of supplies on the Japanese market, particularly as a result of the instability of production of the main prawn exporters over the past four years. Prior to the 1984 1985 1956 1987 1988 kt kt kt kt 70.0 65.0 48.0 16.0 13.5 153.0 75.0 55.0 30.0 14.5 18.4 22.0 27.9 35.4 7.0 15.0 180.0 45.0 82.5 70.0 18.0 23.5 33.6 25.0 265.8 399.9 477.6 100.0 210.0 300.0 adoption of aquaculture, Japan had developed a pattern of stock buildup prior to the main periods of consumption (March to May and October to December). Imports and stock levels are now coming to be driven more by production consid- erations. This appears to be particularly the case with Chinese production and supplies from some other Asian countries where cold storage facili- ties are not available, Fig. 3A shows the imports of prawns by month for the past two years for the Figure Sa: Imports of prawns by Japan By major producer 6000 Indonesia \ eT ae a a, TR XUIVAL TSF *4 EY APO Cea i China —W Figure 3b: Prawn imports to Japan gure Monthly Pp Jap /RpMAM ToT FIG. 3. Imports. of prawns to Japan. a, by major producer; b, monthly. 414 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 5, Consumption of fish and meat per person in Japan. Fish and shellfish Pork td te Wd by bd hd Gd he te td Rb PANIWN fie SP ON lo Se ee bo a RB ic mel Source: ABARE (1988); MAFF (1989). three largest exporters of prawns to Japan. Fig. 3B shows the total prawn imports by month for the past two years compared with 1984 to il- lustrate the changes which have occurred in im- port patterns. COLD STORAGE HOLDINGS A key feature of the Japanese market since the early 1980s has been the rapid buildup of prawn stocks in cold storage (Fig. 4). While initially stocks were held to match the seasonality of sup- plies with demand, the excess supplies on the Japanese market have resulted in growth of stocks to a level where they are likely to have a significant impact on prices paid to exporters. DEMAND FOR FISHERIES PRODUCTS AGGREGATE CONSUMPTION PATTERNS Fundamental changes have taken place in the dietary patterns of the Japanese people. While the amount of food consumed per person has not al- Figure 4: Prawn consumption Domestic production. Pa kt Cold storage has ag 199 79 BY $88 85 187 789 FIG. 4. Prawn consumption. Poultry Meat Beef and veal Total fish and meat ct c 7 oe DS LEENA Nenana SAME PNyPveNro k 0. 5. 2. 0. 6. 5. 3. 7, 9, 0. NNOW UO ha 3 3 4 45 5 5 5 5 5 6 ao Tr ~ oo hh GSN El Pi Be Be bbb = Nawoenmnwopnoa tered greatly — average calorie intake per person growing only moderately, from 2200 calories per day in 1960 to around 2500 calories per day in 1980 (Kester, 1980) — the composition of their food intake has changed considerably. Meat and seafood consumption has more than doubled since 1960 (Table 5), Consumption of carbohydrates, predominantly rice, has steadily fallen, from 115kg per person in 1960 to 88kg in 1975 and 73kg in 1986 (ABARE, 1988). While consumption of fisheries products has continued to increase since 1965 it has done so at a slower rate — though from a higher base — than has consumption of meat products, with the result that fisheries’ contribution to average daily intake of animal protein has fallen from 74% in 1965 to around 45% in 1988. There are a large number of factors influencing the demand for a particular food, including its price, prices of substitute products, incomes, taste preferences, demographic factors and traditions. All of these factors have been important ele- Figure 5: Relative consumer price movements 1970 1985 | 1975 1980 FIG. 5, Relative consumer price movements. THE JAPANESE MARKET ments behind changes in consumption of lisher- ics products. Fisheries products have become more expen- sive relative (o pork and chicken (Fig. 5) and the changes in market shares may reflect consumer reaction to these changes in relative prices, In- come levels have risen strongly over the period and changes in consumption may reflect an abil- ity and willingness to purchase more desirable foods, Changes in lifestyle associated with in- creasing “westernisation’ of Japanese culture will also have influenced food demand. To better identify the relative importance of the major factors behind changes in consumption of fisheries products, ABARE developed a model to analyse the implications of these changes on the demand for seafood (Kingston, Smith and Beare, 1990). Though a number of models of Japanese meat and seafood demand relationships have been developed in (he past, most of these are now likely to be of limited relevance to the current situation in view of the changes which have occurred. (Summaries of the results of a number of these studies are pro- yided in Coyle (1983) and in Dyck (1988).) Another major problem of earlier models ts thal they aggregate numerous seatood types. inevi- tably reducing the rigor of the analysis (Kester, 1980). More importantly from the perspective of people interested ina particular group of seafood products such as crustaccans, agercgated models do not provide the level of detail required to address the key issues, such as those associated with rapidly increasing prawn supplies. The first aspect examined by Kingston et al. was the source of growth in consumption, Demand was examined at three levels: aggregate demand, household demand and demand outside the home, An important effect of Japan's in- creasing prosperity and ‘westernisation’ isthat a high proportion of the increased quantities ot Meat und seafood caten have been consumed outside the home, This pallern is consistent for each of the six commodities included in the study: beef, pork, chicken, tuna, other fish, and crustaceans (Fig, 6), JETRO (1987) attributes this increase in cat- ing-out partly to jncreased leisure time and in- creased disposable incomes, Another possible reason for the increased consumption outside the houschold is the fact that there are more working women in (he workforce, Williams (1989) sup- ports this claim, and notes that with the recent trend of working wives re-entering the wurk- force, most shopping is now done after work and more meals are being consumed al restaurants in shopping centre arcas. This trend has also re- sulted in a grealer proportion of seafood being consumed in restaurants, ESTIMATED PRICK RELATIONSHIPS To ¢stablish the price relationships between the commodities a two stage demand system wpprouch was used. [n the first stage the demand relationships between the three meats and sea- food were examined; in the second stage the seafood group was disaperepated into three com- modities — crustaceans, tuna and other fish. Tables 6 and 7 contain the estimates of the responsiveness of demand to changes in prices of these commodities in the markel as 4 whole and in the houschold sector of the market. The t-ratios given below the estimates were calcu- lated using Monte Carlo simulations of the par» ameter estimates using the variance-covarianee matrix of the estimates. The results obtained from the aggregate model suggest that the demand for seafood in total is relatively unresponsive lo changes in its price bul nevertheless more price responsive than are the other meats examined. Over the total Jia panese market a 10% increase in seafood prices would be expected to result in un 8% reduction in consumption of seafoods and a boost to con- sumption of alternative meats, mainly chicken (up 6%) and beef (up 4%). n the aggregate market the demand for in- dividual seafoods (Table 6B) was found to be less responsive to price changes than was the demand for seafood in total (Table 6A), with a 10% increase in the ‘own price” expected to resultina4% fall in consumption of crustaceans, a4.5% fallin tuna and a 6% fall in fish consump- tion, A surprising aspect of the results was the indication of a complementary: relationship among the seafood commodities. For example. 4 rise in fish prices appears to have a similar downward effect on demand for crustaceans as on the demand for fish. The household sector results (Table 7A) were consistent with expectations. The demand for beef was found to be highly responsive to changes in its price, a result consistent with its luxury status, while pork and seafood were less responsive. There was a strong substitution rela- tionship between beef and seafood (meaning that an increase in the price of ane cammodity will lead to less consumption of that food and more consumption of the other), with the effect of seulvod prices on beef demand much stronger 416 1983 19 MEMOIRS OF THE QUEENSLAND MUSEUM ————_____— ~ ie —— == Away from home _ be RTs 98 83 9 POR ores ee 979 1980 1981 1982 1983 1984 1985 1986 yg oe Household fe FIG. 6. Consumption of the six major commodity types. a, beef. b, pork. c, chicken. d, other fish. e, tuna, f, crustaceans, than that of beef prices on seafood. A 10% rise in seafood prices was estimated to result in a4% increase in beef demand while a similar rise In beef prices would only result in a 2% rise in seafood demand. In the household sector the demand for crustaceans was found to be very strongly re- sponsive to changes in prices (Table 7B) with a 10% fall in prices leading to a 32% increase in consumption. Tuna demand was also found to be strongly responsive to price changes, while other fish, being more of a staple food, was much less responsive to price changes in the household sector. It is relevant to note that the demand for crustaceans was found to be far more responsive to changes in fish prices than was the demand for fish. The difference in results between the home and aggregate analysis indicates that consumer be- haviour is quite different in the household and away-from-home sectors. In particular, the lower price responsiveness in the aggregate sea- food system, and implicitly in the away-from- home sector, suggests thal factors other than THE JAPANESE MARKET TABLE 6A, Aggregate meat and seafood system. Response of with respect to change in price of demandfor Beef Pork Chicken Seafood Beef -0.62 (3.6) 0.18 9 Pork Chicken (1.0) 012 (1.7) Seafood Source: Kingston et al. (199), Figures in parentheses aye [-ratios. TABLE 6B. Aggregate seafood system, Response of demand for with respect to change in price of Crustaceans Tuna Fish Cruslaceans Tuna Fish price, such as tradition, are important influences on aggregate seafood consumption. At the household level, the demand for individual sea- food commodities, particularly crustaceans, shows strong price responsiveness. Significant substitution effects between the three seafoods were also identified. Any fall in crustacean prices should increase overall crustacean consumption, with the greatest growth occurring in the household sec- tor. Trade information supports this view, for although the household market accounted for only 25% of total crustacean consumption in 1986, around half of the increase in prawn sup- plies in 1988 was reportedly being sold through supermarkets for household consumption (FAO, 1990). There appears to be considerable poten- tial ta increase household crustacean consump- tion, though the substitution relationships in the household sector suggest that some of this in- erease will be at the expense of reduced tuna and other fish consumption. RELATIONSHIP BETWEEN SEAFOOD AND BEEF Particularly since the recent decision to liber- alise the Japanese beef industry, an under- standing of the relationship between the seafood and beef markets 1s of concern to the aquaculture and prawn fishing industries, Beef supplies are forecast to increase rapidly, and by 1991 con- sumption is expected ta be 15% above current levels, 417 TABLE.7A. Household meat and seafood system. Response of demand for with respect to change in price of Beef Pork Chicken Seafood Beef Pork WV 0.14 (7.2) (1.4) 0.16 ~0.4 (1.6) (2.7) 0.11 -0.01 (0.5) (0) (1.0) 0.19 -0.04 -0,01 (3.2) (0.5) (0) 0,04 (0.5) -0,01 (0.1) ~(1.39 0.42 (2.3) -0,2 (1.0) -0.13 (0.5) -0.43 (2.4) Chicken Seafood Source: Kingston et al. (1990), TABLE 7B. Household seafood system. Response of demand for with respect to change in price of Crustaceans = Tuna Fish 2.17 (8.0) 0.07 (0) -0,68 (0) (14) Crustaceans Tuna Fish The results suggest that any fall in beef prices following the increase in supplies will lead to a less than proportional increase in total beef consump- tion, and that growth will take place in both the household and away from-home-sectors of the market, However, no significant relationship was found between beef prices and seafood consump- tion al the aggregate level, suggesting that seafood consumption may not fall substantially with in- creasing beef consumption. There is some substi- tution between beef and seafood in the household sector, but changes in the price of seafood appear to have a far greater influence on beef demand than vice versa (an expected result, in view of their relative importance in consumption). It should be nated that the consumption rela- tionships Were estimated in times of very rigid beef import restrictions. The magnitude of the expected change in beef supplies following trade liberalisation may be sufficient to alter existing consumption behaviour, However, it does seem that any resulting changes in seafood consump- tion will occur primarily at the household level. Since most crustacean consumption occurs on the away-from-home market, it seems unlikely that the changes taking place in beef trade will have a strong impact on crustacean markets. INCOME GROWTH Growth in income levels has. been postulated as one of the main factors behind the changes in Japanese food consumption patterns. Japanese 418 economic growth remained consistently high in the 1960s and 1970s, with average annual in- creases in gross domestic product of 7.2% be- tween 1960 and 1983, the highest of any OECD member (the average for all OECD countries was 3.7%). Even though Japan’s savings rate is higher than in most other western industrialised countries, growth in private consumption expen- diture in Japan was stronger than for other OECD countries with average growth of 5.1% per year over the same period (ABARE, 1988: 20-23). Previous studies suggest that the influence of increasing incomes on consumption of prawns is likely to be very low. A study of prawn consump- tion from 1959 to 1981 showed that a 10% increase in per person income resulted in a 0.6% increase in prawn consumption, while the effect of prices was much stronger, with a 10% fall in prices resulting in an 8% rise in consumption (Rackowe et al., 1983). While this study is now dated, the continued high importance of price factors suggest that the influence of consumer income on prawn consumption is still low. IMPACT OF AQUACULTURE ON SEAFOOD DEMAND Prawns are the dominant crustacean output from the aquaculture industry at the moment, but it seems inevitable that techniques will be developed to enable large scale farming of a wide range of fish and shellfish species. The consequences of such developments are likely to be substantial, significantly altering prices for those and substitute products. As the results outlined indicate that Japanese demand for seafood in general, both in the aggre- gate market and in the household sector, is re- sponsive to changes in seafood price, it would appear that increased supplies from aquaculture will result in a more than proportional fall in prices in order to stimulate consumption suffi- ciently to absorb those increases. For aquaculture species of prawns, however, at current supply levels, import prices will largely be determined by the household market, as this is the marginal market for these prawns in Japan. The household market for crustaceans is extremely price sensitive, and a small fall in prices will lead to a very much larger percentage increase in household consumption. As a result this market may in future act as a buffer to further major falls in price. (Conversely, if there were any significant increase in retail crustacean prices, due to a reduction in imports or a weak- ening of the yen, the household market is likely to contract sharply to absorb those increases.) MEMOIRS OF THE QUEENSLAND MUSEUM The segmentation of the Japanese market, based on species characteristics, has weakened as a result of the strong growth of cultured sup- plies of black tiger and taisho prawns. There is now much greater emphasis on relative prices, and considerable substitution between farmed and captured prawns. With the continued strong growth in supplies of cultured prawns and ongo- ing marketing problems, a key issue for capture fisheries will be to protect their specific market niches. The price differentials between species and counts which existed prior to the expansion of aquaculture have changed considerably with the changes in species composition, and this trend will continue, with pressure to substitute black tiger prawns for more highly valued spe- cies with similar characteristics. FUTURE PROSPECTS The key influence on prospects for the Ja- panese prawn market is the likely future growth in supplies. While the large majority of capture fisheries are either at full exploitation levels or overexploited, there remain two potential areas of growth in supplies to the Japanese market — an increase in aquaculture production, and an increase in the proportion of production entering international trade. Though a slowdown in growth is expected in the 1990s, it is nonetheless anticipated that cul- tured prawn production will be between 800kt and 1300kt by the mid-1990s. With capture fish- eries largely fully exploited, this growth in cul- tured prawns will result in an increase in world supplies of between 11 and 33% to between 2300kt and 2800kt in the mid 1990s. The differ- ences in these available estimates are crucial in examining the long term prospects for prawns, and point to the need for reliable monitoring of supply developments. There are several factors which suggest that the recent downturns in prawn prices will result in only a minor slowing in the rate of increase in prawn supplies to Japan. Prawn exports have increasingly been encouraged as a means of rais- ing foreign exchange earnings. This has resulted in a high emphasis on development of aquacul- ture operations geared to export markets, while in many capture fisheries it has meant a transfer from subsistence fishing to commercial opera- tions, with a consequent increase in fishing effort and catches. It has also resulted in a higher proportion of total catches entering world trade. As trade relations have improved in Asia, THE JAPANESE MARKET prawn exports have been seen as one means of financing increased imports of manufactured goods. Both China and Vietnam have entered arrangements with Japan which have involved the transfer of fishing technology and vessels in exchange for prawns. Much of the aquaculture industry in South-east Asia has also been developed specificially for the export trade. While it is difficult to assess the alternatives available to culture operations, it is likely that a high proportion of prawn culture operations have few alternative uses, particu- larly in the short and medium terms. The fall in Japanese prices is likely only to slow the rate of investment in new ventures. The lower costs of production in these countries, particularly in ex- tensive and semi-intensive operations, is ex- pected to ensure continued, but lower, profitability in existing prawn culture activities and only a small slowdown in the growth of supplies. While there is scope for further increases in Japanese consumption of prawns, these in- creases will largely be as a result of lower prices to consumers. The results of the ABARE study outlined here suggest that to further stimulate Japanese consumption of prawns, some further falls in prices will be necessary, but these may be less severe than those recently experienced. However, a major contraction of supplies would be required before any recovery of prices on the Japanese market could take place. ACKNOWLEDGEMENT This tesearch was supported by a grant from the Fishing Industry Research and Development Council. LITERATURE CITED ABARE, 1988, ‘Japanese agricultural policies: A time of change’. Policy Monograph No, 3. (AGPS: Canberra). 359p. COYLE, W.T. 1983. ‘Japan’s feed-livestock economy: Prospects for the 1980s, FAER-222". (Economic Research Service, US Departmentot Agriculture: Washington DC). DYCK, J.H. 1988. ‘Demand for meats in Japan, A review and update of elasticity estimates”. ERS 41y Staff Report, AGES 880525. (US Department of Agriculture: Washington DC). FAO (Food and Agriculture Organization of the United Nations), 1989. Fishery Statistics: Catches and Landings 1987. Vol. 63 (Rome) (and previous issues). FAO, 1990, INFOFISH Trade News (Kuala Lumpur). February (and previous issues), FERDOUSE., F. 1989. “Asian shrimp situation’. In INFOFISH Marketing Digest No.1/90. (FAQ, Kuala Lumput.) FISHERY JOURNAL 1989. Kuruma prawn culture in Japan. Fishery Journal 30: 3-7. (Yamaha Motor Co Lid, Shizuoka). JAPAN TARIFF ASSOCIATION, 1986. ‘Japan: Ex- ports and imports — Commodity by country’. January (and previous issues). JETRO (Japan External Trade Organisation), 1981, ‘Japanese fisheries and trade of fishery pro- ducts’, AG-S, March (Tokyo), 1987, Food Market in Japan, AG-20. (Tokyo). KESTER, A.Y. 1980, ‘Demand for fish in Japan and the westernizalion of the Japanese diet’. Paper presented lo the workshop on Trans-Pacific Ag- ticultural Trade, Resource Systems Institute, East-West Centre, Honolulu, Hawaii. 21-25 July. KINGSTON, A.G., SMITH, P.B, AND BEARE, 5. 1990, “Japanese seafood demand’. Paper pre- sented to the 34th Conference of Australian Ag- ricultural Economics Society, Brisbane, February 1990, MAFF (Ministry of Agriculture, Forestry and Fisher- ies, Japan) 1989. Statistical Yearbook of Ja- panese Agriculture, 1987-85 (and previous issues). (Tokyo). NATIONAL MARINE FISHERIES SERVICE, 1990. (NOAA, US Department of Commerce). ‘Foreign Fishery Information Release No, 90-5°. (and previous issues), RACKOWE, R., BRANSETTER, H., KING, D. AND KITSON, G., 1983. “The international market for shrimp’. ADB/FAO INFOFISH Market Re- port, Vol.3. (Kuala Lumpur). WILLIAMS, S.C., 1989, ‘The Japanese tuna markets: A fundamentalist’s view’. Association of Busi- ness Academics Working Paper Series, (Darling Downs Instilute of Advanced Education: Too- woomba). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 420 LETHAL EFFECTS OF ACIDIFIED SEAWATER ON PENAEUS MONODON AND THE INTERACTION OF SALINITY AND PH ON SUB-LETHAL EFFECTS Acidification commonly occurs in marine aquaculture $ys- tems when ponds are buill using acid-sulphaie soils contain- ing pyrite (Boyd, 1982). Low salinity'can accompany low pH in silvalions where run-off from acid-sulphate sediments in pond dykes enters ponds during heavy rains. Low pH can predispose prawns to disease and influence the loxicity of other toxins, eg. ammonia and aluminium. and in acid waters crustaceans may experience impaired tonic Tegulation (Morgan and McMahon, 1982). The aims of this Study were to estimate lethal and “minimum acceptable’ levels of low pH for Penaeus menodan in acidified water and to investigate the interactive effects of low pH and saliniy on prawn weight gain, moulting frequency, dry matter con- tent and haemolymph osmotic pressure, Sintic bioassays were conducted in 70 Laquaria with three replicate aquarta, each containing 1() prawns, for all low pH treatments. pH wis adjusted using 10 N HCT and all aquana were lightly aerated (100 mL min') to maintain. dissolved oxygen levels above 5.0 mg O2 L'. The average individual initial prawn weigh! was between 4 and 6g forall experiments, To estimate lethal levels a bioassay was run for 96 h wilh pH levels of 7.8, 7.0, 6.1, 5.1, 4.1, 3.8 and 3.0, Prawns survived well (>90%) at pH levels of 5.1 orabave. The 96 b LC59 (YS% cénfidence limits) estimated was 3.7 (3.4, 4.1). To assess sub-lethal effects a langer term (23 d) growlh experiment was conducted. Fight treaiments were established, six at 30 ppt with avetage pH yalues of 7.8, 7.3, 6.7, 6.1, 3.5 and 4.9 and two others al 15 ppt with average pH valugs af 7.8 and 5.5, The effects of treatment on survival tate were nob significant (P>0.05). Other performance data were analysed using single factor ANOVA (including all cigh| treatments) ar using two factor ANOVA (including data from treaments at pH levels 7.8 and 5.5 for both salinities, 15 und 30 ppl, Growth was depressed at pH < $5 at 30 ppt (Pefi.05) and although salinity did not affect growth (P>0.05) there was a significant pH/salinity interaction (P<0.05). The absence of a significant difference in growth between 15 and 30 ppt wits surprising as prawn farmers in Australia dnd overseas place great em- phasis on maintaining low salinity levels in P. monodon ponds. This does not appear necessary in terms of he phys- iological requirements of P, monudon although low salinity could influence other bioticcamponents of pond ecosystems, The ‘minimum acceptable” level was defined as. that level which reduced growth by 5% (the BCs) and was estimated, using two-phase linear regression analysis (Sedgwick, 19749), as being 5.9 pH units for P. menadon att salinity of AU ppl Moulting frequency was highest at pH4.9(30 ppt) and was inversely related to salinity, while the interaction was nol significant (P>0.05), The dry matter content was depressed at pH 4.9 (30 ppt) but unaffected by salinity or the interaction (P>0.05), Juvenile Penagus monedon arc elficten|osoregulatars iN (ho range 1510 30 ppt with an isosmotic pointof hetween 23 MEMOIRS OF THE QUEENSLAND MUSEUM and 25 ppt (Cawthorne er al. 1983), However, a reduction in internal osmolarity at reduced pH had been recorded for number of freshwater crustaceans and fish (Morgan and McMahon, 1982; Hobe era/,, 1953). To investigale whether chunges in osmotic pressure might explain the pH/sulinity interuction prawns were exposed to combinations of two. pH (7.8and §,6)and salinity (15 and 30 ppt) levels for three days, sufficient time for osmotic and ionic equilibrium to be reached. At the end of the experiment o¥matic pressures in ihe waler and prawn haemolymph were measured and the difference between these two values (Dop) calculated as an indication of osmoregulatory ability. At both salinities (15 and 30 ppt) haemolymph osmotic pressure was claser to ambient osmotic pressure at reduced pH (5.6), Both salinity (P<0.001) and pH (P<0.01) significantly reduced Dop, and there was no inleraction (P>0.05). Although the results of this experiment showed thal reduced pH lowered osmoregulatory ability in Penaeus monodon, they did not confirm the hy- pothesis that differences in osmoregulatory ability were fe- sponsible for the interaction between pH and sulinity on weight gain. The interactive effects of pH and sulinily on ionic regulation may warrant further investigation, The estimation of lethal and sublethal low pH Jovels fur P. monodon (3.8 and 5.9 pl units respectively) should assist prawn farmers with the management of acidic ponds. Literature Cited Boyd, CE. 1982, ‘Walter quality management for warm water fish culture’, Developments in Aquaculture and Fisheries Science, Vol. 9.( Elsevier: Amsterdam). 318p. Cawthorne, D.F., Beard, T,, Davenport, J. and Wickins, J.F. 1983, Responses of juvenile Penaeus monodon Fabri- clus 10 natural and artificial sea waters of low salinity. Aquaculture 32; 165-174, Hobe, H., Wilkes. P.R.H., Walker, R.L.. Wood, C.M, and McMahon, B.R, 1983, Acid-base balance, jonic status, and renal function in resting and acidexposed white suckers (Catostonns commercam). Canadian Journal of Zoology 61; 2660-2668. Morgan, D,O, and McMahon, B,R. 1982, Acid tolerance and effects of sublethal acid exposure an iono-regulation and acid-base status in two crayfish Procambarus clarki and Orconectes rusticus, Journal of Experimental Biology 97; 241-252. Sedswick, R.W. 1979, Influence of dietary protein and energy dn growth, food consumption, and food conver- sion efficiency in Penaeus mterguiensis De Man, Aqua- culture 16; 7-30. Geoff L. Allan and Greg 8, Maguire; NSW Agriculture and Fisheries, Brackish Water Fish Culture Research Starion, Salamander Bay, New South Wales 230), Australia, Present address, GBM. Key Centre for Teaching and Research inAquaculture, Tasmanian State Institute of Technology, Box 12/4, Launceston, Tasmanta 7250, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum ECONOMICS OF PRAWN FARMING IN AUSTRALIA 1,8. PETER HARDMAN, RHONDA TREADWELL, AND GREG MAGUIRE Hardman, J.R.P., Treadwell, R. and Maguire, G. 1991 09 U1: Economics of prawn farming in Australia, Memoirs of the Queensland Muscum 31: 421-434. Brisbane. ISSN 0079-8835. The current structure of the ptawn farming industry in Australia is defined, the costs of production are estimated and the importance of variation in yield, price, and cost of feed is determined. The importance of economies of size 1s also demonstrated. A census conducted in November 1 989 indicated thal, during 1988-89, there were 25 farms using 249 ha of ponds stocked with marine prawns on the east coast of Australia. Almost all farms were established within the past five years. Total production increased rapidly during the 1980s, and in 1958-89, 3511 of prawns (mainly Penaeus monodon) were produced, Casts of production for two separale geographical locations were estimated as follows. First, using a combination of the census data and the opinions of informed growers, characteristics of representative farms were specified. Costs were (hen assigned to these farms based on aclual grower experience. The results indicate thal relative to current world prices and prospects, Australian costs of production are high. Sensitivity analyses indicate that farm profitability is very sensitive to price, yield and farm size, Though feed is an important component of total costs (12-38%), it requires a very large reduction jn feed costs to significantly reduce the cost of production. The overriding conclusion from |he analysis is the high uncertainty of returns to prawn farming in Australia, Significant reductions in costs may be necessary, in view of the prospect of further price falls with the likely continued expansion of prawn aquaculture in South-East Asia. () Prawa farming, prawn aquaculture, profitability, costs of production, prawn farm economics. JR, Peter Hardman, Queensland Department of Primary Industries, Brisbane, Queens- land 4000, Australia; Rhonda Treadwell, Australian Bureau of Agricultural and Resource Economics, Canberra, Australian Capital Territory 2600, Australia; Greg Maguire, National Key Centre for Teaching and research in Aquaculture, University of Tasmania, Launceston, Tasmania 7250, Australia; 6 July, 1990. Marine prawn farming industries have ex- panded dramatically in many tropical countries, 50 that by 1989 production from farms accounted for an estimated 26% of total prawn production from fisheries and farms (Rosenberry, 1990). Traditionally, prawns have been farmed in Asia at low stocking densities and with minimal man- agement (less than I t/ha/y). However, tech- nology has allowed farmers ta increase stocking densities and production intensity to ‘semi-in- tensive’ (1-10 t/ha/y) and ‘intensive’ (more than 10 t/ha/y)(Wickins, 1976). Figures for the eight major prawn farming countries indicate that average yields per hectare are in the low to Semi-intensive range (Rosenberry, 1990). Many Asian countries have greatly increased produc- tion through expansion of total ponded area and intensification of farming methods (Handlcy and Moore, 1989). In contrast, prawn farming has remained a small industry in Japan, and has grown slowly in other developed countries such as the United States, where farms are located in warm-temperate areas (Lawrence and Huner, 1987). In Ausiralia a few unsuccessful prawn farms were established before 1980 (Heasman, 1984), Subsequently, several farms were constructed in the warm-lemperate area of northeastern New South Wales, stocked initially with school prawns (Metapenaeus macleayi) and later with leader prawns (Penaeus monodon). The latter ts the main species stocked in farms which have been established in tropical and warm-temperate areas on the east coast of Queensland (Maguire and Allan, in press). Production of Australian farmed prawns rose rapidly to 351 t in 1988/89, and expectations of farmers indicate much greater production in 1989/90 (Potter and Jones, 1990). Despite such progress, the major factors affecting the economic viability of the Australian industry have yet to be analysed. Several economic analyses have indicated that production costs for farmed prawns vary mark- edly between countries and with intensity of farming (Shang, 1983). Griffin et a/. (1986) con- cluded that prawn farming would be more prof- itable in a tropical country than in a Warm-temperate region, Though many economic assessments have been based on re- sults fram experimental rather than commercial prawn farming, those variables which are ex~ pected to most affect profitability have been identified. These include unpredictable en- vironmental factors (Griffin er al, L981), stock- ing strategies, including density (Pardy e¢ al,, 1983), species grown and polyculture (Huang er al., 1984), farm and pond size (Hanson ef ul, 1985), survival rate (Hollin and Griffin, 1986), use of passively heated nurseries (Juan ¢¢ al., 1988), and prawn sizes al stocking and harvest (McKee et ef, 1989). Most analyses have used deterministic models with single estimates for each variable, although stochastic modelling has been employed (Hansen ef al., 1985). This tech- nique uses a range of estimates for cach variable and provides a probability value for any particu- lar rate of return. The relevance of risk analysis to prawn farming, particularly in relation to in- creasing intensity of farming and suboptimal seasons, has also been recognised (Hatch et al., 1987). The collapse of the Taiwanese industry emphasises the importance of risk in prawn farming (Kwei, 1989). The emphasis in Australian prawn farming research has been on developing appropriate lechnology rather than on economic analyses, Heasman (1984) adapted a US farm model (Parker and Hayenga, 1979) and applied this to a hypothetical P, mwonedon farm in north Queensland, Hardy (1985) predicted good te- lurns for M. macléay: farms in northern New South Wales; Maguire and Leedow (1983) opti- mised stocking density and feed rate for that species using simple cash low models, Cook and Lightfoot (1987) predicted attractive returns lo farming P. monoden in north Queensland, based on model farms of 20 and 100 ha with a low stocking density (7 post larvae/m?). Yang (1987) adapted a Taiwanese model using Australian cost data and demonstrated the im- portance of stocking density and survival rate Lo economic returns, The approach taken in this study is as follows, First, the current and future market situation is reviewed, Next, the current structure of the prawn industry is determined by means of a census of prawn farmers, This in conjunction with Input from farmer groups is used as.a basis MEMOIRS OF THE QLEENSLAND MUSEUM for specitying the prawn tarm models, The mod- els are specified to allow comparison between the tropical and warm-temperate farming re- gions and between intensities of operation, This is followed by the derivation of the costs of production and rates of return to prawn farming in Australia based on the model prawn farms, Sensitivity testing of results and stochastic analysis of returns are included, not only to de- monstrate the risky nature of prawn farming at this stage but also to delineate the major varia- bles which affect profit. MARKET OUTLOOK To date, most sales of Australian farmed prawns haye been on the domestic market. The Australian prawn market closely follows trends in the international market, because over half of Australian production of wild caught prawns is exported (1988-89 exports being 1).5 kt; ABARE, 1989) and a similar volume is im- ported. Therefore the prices that Australian prawn farmers receive are largely sct in the in- ternational marketplace. That market is in- fluenced mainly by demand of the major importer, Japan, and the increasing world supply of cultured prawns, However, domestic prices do fluctuate with seasonal variations in supplies of wild caught prawns. Asian countries provide more than 80% of the world's supply of cultured prawns. Around half of Asian cultured prawn production is P. mono- don. 1n 1989 cultured prawn production by Asia reached S00 kt, almos} double that of 1987 (Rosenberry, 1990), This increase was laracly due to a rise in production af P. merodon by Thailand and fndonesia, China remains the largest producer of cultured prawns with 220 kt in 1989, bur, after recent large increases, produc- tian in China appears to be stabilising in 1990, reportedly due to disease problems (Anon, 1989), However, total Asian production of cul- tured prawns is expected to continue to expand and has been forecast to reach 800 kt by the year 2000 (Anon., 1958). Such an increase would continue to put downward pressure on prices, On the demand side, Japan is the major world importer of prawns and absorbs most of Australia’s exports of prawns (around 80%), Australia has very limited influence on the Ja- panese market, accounting for only aboul 5% by value of Japanese imports (Battaglene and King- ston, 1990), The major suppliers to the Japanese market are the Asiaa countries, Al the same time ECONOMICS OF PRAWN FARMING IN AUSTRALIA us supplies of prawn have increased, the growth in Japanese consumption of seafood has slowed, Although seafood's share of Japanese meat and seafood consumption has fallen from 74° in 1960 to 44% in 1985 (Kingston er al, 1990), prawn consumption did increase between 1984 und 1987 from 2.5 kg to 3 kg per person a year. However, the increased supply of prawns has exceeded the moderate merease in consumption. the result being 4 90% increase in cold Storage holdings since 1984 and falling prices on the Japanese market. If prices continue ta fall the quantity demanded is likely to rise. In the longer term there appears to be no relief from lower prices on the Japanese market, be- cause aquaculture production is expected to rise in Asia. Currently. Australian cultured prawns are mainly sold in Australia in bulk through wholesalers, and most production is of P. »ono- don. Thus, these sales would be in direct com- petition with the Asian cultured prawns, whether on the Australian or world markets. There are options which would enable Austialian pro- ducers to remain in this very competitive market. Prawn farmers may be able to time production to take advantage of seasonal fluctuations. and thus obtain higher prices by supplying the murket when alternative supplies are low. Efforis could be directed to supplying a reliable, high quality. well-presented product, bul this would raise marketing casts. Alternatively, management could be directed af producing larger prawns which command a premium in the marketplace. Although 25 g prawns are sold in Australia there is a limited export market for this small size. If production continues to expand, farmers may need to assess the option of larger prawns for the export market. Another option is to supply larger, fresh or live prawns to the restaurant (rade, which offers a significant premium over the supermarket or commodity market, particu- larly in Japan. In addition, farmers could switch production from the commonly produced P. monodon to the culture of higher-priced species such as P. japonicus or P. esctulentus, Such a switch in production would require developmen! of appropriate farming methods for these species. STRUCTURE OF THE PRAWN FARMING INDUSTRY IN AUSTRALIA The industry is small but expanding rapidly (Fig. 1). Gross value of production could reach $12 million in 1989-90 (O'Sullivan, 1990). Queensland has replaced New South Wales as the major producer of farmed prawns, mainly duc to the faster growth rates achievable in the higher water temperatures. Production in other sluies is negligible, ‘The majority of Australian farms are < 10 ha, with a few large farms responsible for most of jhe production. ‘The region between Townsville and Cuims contains 55% of Queensland's farms, while Mackay has 22% and Brisbane region 11%. ‘The greatest growth in farm area is occurring in the Townsville-to-Caimms region. The data in Table | indicate a rapid development Process in the prawn industry as evidenced by the following changes from 1988-89 to 1989-90: ¢ 023% inctease in total ponded area (all within Queensland): ® 4 60% increase in total stocked area; ® 4 25% increase in stocking density. The wide range between farms for most of the parameters used for measuring productivity (stock- ing rate, feed conversion ratio and yield) also indi- cules the developmental stage of the industry. In addition, the average feed conversion ratio of 2.265: 1 (feed weight to product weight) is signifi- cantly higher than overseas results which suggest thal long term averages of 1.8:1 or better can be achieved (Chen et al, 1989), Due to the current rapid development phase it js difficult to define a model or average prawn farm for analytical purposes. Regression analy- sis of farm parameters yielded two statistically significant relationships: as farm size increased, so did pond size (R? = 0.58, p <0,001) and the number of ponds (R2=0.59, p 0.05). That is, the industry has not developed sufficiently for a clear management pattern to emerge. With the assistance of prawn farmers, the repre- sentative model prawn farm was defined to be six 1 ha ponds as a family farm unit (Table 2). Al- (hough this is less than the industry average of 13 ha, the majority of farms are < 10 ha with a few very large farms of up to 95 ha. The 6 ha farm was considered to be representative of most farms, particularly in far north Queensland (FNQ), For comparative purposes the growers in the northem New South Wales/southeast Queensland region (NSW/SEQ) accepted the basic 6 x 1 ha prawn moucl as defined by FNQ growers. although farms tend to be larger in NSW/SEQ. The most obvious difference between the regions is the number of crops per vear, the NSW/SEQO region usually hav- 424 Production (Tora! Productian (fonnes) : 0 400 9200 ~ 11200 400" mcr 400 AZ 200 it 260 D : a Dec dun Cec Jun Dec aun dul i986 | 1987 1985 | wi | 1980 Date | — ap NSW Total | FIG, 1, Production from Australian prawn farms 1986-90, Source: Queensland Department of Pri- mary Industries, ABARE and Allan (1989a). Note: December 1989 to June 1990 — estimated produc- tions. ing only one crop a year while two crops a year was considered achievable in FNO. Farm operation intensity was defined in terms of stocking density. Two stocking densities, low and high, were accepted as representative, The model low stocking density (8 post larvae (PL)/m*) falls within the range reported for Australian prawn farms in 1988, of 5-15 PL/m? (Robertson, 1988). As isseen from Table 1, stocking density increased again between 1988/89 and 1989/90, The model high stocking density (25 PL/m2) was chosen to reflect this trend, The low stocking density model was considered by farmers to depict a learning stage rather than a long term farming proposition, For these low densities substantially larger ponds are more appropriate (Scura, 1987) Tn the model farms, both survival rates and growth rates declined with increasing stocking density (Table 2). Accordingly, for the lower stocking density the average prawn size at harvest was set higher than for the high stocking density. This relationship between growth and density accords with experimental re- sults reported by Allan and Maguire (1988). How- ever, they concluded that survival rates were not affected by stocking density in their experimental ponds. This indicates that yields may be improved in the future as farmers gain more experience in feeding regimes and pond management. COSTS OF PRODUCTION Costs were eslimated for the 6 x J ha farm model by fatmers who attended group assess- ment meetings held in far north Queensland and northern New South Wales, with additional in- formation from equipment suppliers. MEMOIRS OF THE QUEENSLAND MUSEUM Feed is by far the largest component of annual operating costs, accounting for 57% for the high density model farm in far north Queensland (Table 3). Prawn fry is the other major operating cost, comprising about 20% for the low density farms and 23% for the high density farms. The major costs of establishment are land and carthworks (Table 4), To achieve six 1 ha ponds a total land area of 12 ha would be required to allow provision of sheds, roadways and chan- nels, The cost of surveying and constructing ponds varies markedly ($12 000-40 000/ha), de- pending principally on topography, soil type, wall slope and pond configuration, For the model farm of six | ha ponds a flat site with a suitable clay base was assumed and a corresponding cost of $20 000/ha used in the analyses, The cost of a pumping system also varies substantially, de- pending on the level of water exchange required, tidal limitations and the desired speed of filling. IU is feasible that farmers could install cheaper pumping systems than those listed in Table 4. The total establishment cost of around $0.5 million including land purchase (Tables 5 and 6) constitutes a substantial obstacle. However, in the case of sugar cane farmers who enter prawn farming, these capital costs may be considerably reduced through the use of existing surplus land, equipment and possibly underutilised labour. Table 4 outlines costs for a farm of twenty 1 ha ponds, These figures are used below in an inves- tigation of economies of scale. Total production costs for the low stocking density mode] are shown in Table 5, In the NSW/SEQ region, the total cost of production, at $15,67/kg, is too high given current market prices and outlook. In far north Queensland, with two crops a year, the production cost is much lower, at $9.38/kg. For the high density farms (Table 6) the difference between regions is much less, with FNO costs of production $1.54 lower than those in NSW/SEQ, These costs are very close to current market prices. Jn carly 1990 the farm gate price for 25 g prawns varied in the tange S8-l2/kg, with an average price of $10/kg. Prices increase with the size of prawn, and 30 g prawns fetched about $2/kg mare. Therefore, in the analyses prices were varied according to the size of prawn produced (Ta- hies 2, 5 and 6). Given the possibility of further price falls in ihe future, itis important to examine the oppor- tunities for reducing costs. The cost of feed may he lowered in two ways; by a drop in the cost of feed per tanne, or by a decrease in the feed ECONOMICS OF PRAWN FARMING IN AUSTRALIA 425 TABLE 1. Prawn Farming Industry: census results. Total | Average Feed Average yield number | area of Stocked Stocking | conversion Total per unit Variable of ponds| ponds area density ratio production stocked area(a) ha 1988-89 Total for all farms s 248.55 Range for all farms 0.45-50 Average for all farms : 9.94 1989-90 Total for all farms 1130(p) Range for all farms 4-280(p) 1-13.5(p) Average for all farms ~ 37.67(p) 2,85(p) Source: Telephone census, November 1989. of all known prawn farmers in Queensland and New South Wales (25 farms). (a) Average yields per stocked area in 1988/89 were mainly based on one crop per year. Only 3 out of 25 farmers double cropped. Average yields per stocked area in 1989/90 are higher than 1988/89 in part because 14 out of 30 farmers indicated their intention to double crop. nc= data not collected. p= projected by Queensland Department of Primary Industries, ABARE and Allan (1989a). PL= post larvae (prawn fry). TABLE 2. Description of model 6 x 1 ha pond prawn farms. i Low stocking density High stocking density tem unis | rNo | NSwisto NSWISEQ [Aeration | | to | ro ves ves Numberoferopsyear | no | 2 | st | et Averagesizeotprawns |e | 27s | 30 | ts Ts Stocking rate ~ average - range Survival rate - average - Tange Yield - average - range 3.04.3 . t/6 wT Source: Group assessment meetings, South Johnstone. Queensland, and Palmers Island, New South Wales, March 1990. FNOQ, Far north Queensland. NSW/SEQ. New South Wales and south-east Queensland. 426 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 3. Annual operating costs: 6 x 1 ha pond farm model. Low Stocking High Stocking Densit Number of crops/year : 2 Total production 18.48 Feed conversion ratio 1.8:1 Feed consumed 33.26 Total feed cost @ $1500/t 49 896 19 200 8 000 10 000 3 000 8 000 3 000 Cost of prawn fry @ 2c Casual labour Electricity Fertiliser Repairs & maintenance Miscellaneous 1 2 7.2 45 1.3:1 2.25:1 9.36 101.25 14 040 151 875 9 600 60 000 8 000 13 000 3 000 22 000 1 500 5 000 8 000 10 000 3 000 4000 Source: Group assessment meetings: for FNQ, South Johnstone Research Station, Queensland, and for NSW/SEQ, Palmers Island, New South Wales, conversion ratio. It is evident from the sensitivity tests that it would require a very large saving in feed costs to effect a significant reduction in production costs (Table 7). For example, to ef- fect a saving of about 50c/kg in the total cost of production requires a decrease in feed cost of between 15% (for the FNQ high intensity farm) and 25% (for the low intensity farm in the NSW/SEOQ region). Such large cost savings may be difficult to achieve. However, reductions in feed conversion ratios can be effected through more appropriate feed rates (Allan, 1989b). Yields per hectare may be raised by either increasing the stocking density and/or improving the survival and/or growth rates. The sensitivity tests reported here were based on increasing the stocking density, with feed conversion ratios held constant and no change in survival or growth rates. (The savings in costs would be larger if the same yield increase were achieved at least partly by improved survival and/or growth rates). To achieve a saving of around $1/kg in the total cost of production would re- quire an increase in yield of between 8% (for the low density NSW/SEQ farm) and about 30% (for the high density FNQ farm) (Table 8). This latter increase would imply a yield from two crops totalling 9.8 t/ha/y. Such an increase may be achievable in the future if improved pond man- agement allows higher stocking densities as well as better survival and growth rates. Economies of size may offer a further option for reducing the unit cost of production. A larger farm of twenty 1 ha ponds with high stocking density was analysed (Table 9). The unit costs of production for the larger farm model are almost 20% lower than for the 6 x 1 ha farm model. This result is not surprising, given that overhead costs comprise 33-46% of total costs for the high density 6 x 1 ha farms (Table 6). Similar size economies are likely for low density farms, for which overhead costs account for an even greater share of total costs. RATES OF RETURN TO PRAWN FARMING The previous sections have shown that costs and yields in prawn farming in Australia vary with region and stocking density. Account must also be taken of the high degree of uncertainty surrounding prices, costs and yields for similar farms within the same region. A rate of return based only on the most likely estimates does not fully reflect the nature of returns to prawn farming. Sensitivity testing over the range of possible values for the uncertain parameters would be- come unwieldy and difficult to interpret. The alternative approach used in this paper is stoch- astic investment analysis. This approach is based on the stochastic analysis of returns to new hor- ticultural crops by Treadwell and Woffenden (1984). The analysis uses the estimated range for each uncertain parameter — that is, for costs, market prices and the parameters set out in Table 2. For each simulation, a value (or a fluctuating time series) was randomly generated for each parame- ECONOMICS OF PRAWN FARMING IN AUSTRALIA 427 TABLE 4. Capital costs for model prawn farms with 1 ha ponds, for both regions. Total value Years High when density purchased J 120 000(a) 3.000 4000 2500 10 360 24 000 Earthworks (ponds & channels) Pump(s) Motor(s) Belts, pulleys, pump base, etc. Pump shed, valves, filters Pipes. gates, screens, boards Electric power supply 40.000 Generator (standby) 5000 Rotary hoe - Spike tooth harrows ooo Slasher 1500 Bucket - Blade 1000 Fertiliser spreader 2500 Farm truck (2nd hand) 20 000 Tractor (2nd hand) 10.000 Motorbike _ Blower pipe (feed) ano Aeration units _ Retrig. plant, esky, bins, etc S000 Ice machine (1 t/day) 13 uuu Prawn weighing scales Sti) Harvest equip (nets/cages) 1500 Prawn handling area & equip. (washes, trays, loader) Farm shed Tools Test kits Bout (2nd hand) Office equipment Miscellaneous 120 000(a) 30.000 & 000 5 000 10 360 24 000 80 000 Heo 3.000 1000 1s00 1000 1000 2S 20 000 10.000 2000 TOu0 33.000 14.000 13.000 1000 7500 300 000(b) 0 40 668 0,5,10,15 40 667 0,5,10,15 6665 0,3,6,9,12,15,18 15 200 0 80 000 0 200 000 0 20.000 0,10 5000 0,10 2000 0,10 2000 0,10 5000 0,10 1500 0,10 2500 0,10 20 000 0,10 15 000 0,10 2000 0,5,10,15 1000 0.3,6,9,12,15,18 135.000 0,5.10,15 22.000 iu 13 000 111 2500 1.4.7,10,13,16,19 4.000 1,4,7.10,13,16,19 8000 10.000 2 000 2000 1 S500 3.000 2000 10.000 15.000 4000 4500 1500 3.000 3.000 10.000 1,11 25 000 0 10 000 0,5,10,15 4500 0,3,6,9,12,15,18 2500 0,10 3 000 0,5,10,15 3.000 0.5,10,15 (a) Plus purchase of 12 ha of land, at $6000/ha in FNQ region and $4000/ha in NSW/SEQ, (b) Plus purchase of 35 ha of land at same prices as in (a). ter from its observed distribution. Each such set of parameter values was used to calculate a specific stream of costs and returns, from which the internal rate of return was derived. This procedure was repeated a large number of times (700), to generate a set of internal rates of return (IRR). These were then ranked and their cumulative probability func- tion was calculated. This function gives the prob- ability of the internal rate of return being less than any particular level. The advantage of this stochastic approach 1s that it not only produces the expected or mean internal rate or return but also indicates the effect of uncertainty by providing the range of internal rates of return with their corresponding prob- abilities of occurrence. This procedure avoids the need for sensitivity analysis on individual parameters, as the overall] uncertainty is reflected in the probability distribution of internal rates of return. However, individual sensitivity tests can still be undertaken to show the specific effect of variation in a particular parameter. The stochastic investment analysis was con- ducted for the four prawn farm models using the 428 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 5. Cost of production: low stocking density system, | PHYSICAL DESCRIPTION | DESCRIPTION Number of ponds Area/pond (ha) Total farm area (ha) Production/crop (t/ha) Number of crops/year (no.) Total production of prawns (1/y) Feed conversion ratio Feed consumed (t/y) Capital costs of establishment(a)(3$) FINANCIAL DESCRIPTION Gross income Operating costs Overhead costs Ratio of overhead to total costs (%) Return to management estimated range in parameter values as sct oul in previous sections. The analysis was on a pre-tax basis, using private costs and benefits, and was conducted over 20 years, the estimated life of ponds. The analysis was based on the following assumptions. Costs do not change relative to prices during the period of analysis — that is, constant (1989-90) values are used. ® ‘The interest rate on money borrowed equals the internal rate of return. e During the period of analysis, no technical changes occur which result in major increases in yields or substantial changes in the relation- ship between yields and costs. e There is no correlation between prices, yields 203 280 — Feed 49 896 2.70 14.040 1,95 — Casual labour 8 000 0.43 8000 1.41 — Electricity 10.000 0.54 3.000 0.42 — Prawn fry 19 200 1.04 9600 1.33 — Fertiliser 3.000 0.16 1500 0.21 — Repairs & maintenance 8 000 0.43 8 000 1.11 — Miscellaneous 3.000 0.16 3000 0.42 Total operating costs 101 096 47.140 — Depreciation & interest(b) 40214 2.18 38 774 5.39 — Allow. for farmer's labour 26 080 Al 20 872 2.90 — Permanent hired labour 0 0 0 0 — Administrative costs 6000 0.32 6000 0.83 Total overhead costs 72304 3.91 65 646 Total costs 173 400 9.38 112 786 29 BRO (a) Derived from Table 4 plus land purchase. (b) Assuming real rate of interest 6%. 86 400 +26 386 and costs (as Australian prawn farms supply only a minor segment of the market). e Full production is possible from the first year of operation. e The farm is well managed and located on a suitable site with ready access to water. There are no disasters such as would cause total loss of crop. The effects of the last two assumptions, in par- ticular, is that the average internal rates of return generated will be higher than the industry average. The results will reflect more closely the results of more experienced farmers with suitable sites, rather than the average of a new and expanding industry. The cumulative probability distributions for the four prawn model farms are summarised in Table ECONOMICS OF PRAWN FARMING IN AUSTRALIA 429 TABLE 6, Costs of production: high stocking densily system. Item PHYSICAL DESCRIPTION Number of ponds Area/pond (ha) Total farm area (ha) Production/crop (t/ha) Number of crops/year (no.) Total production of prawns (t/¥) Feed conversion ratio Feed consumed (t/v) Capital costs of establishment(a)($) FINANCIAL DESCRIPTION Grass income Operating casts — Feed — Casual labour — Electricity — Prawn fry — Fertiliser — Repairs & maintenance — Miscellaneous Total operating costs Overhead costs — Depreciation & interest(b) — Allow, for farmer's labour — Permanent hired labour — Administration costs Total overhead costs Total cost 450 000 151 875 13.000 22 000 60 000 3 000 10.000 4000 265 875 61 663 26 090 37 500(c) 6 000 131 253 397 128 NSW/SEQ tw et toa ayo bo oe 19 —-W— wane oO 101.25 507 860 = o wn 126 250 60 223 20 872 20 000(d) 6 000 107 095 10. The highest average internal rate of return is that for the high density farm in north Queens- land, followed closely by the low density farm in north Queensland. The uncertainty of the re- turns is similar for these two types of operation, as is Shown by their respective cumulative prob- ability functions (Fig. 2). As noted above, the low stocking density model was considered to be a developmental stage and not a long term prop- osition. This is certainly true for the NSW/SEQ tegion, where the low density model did not generate positive returns, The difference in returns between the two re- gions is notable, with the internal rates of return for NSW/SEQ falling well below those for FNQ. The higher profitability of the tropical region Tee GLO mun Oanayp FIG. 2. Cumulative probability of IRR: 6 ha prawn farm models. 430 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 7. Estimated costs of production resulting from decreases in feed cost. FNQ Skg 9.38 corresponds with worldwide experience (Griffin et al., 1986). The sensitivity of returns to the number of crops indicates a need to research the necessary requirements (in addition to climate) which facilitate two crops a year. Few farmers produced two crops in 1988/89. Options worthy of consideration include three crops in two years in the FNQ region — with perhaps a larger sized prawn being harvested than is obtainable at two crops a year — or, in the NSW/SEQ region. the production of one prawn crop per year while using the same ponds for other aquacultural pro- ducts such as oysters in the cooler months (Ma- guire ert al., 1981). A significant difference between the regions in practice is that prawn farms in NSW/SEQ tend to be larger than those in FNQ, and larger than the 6 x 1 ha pond operation used in this analysis. Therefore, a larger farm of twenty 1 ha ponds was simulated. The expected internal rate of return for the larger farm is more than double that for the small farm. This indicates the existence of significant economies of size in prawn farm- ing. (There may be similar economies in relation to pond size, but that question would require further research which was not possible in this study.) As in the previous section on costs, the sensi- Reduction in feed cost | rNQ. | Nswsco Sky 15.67 15.47 15.08 FNOQ Sikg 8.83 8.49 NSW/SEQ S/kg 10.37 10.10 tivities of rates of return to a 10% drop in feed costs and a 10% increase in yields were analysed, and the results are summarised in Table 10. Again, the 10% drop in feed costs has a smaller effect on returns than a 10% increase in yields (Fig. 3). For example, for the low density FNOQ farm the average rate of return rose by 26% in Tesponse to the 10% increase in yield but rose only by 9% given a 10% drop in feed cost. Another very uncertain factor is the market outlook. Rather than prices remaining constant relative to costs it is probable that relative prices may fall, in view of the continuing expansion of prawn aquaculture, particularly in South-east Asia. If prices were to fall continuously at an annual rate of 1.5%, returns to prawn farming would be expected to fall substantially. For in- stance, mean returns to the high density NSW/SEQ 6 x 1 ha farm model fell below zero (Table 10). For the twenty 1 ha NSW/SEQ farm model the mean return was less than half that derived with constant prices. However, in the face of a continual price decline prawn farmers would be likely to improve yields and/or reduce costs to offset the effects of the price fall, as has occurred in other primary production activities. Overall, the simulated distribution of returns to prawn farming indicates that it is a very un- TABLE 8. Estimated costs of production resulting from an increase in yield. Yield increase 8.29 Low density svstem FNO NSW/SEO FNO S/kg Sikg S/kg S/kg a Se ee eee 15.67 8.83 10.37 Pp tOTCC“‘RSC‘CW SOTTO] 8S 9.78 8.64 8.44 13.59 13.17 2): High density system 8.00 ECONOMICS OF PRAWN FARMING IN AUSTRALIA 431 TABLE 9. Costs of production for 20 x 1 ha farm with high stocking density. NSW/SEQ Number of ponds Area/pond ha Total farm area ha Production/crop t/ha Number of crops/year no. Total production of prawns t/y Feed conversion ratios Feed consumed t/y Capital costs of establishment(a) $ FINANCIAL DESCRIPTION Gross income 1500 000 Operating costs — Feed — Casual labour — Electricity — Prawn fry — Fertiliser —Repairs & maintenance — Miscellaneous Total operating costs Overhead costs — Depreciation & interest(b) — Allow. for farmer's labour — Permanent hired labour(c) — Administration costs Total overhead costs Tolal costs 306 250 45 000 73 300 200.000 16 700 15 000 6 000 862 250 14] 937 26 090 75 000 11.000 254 027 L116 277 Ratio of overhead to total costs (%) Return to management oY Sw We OMUmNK Oo pry way Yu ty Wen aAneS 202 500 22 500 40 000 100 000 5000 12.000 6 000 388 000 137 737 26 090 75.000 11 000 249 827 (a) Derived from Table 4 plus land purchase. (h) Assuming real rate of interest of 6%. (c) 3 full-time people. IY iret Tree —— Hormel baw tae waa = gg Yen FIG. 3. Cumulative probability of IRR: far north Queensland 6 ha high density prawn farm model. certain business. For example, the average inter- nal rates of return on the two modelled 6 ha North Queensland farms are 16.8% and 13.8%, but there is a 25% chance that the return could fall below those averages by overa third. In addition, variations in prices, yields, feed costs and the size of farm have very marked effects on returns. CONCLUSIONS The principal aim of this study was to provide industry statistics and an analysis of the econom- ics of prawn farming to assist industry, govern- ment and researchers to determine future directions. In 1989-90 Australian production of cultured prawns came from 30 farmers with al- MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 10. Internal rates of return to prawn farming: stochastic simulations. Farm model* FNQ NSW/SEQ FNQ NSW/SEQ Feed costs reduced by 10 percent Low density: High density: Low density: FNQ NSW/SEQ High density: FNQ NSW/SEQ Yields increased by 10 percent Low densily: FNQ NSW/SEQ High density: © FNO NSW/SEQ Prawn prices deflated by 1.5% a year Low density; © FNOQ NSW/SEQ High density: FNQ NSW/SEQ 20x J ha pond farm, high density Constant prices: FNQ NSW/SEQ Prawn prices deflated by 1.5% a year: FNQ NSW/SEQ most 400 ha of ponds along the east coast. The industry is undergoing rapid change as it ex- pands and develops beyond the infant stage and a clear management pattern has not yet emerged. The economic analyses were based on a6 x 1 ha model prawn farm with two intensities of operations in two regions, far north Queensland and New South Wales/south-east Queensland. Given the risks and lead time associated with developing a new industry, the establishment costs of about $0.5 million per farm present a large obstacle. Overhead costs are 33-46% of total costs for the high intensity farm, so itis not surprising that there are substantial economics in operating a larger farm as indicated by the results from a 20 ha model. The costs of production and returns for both intensities of operation are sim- * 6x 1 ha except where otherwise indicated. — Negative. 75% probability that IRR is more than: 75% probability that IRR is less than: ilar in far north Queensland, but there are marked differences between the two regions which re- flect the climatic constraint of being able to produce only one crop per year in the more southerly region. The overriding conclusion to be drawn from the analysis is the high uncertainty of returns and tisk involved in prawn farming. At current prices for the product, returns to prawn farming in Australia are adequate, but its profitability 1s very sensitive to price. With the prospect of further price falls in the future, returns to Australian prawn farmers may be reduced sub- stantially unless savings in production costs can be achieved and/or production is switched to higher priced products. The effect on profitabil- ity of production of higher priced products — ECONOMICS OF PRAWN FARMING TN AUSTRALIA 43 such as higher priced species, live prawns or larger prawns — would require further research (han was possible in this study. As the industry is still in a developmental stage it may well be possible to effect significant cost savings through increasing yields. The analysis showed thal returns were more responsive to changes in yield than to reductions in feed costs. Also, unit costs may be substantially reduced and returns raised by increasing the size of the farm, ACKNOWLEDGEMENTS The authors with to acknowledge the support of the Fishing Industry Research and Develop- ment Council, which provided the research grant to ABARE that enabled Ms Treadwell and Dr Maguite to participate in this study. The following people are acknowledged for their contribution in the compilation of this re- port. Mr Tim Jones, biologist: formerly Fisheries Branch, Queensland Department of Primary In- dustries (QDPI). Dr Noel Gillespic, Project Manager, Bribie Island Aquaculture Centre, QDPI. Mr Noel Moore. Northern Queensland Manager, Fisheries Branch, QDPI, All 30 prawn farmers who responded to the telephone census. 22 prawn farmers who attended the group assess- ment meetings at South Johnston Research Sta- tion, Queensland, and Palmers Island, New South Wales, Mr Barry Smith, Defiance Re- search P/L, Toowoomba, Queensland. 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(Aquaculture Digest: San Diego, CA). 28p. SCURA, E.D. 1987. Review of world prawn farming. 1-12. In P. Sloane (ed.) ‘Prawn farming for profit — Potential for success’. (SCP Fisheries Consultants Australia P/L: Sydney), SHANG, Y.C. 1983, The economics of marine shrimp farming: a survey. 7~19, In G.L, Rogers, R. Day and A. Lim (eds) ‘Proceedings First Inter- national Conference on warm water aquaculture — Crustacea’. (Brigham Young University, Hawaii Campus: Laie, Hi). TREADWELL, R.F. AND WOFFENDEN, K. 1984. “Estimating returns from growing some new horticultural crops’, Paper presented to the 28th Annual Conference of the Australian Agricul- tural Economics Society, University of Sydney, 7-9 February. 13p. WICKINS, J.F., 1976. Prawn biology and culture. Annual Review Oceanography Marine Biology, 14: 435-507, YANG, J., 1987. Cost analysis of a prawn grow-out farm. Append. 10-15. In P.Sloane (ed.) “Prawn farming for profit — Potential forsuccess*, (SCP Fisheries Consultants Australia P/L: Sydney). MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum WORLD SHRIMP PRODUCTION SJEF VAN EYS Van Eys, S. 1991 09 01: World shrimp production, Memoirs of the Queensland Museum 31: 435-446. Brisbane. ISSN 0079-8835. Total world shrimp supply at the end of the 1990's is expected ta exceed 3 x 10° ¢. In 1989, 103 counties were involved in shrimp production; 10 of the top 16 counties were Asian and together produced more than half the worlds production. Tropical shrimps represent 90% of the world shrimp market. The production f from wild harvest fishing operations is fully exploited and will remain stalic al ca. 1.5 x 10°. Shrimp production from aquaculture has shown a dramatic increase over the last 10 years due in part to the development of hatchery techniques and the production of hatchery reared post-larvae. The culture is centred on tropical prawns (Penaeus species) grown in Southeas| Asia, Latin America has the potential to be a large producer of aquaculture product bul its development is hampered by lack of technical expertise and capital. ( Shrimp, prawn, aquaculture, wild harvest, fisheries, world. Sjef van Eys, Infopesca, Adpo,. 641894, El Darado, Panama, RP; 16 January, 1991. Shrimp are found in all regions of the world in fresh, coastal and oceanic waters. Many species have high value and form the basis of major commercial wild harvest fisheries and culture industries. There are five major market groups of shrimp: }. Warmwater or tropical marine species. They mature rapidly and often grow to a large Size, 2. Coldwater marine species. Inhabit tem- perate waters, grow slowly and are generally small. 3. Freshwater species. Live in inland water bodies and rivers, mostly in the tropics and often grow to a very large size. 4, Deep sea shrimp, Grow and reproduce slowly and are of limited commercial valuc. 5, Krill, Landings of Antartic krill (Euphau- sia superba) topped 500,000 t in 1989. The biomass is estimated at 100 x10° t, New uses of knill by-products and increasing use for hu- man consumption (e.g, in Japan) should en- courage more attention to this species. The world supply of shrimp increased rapidly from 1.09 x10® tin 1970 to 1,63x10° tin 1977 (live weight). Supply of shrimps remained relatively stable until 1981, when landings quickly accel- erated to reach about 2.5 x10° t by 1989. According to FAO statistics in 1989, 103 coun- tries were involved in the production of shrimp, both wild and cultured. Ten of the top 16 producing countries in 1988 were Asian and together pra- duced 1.6 x10° t (live weight), equivalent to 65% of the total world production (Table 1). For 1989 this should increase further as a result of con- (tinued strong cultured shrimp output. Estimates reveal that 90% of the total world market supply consists of tropical shrimp. Coldwater shrimp landings have shown con- siderable fluctuations, mainly due to incompat- ible fishing efforts and the natural characteristics of the resource (slow growth and rate of re- covery). This has led to major collapses: United States Pacific fishery in early 1980's, Norway TABLE |. Sources of shrimp production (x107 t), by principal country. 1980 1985 184 250 136 162 133 1986 1987 1988 457 584 197 237 187 202 165 15] 150 *150 176 «(111 Country China India Indonesia USA Thailand Taiwan Ecuador ; : 79 «BI Philippines 2 68 80 Mexico 84 = 73 Malaysia *73° «473 Greenland 64 «65 Braz)! 53 55 S88 Vietnam : 56 *56 Rep, of Karea = 5 45 = 50 Japan 5 48 “48 Norway 5 42 42 Australia : Z 20 20 World Production 1,781 2,298 2.426 2,605 2,763 *Estimated. 436 TABLE 2. Catches of coldwater shrimps (x10° t), by selected countries. 1980 1985 35.8 52.4 45.3 91.2 44.7 19.5 Canada 12.0 14.1 Iceland 10.0 24.9 Denmark 7.0 10.3 USSR 12.1 33.4 12.0 FRGermany 15.4 17.7 17.0 14.3 Argentina 0.8 #103 28 *2.8 Total 183.1 273.8 256.3 254.5 1987 64.4 42.2 37.8 25.4 38.6 16.1 Countr 1988 65.1 41.7 36.7 34.5 29.6 *16.1 13.7 Greenland Norway USA *Estimated. and Argentina in 1986. Most of the fisheries appear to have recovered (Table 2) and fishing is now strictly regulated. No major increases are expected for this group and aquaculture has limited potential. Freshwater shrimp output has remained stable. Initially, demand suffered as marine shrimp supplies increased. However demand is now increasing, due mainly to market demand for large shrimp. Smaller shrimpare used as market subsitutes for small marine shrimp e.g. Crangon spp. The growth in production of cultured shrimp (mainly Penaeus species) has been spectacular. In tropical coastal countries, using simple earth ponds, tidal or pumped water supplies, local or hatchery-reared seed, and simple fertilisation or feeding, a marketable crop of 15—30g shrimp can be reared in as little as 3 or 4 months. Annual yields range from 200 to 500 kg ha’ in simple extensive tidal ponds, to upwards of 10 t ha in modern intensive systems using formulated feeds, aeration and regular water exchange. MEMOIRS OF THE QUEENSLAND MUSEUM In production terms, the results of the blue revolution have been impressive. In 1981, cul- tured shrimp accounted for only 2.1% of total world shrimp harvest, while in 1989 this was estimated to have reached 27% with output of 560,000 t, corresponding to a farm-gate market value of about US$2.5 billion. Much of this originates from the developing world, particu- larly Southeast Asia and Latin America. As aresult of this development, rural coastal land of limited agricultural potential, has acquired a new status. There are also new prospects for income and employment; traditional brackish water fishpond operators have a new source of income; fishing communities can get involved in catching seed shrimp and broodstock; farm and hatcheries in tural areas offer local employment and training for young people. There are new services industries; in Southeast Asia backyard hatcheries have created excellent opportunities for small family-based bus- iness, whose earnings in turn give stimulus to local economies. These spin-off benefits can be simply staggering, which is probably a major reason why governments continue to be keen to promote this activity despite the current problems on the market- ing level. The producing countries are discussed on a regional basis below(including the smaller pro- ducers, some of which are major suppliers to select markets) , followed by an overview of the international trade for shrimp and prospects for future markets. EUROPE CAPTURE FISHERIES European Economic Community (EEC)’s dom- TABLE 3. Cold water shrimp production (x10° t) from selected countries in the European Region. Countr 1982 1983 1984 Pandalus borealis Norwa Icelan Greenland Denmark Others Total -_— a Ns ANNSwL- m Une JD OF Crangon crangon Germany Netherlands 1985 1986 1987 1988 WORLD SHRIMP PRODUCTION aay TABLE 4. Shrimp production (10° t) by countries within the European Economic Community. Countr 1982 1983 1984 Germany Spain Denmark Netherlands Ttaly Greece Ireland Belgium Portugal UK France Total “Estimated. estic production of shrimp increased from 60,000 t in 1981 to over 80,000 t in 1987 (Table 4). Most of this production is. made up of Crangon crangon, a small coldwater species caught by the fleets of Germany and the Netherlands (Table 3). Spain and Italy contribute c. 15,000 t of Para- penaeus longirostris, a warmwater species. From the early 1970°s European and North Atlantic catches of Pandalus borealis increased steadily from 30,000 t to a peak of 192,000 t in 1985. Since then the landings have declined, due to smaller catches by Norway, to 163,000 t in 1988 (Table 3). Norway used to account for roughly half of the world's Pan. borealis land- ings, but Greenland with 72,500 t in 1988 has become the leader, Iceland's catch of this species. tripled between 1983 and 1986, However stock started to decline due to overfishing.Quotas were introduced with the result that catches dropped from 39,000 tin 1987 to 30,000 t in 1988, Spanish shrimp production reached a peak of 25,000 t in 1985, due to record catches of Par. longirosiris. Landings then declined to 19,000 t where they have remained. Coldwater shrimp represent a very small proportion of the Spanish shrimp catch. Domestic supply accounts for ap- proximatelty half of the total shrimp consump- tion in Spain. UNITED STATES OF AMERICA CAPTURE FISHERIES The United States domestic shrimp production Was 331 x 10°lbs (150,000 t) in 1988 (Table 5) and comprised about 7% of the world’s supply. 1985 1986 1987 United States total shrimp landings increased from 192 x 10°lbs (73,000 t) in 1950 to a record level of 467 x 10°lbs (216,000 t) in 1977, the result of high landings in the Gulf of Mexico fishery and a record harvest of cold water shrimps production in subsequent years, United States total landings averaged 329 x 10°lbs (150,000 t) during the period 1980-88, as com- pared to an average of 391 x 10°lbs (178,000 t) for the period 1971-79. However the total deflated ex-vessel value of shrimp has shown an overall rising trend during the period 1971-88. Landings of coldwater shrimp increased rapidly up to 1977, largely as the result of heavy production in Oregon and Alaska, The number of trawlers in the Pacific fishery has since de- clined. A combination of declining shrimp stocks and reduced prices caused by imports of coldwater shrimp from Norway led to a major drop in Pacific landings during the 1985-85 period. In addition, many production areas in Alaska were closed to permit the resource to recover. Since 1985 catches have improved in Washington, Oregon and California, but a high incidence of small-size shrimp at times has re- sulted in lower ex-vessel prices. Alaskan stocks show no signs of recovery. The tropical shrimp fishery has not undergone major fluctuations in recent years. This fishery averaged 253 x10%Ibs y~ (115,000 t y") during the period 1980-88. Since all major United States shrimping grounds are already exploited to a maximum, the total supply from the warm- water capture fisheries is not expected to in- crease in the future. MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 5, Shrimp Production (x10° Ibs), by regions, in the United States of America, Mid Atlantic South Atlantic 31,200 25,248 24,557 27.09] 24,926 26.108 18.021 20,138 7 32,295 3 32,996 7 16,514 5 25,580 26,615 )9,179 27,970 23,120 24,536 24,461 20,739 7,515 11.655 2,254 540 y 3,469 7,114 9,254 10,328 There has been a steady increase in the number of vessels in the fishery for tropical shrimp in the past 10 years. Between 1975 and 1987 the num- ber of shrimp vessels (fishing craft over 5 { gross) in the Gulf of Mexico rose from 3,743 to an estimated 5,800. At the same time, shrimp ves- sels have become large and more sophisticated. The Gulf of Mexico shrimp trawlers re- portedly operated profitably during the period 1971-80. This trend stimulated the continued expansion in the fleet, despite periodic down- turns in shrimp prices and generally rising operating costs. Historically the Gulf of Mex- ico shrimp fishery has displayed symptoms of overcapitalisation, but regulatory efforts to limit access have generally not been accept- able to the United States industry, CULTURE Total cultured tropical shrimp production was c.1,100 t in 1988. Climate conditions, high labour costs and shortage of suitable land have generally resulted in United States investors gomg abroard. Initially this was Latin America. Currently the focus of United States investors is Southeast Asia (Thailand, Philippines and Indonesia). MIDDLE EAST AND NORTH AFRICA CAPTURE FISHERIES Total shrimp production in Middle East and Pacific 227,367 228,941 182,206 186,208 170,083 210,167 265,158 248,327 206,564 208,280 268,190 209,926 198,457 254,254 262,908 304,051 107,790 108,811 152,220 142,759 149,067 167,865 192,433 154.403 96,019 97.697 67.496 44.738 21,124 20,807 33,509 62,686 390,902 387,461 379,722 373,573 346,731 406,394 476,452 422,875 335,950 339,704 354,471 283,627 249,664 301,354 333,641 400,185 North African countries was probably between 20,000 1 and 30,000 t in 1988. Shrimp is caught both by industrial trawlers and by artisanal fish- ermen., The principal shrimp catching countries in the region are Algeria, Bahrain, Egypt, Kuwait, Saudi Arabia and Tunisia (Table 6), Most fish- eries for shrimp in the region are considered to be fully exploited. However, there may be scope for increased landings in Algeria, Qatar and the Yemen Arab Republic. CULTURE Although there is some experimental activity in a number of countries in the region, there are no commercial shrimp culture operations, There are major constraints to the development of shrimp culture, including the availability of suitable species, lack of freshwater, and soil and climatic conditions, In the Middle East countries itis anticipated that little progress will be made, but a country such as Tunisia may be able to develop a shrimp culture industry. EXPORTS Total shrimp exports from the Middle East and North Africa were less than 10,000t in 1988, The principal exporting country in 1988 was Tunisia, which in that year shipped over 3,000 t. Other countries in the region normally export WORLD SHRIMP PRODUCTION TABLE 6. Shrimp production (t) from selected coun- tries in the Middle East and North African Region. Countr 1985 1986 1987 1988 8.750 6.058 1.843 Liles ZS na 2443 4,999 200 na 100 2260 = 2600) 3,798 = 3,135 275 KO 36) 273 Algeria wa Bahrain 1,324 Eygp! 1,939 Kuwalr 2.128 Oman wa Qatar 53 6! "Saudi Arabia Tunisia Yemen (P,D,.R.) Yemen Arab Republic 2,400) 1,756 2 390 320 * Estimated less than 1,000 t y'. Export destinations are primarily Europe and Japan. QUTLOOK There is little prospect for any increase in supply from the Middle East and North Africa. Most capture fisheries are fully exploited and culture production will be difficult to develop. Exports from the region have little impact on world trade in shrimp. This situation is not ex- pected to change. WEST AND EAST AFRICA CAPTURE FISHERIES Total shrimp catches in West Africa have probably averaged over 30,000 t in the period 1983-86. It is likely that more than 50% was caught by vessels from non-coastal countries. Of the West African coastal countries, Senegal is the largest producer with over 5.000 ty"! inthe period 1983-87. The only other coastal countries to produce consistently over 1,000 t y' are Nige- ria, Morocco and Gabon (Table 7). Spain is the leading producer of the non- coastal countries, with an average of $900 ty’! in the period 1983-86. Its vessels operate under bilateral or EEC negotiated agreements, or joint venture agreements. Fishing effort in West Africa has tended to concentrate on pink shrimp (Penaeus notialis), In several countries, notably Senegal, Came- toon, Sierra Leone and Nigeria, industry sources have expressed concern at decreasing catches and a decline in the size of shrimp caught, which can be taken as a sign of over-exploitation It is thought likely that local fishing vessels will be directed increasingly towards calching the deepwater rose shrimp (Par. /ongirosiris), 439 which has been taken almost exclusively by the Spanish fleet. Local aperators will have to invest in certain changes in equipment, notably the winches, to enable their vessels to fish at the depths required. In East Africa the principal producing coun- tries ure Madagascar and Mozambique. In the period 1986-88, over 7,000 t and 5,000 t respec- lively, Were Caught annually. CULTURE Shrimp culture activities in Africa are still at an initial stage. While experimental work is being undertaken in several countries, there are as yet no commercial shrimp farms in full opera- tion. Trial production is taking place in Gambia, Madagascar and Tanzania. Madagascar has the besi potential. At this stage it is not clear which shrimp species will be found suitable for culture in West Africa, Currently, West Afncan operations work with im- ported species (Pen. monodon and Pen. vanamei), while in East Africa (Madagascar and Mozam- bique) there is a resource of Per. monodon. EXPORTS Western Europe has been the principal outlet for shrimp from West Africa, with France the most important market. African shrimp are very popular due to existing speci¢s/taste preference. Japan is the principal market for exports of shrimp from East Africa (Pen. monoden and Pen. indicus). AUSTRALIA CAPTURE FISHERY Australian fisheries for shrimp produce ap- proximately 20,000 t. All Australian fisheries are managed under systems of limited entry, restrictions on gear and closed seasons. The northern prawn fishery is the most impor- tant with landings of about 10,000 t. The re- source is considered ta be fully exploited. The principal species caught is the banana shrimp (Per. merguiensis) which, between April and Seplember—October, forms schools in shallow water. Other species caught include white shrimp (Pen. indicus), tiger shrimp (Pen. semisuleanus and Pen. esculentus), endeavour shrimp (M, ¢- deavouri), western king shrimp (Pen. latisulcatus) and red spot king prawn (Pen. longistylus). The western trawl fishery was originally di- rected at western school prawns (M. dalli). In the 1960's a modern trawl fishery began, for which 440 TABLE 7. Shrimp production (t) from selected coun- tries in the West and East African Region. Source: FAO Yearbook of Fisheries Statistics and IN- FOPECHE. 1984 WEST AFRICA 1985 1986 1987 _ 1986 Coastal Countries Morocco 1,400 Mauitania 300 Senegal 5,300 Gambia 500 Sierra Leone 700 Cov d'Ivarre 400 Chana 200 Nigera 2,300 Cameroon 900 Gabon 1,400 1.700 200 5,500 500 700 500 500 1,500 #00 1,700 1,000 500 L300 2.100 600 1.200 S600 5.400 ava 500 soo S00 700 wai afa 600 S00 400 600 1.600 nv 1.600 3.200 2.500 R00 ao Oo 1,900 2.100 2.000 Non-coastal Countries Spain 9,400 10,500 haly 600-800 Greece 1,800 2,400 5,801) 1,100 2,400 EAST AFRICA 9,020 7,707 5.570 3.640 1,262 1,324 Madagascar 6,052 Mozambique*25,845 Tan¢ania 294 *Industnal fleet only the principal species are brown tiger shrimp (Pen. esculentus) and western king shrimp (Pen, latisulcatus). In recent years catches of these species have declined sharply, Jeading to the closure of spawning areas. Landings from this fishery account for about 15% of the total Australian catch, The southern trawl fishery lands only western king shrimp (Pen. latisulcatus). The fishery is considered to be fully expoited and has had a system of limited licences since the fishery developed in the mid 1960's. The eastern shrimp fishery is a complex of sub-fisheries, cach targeting a complex of spe- cies, The fishery is mainly based on king (Per. plebejus, Pen. longistylus and Pen. latisulcatus), banana (Pen. merguiensis and Pen, indicus), tiger (Pen, esculéntus and Pen. semisulcatus) and endeavour (M. endeavouri and M. ensis) shrimps offshore and school (M. macleayi) and greasyback shrimps (M. bennetiae) inshore and in estuaries, with some deepwater species such as jack-knife prawn (Haliporoides sibogae) and scarlet shrimp (Plesiopenaeus edwardsianus) also taken, MEMOIRS OF THE QUEENSLAND MUSEUM CULTURE Culture production is limited although some 40) farms are reportedly involved in this activity. Most farms use extensive technology and total production has not exceeded 1,500 ty”. The principal culture species is black tiger (Pen, monodon), although there are some ongo- ing trials with other local species. The selection of the black tiger as the principal species puts the entire Australian culture industry in doubt as it is unable to compete nationally and internation- ally with SE. Asian black tiger supplies because of climatic and lower production costs. EXPORT Total exports during 1988/1989 were 11,594 t with Japan as the major outlet. With its market position in Japan seriously challenged by Chinese white, and particularly black tiger, Australian exporters are successfully targeting the Spanish market for head-on shrimp. Australia is also a significant importer. Im- ports are mainly from Asian countries, with Thailand, Malaysia and Vietnam the major sup- pliers. Annual imports are about 11,000 t, and consist primarily of cheaper products. LATIN AMERICA Shrimp production in Latin America is sum- marised in Table 8. In 1988 landings from cap- ture fisheries. exceeded 200,000 t (live weight), while cultured production was about half that volume. The shrimp industry in Latin America developed rather favourably because it supplied a growing United States market, which was also willing to support the industry or at least invest considerable sums of money in it. The vast majority of facilities are of United States design and are therefore set up to suit its market requirements. This is perhaps also the reason why the Latin American shrimp sector has not been very successful in penetrating other markets. CAPTURE FISHERIES Mexico is the largest capture fishery in the region with an annual production in excess of 70,000 t y* (live weight), followed by Brazil with 50,000 t and Argentina which has produced up to 20,000 t. Panama produces about 15,000 t. Other countries in the region normally land less than 100,0001 y". A drop in production is antic- WORLD SHRIMP PRODUCTION YABLE 8. Shrimp praduction wa t). by countries in the Latin American Reginn. 1984 1985 23.1 103 67.5 19861987 7 Country Argentina Brazil Chile Colombia Cuba Equador Panama Peru Mexico Venezuela Oy mS nm te fata sw lo min Sin te —! 3,9 8.1 5.3 9.9 0.3 2.5 9.9 5.2 ipated because of significant over-exploitation and poor management. CULTURE Except for Ecuador, culture output for the re- gion has been disappointing. Currently the cul- ture sector is passing through a very difficult phase, as a result of: — limited availability of local and foreign in- vestment capital. —untavourable climatic conditions resulting in low wild fry supply and diseases, — hatcheries not operating or operating on limited scale only with poor results (low output and weak animals duc to use of antibiotics result- ing in deformities, diseases, slow growth and high mortality in grow oul ponds), — low prices in international markets. — lack of research and development, In the Latin American culture industry there are seven countries thal deserve to be mentioned: Ecuador, Mexico, Honduras, Brazil, Peru, Pan- ama and Colombia. Ecuador has accounted for over 75% of the annual production of cultured shrimp in Latin America. Production in 1985 was reportedly about 75,000 t (live weight) bul was expected to be approximately 10% Iess in 1989. No other country in the region produecd more than 5,000 t. Yields vary widely. The best managed farms produce more than 2. ha‘!y"', although the aver- age production was estimated by industry sources a( 700 kg hay. Ecuador is reported to have 124,000 ha of ponds, but in 1989 according to industry sources only 75,000 ha were in operation, owing to shortages of seed. Although there are abou! 60 hatcheries they have not been able to supply more than 25% ol the farmer's need. Thus the industry is still dependent 441 to a great extent On supplies of wild seed, which vary in abundance from year to year. Shrimp culture in Mexico is conducted exten- sively in about 10,000 ha of ponds with low yields (350 kg ha'y'). Potentially there are 100,000 ha of land suitable for culture. Growth in the industry is constrained by lack of invest- ment capital and by legislation reserving the ownership and use of land for cooperative groups of farmers. Nevertheless, this is all sct to change from 1990 with private ownership of land and trade in shrimp possible as new legisla- tion comes into effect. The fastest growth in the region 1s taking place in Honduras where there were 4,200 ha in use in 1989. It is thought that the total area suitable for shrimp culture is between 20,000-25,000 ba_ In Brazil there are reportedly 3,800 ha of ponds. With a long coastline and a favourable climate, this country appears to have enormous potential for shrimp culture. A number of differ- ent species have been tried. Progress has been slow, apparently as a result of technical and administrative difficultics. The area under cultivation in Peru is estimated to be 3,600 ha from which 2,190 t were re- portedly produced in 1988, These figures would indicate an average yield of 600 kg ha'yr!.'"The government estimates that 5,000 ha of additional land are available. Shrimp culture is possible only in the extreme northern part of the coast, It is considered that the area onder cultivation might increase to 8,000 ha. The principal species cultured are Pen. van- namet (95%) and Pen, stylirostris (5%), There are three hatcherics in operation using nauplii from Ecuador. In Panama 43 shrimp farms with a total area of 3,300 ha are under extensive cultivation. Pro- duction was reported to be 2,800 t in 1987 and 3,500 tin 1988, These figures would indicate an average yield of 1,050 kg ha‘'y’', Despite the fact that this country was one of the earliest to have major investments in shrimp culture, growth in the industry has been slow, chiefly as a result of lack of technical personnel, poor site selection (especially in relationship to the use of mangrove areas), lack of operating experience and political instability. Colombia shows potential for development, with the area of ponds and production showing favourable growth, Production has increased from 1,500 t in 1986 to 3,500 { in 1988, Other countries in the region have Jess than 2,000 ha of ponds tach, #42 If the sitaation tm the capture as well a8 culture industry does not change quickly (in quantitative and qualitative terms) the industry will continue to lose established market outlets to Asian pro- ducts, Latin American countries have the advan- tage of traditional relations and species preference in the United States and certain European markets, but are pressed to compete on price, not to mention consistent supply. For in- stance, Chinese whites are gaining market sup- port with processors in the United States. Similarly, Australian product is penetrating the Spanish market for head-on shrimp. ASIA The shrimp industry in Asia has experienced profound changes over the last 10 years, mainly on account of developments in the culture of marine shrimp (Tables 9,10). These develop- ments have brought aboul serious socie- economic and ccological repercussions on national and regional levels, and upset tradi- tional world marketing structures. Asia now accounts for about 60% of the world shrimp production, or in excess of 1.6x10" t, due to greatly increased aquaculture output. The outlook for the Asian shrimp industry is brighter than for any other region because of its competitive position in terms of production costs, and consistent supplies. In addition, the processing sector is gaining the world’s esteem because of its efficiency and high output of qu- ality product, CAPTURE FISHERIES Capture fisheries have reached maximum levels in most countries. Slight increases may still be expected from improved handling and gear. Resource conservation measures are being imposed in the majority of countries Inland capture of freshwater shrimp for export is limited, Landings appear to be affected by pollution and competition from the more readily available marine shrimp. CULTURE The marine shrimp aquaculture indusiry has developed rapidly and has reached the stage where mass production is a reality, This has mainly been the result of a production oriented mentality. Governments strongly supported this development as it was considered a potentially important source of foreign exchange and em- ployment, with significant spin-off benefits. MEMOIRS OF THE QUEENSLAND MUSEUM The prime example is Taiwan where large volumes of shrimp were cultured at high profit margins, After initial hesitation and/or a period of adaptation of the culture technology to local conditions, production virtually exploded all over the region. Pen. monodon is the prime spe- cies cultured with the exception of China where Pen. orientalis is the principal species. In most countries a number of favourable fac- tors allowed rapid development of aquacullure; — tropical climate — sound resource of broodstock and/or wild fry. — positive government support — suitable species (Pen. monadon) — tradition in culture of aquatic species. The improving availability of formulated feed and hatchery-reared fry was another significant boost for the development of the sector, Aquaculture has developed rapidly, particu- larly in Southeast Asia, On the Indian subconti- nent development has been slower, mainly because of bureaucratic constraints and limited local investment capital and knowhow. Systems employed are primarily of an extensive nature. The developmentof the culture sector in China shows a number of marked differences from other countries in the region; — shrimp culture developed in the colder northern region — the principal species is Pen. orientalis — development is centrally planned — mostly extensive operations. Nevertheless, production also increased in China at an accelerated pace, initially due to a rapid increase in pond area. Currently, the cul- ture of Per. monodon in the more temperate southern provinces is also gathering consider- able momentum, The marine shrimp culture industry in Asia has reached a critical point: — prices have dropped asa result of oversupply on the world market. Although the supply situa- tion has returned to normal, price Jevels have temained depressed since the end of 1989. Farmers will have to decide whether to continue 10 increase production with current technology, or concentrate on efforts to improve efficiency in existing operations and develop more cost effective inpuls, — current output is basically limited to two species cultured to medium sizes. Specics diver- sification could result in improved market move- ment and lower pressure on inputs. ~ major investments are needed in research and WORLD SHRIMP PRODUCTION 443 TABLE 9. Aquacultured shrimp production (1,000 t) from selected countries in the Asian Region, Source: FAO Yearbook of Fisheries Statistics and FISHDAB, Countr 1984 1985 China Taiwan Indonesia Thailand Bangladesh India Vietnam development to improve efficiency. The need for cheaper and more productive inputs and the cur- rent occurrence of various devastating discases, clearly indicate the need for considerable invest- ment in research and development, Asia has contributed considerably to im- proving supplies to major world markets, even to the extent that it is harming its own industry. This situation seems to have resulted in more secrecy and a decrease in the flow of information on actual production estimates. Producers and exporters believe that information on production has a negative effect, basing their arguments on last year’s experience. Traders in major markets respond with a wait and see position, resulting in small volumes being moved, little advance buy- ing, little confidence in the future markel, and consequently, a continuation of the depressed market prices. INTERNATIONAL TRADE IMPORTS World imports of fresh, chilled and frozen shrimp into the principal market countries during the period 1980-87 increased by 87% in volume and by 134% in value. The dominant importing countries throughout the period were Japan and the United States. During the period 1980-1987 these two coun- tries maintained their share of world markets, in terms of quantity, at58%. During 1988 and 1989 imports into both countries have continued to increase although at a more moderate rate. How- ever, the supply patterns by country of origin has experienced considerable changes particularly in the United States market. The EEC is the third largest market, and has. shown considerable growth in consumption levels, while its growth poiential is rated as impressive. 1986 1987 153.0 45.01 1988 1989 3 —" oS ht — De as Seno: | | add rs oo bo Growth in imports, by value, in the period 1980-1987 has been notably rapid in countries such as Singapore (1,750%), Italy (319%), Den- mark (312%), Hong Kong (238%) and Spain 223%). The rapid growth in imparts in such countries as Singapore, Denmark and Hong Kong has to be associated with an important re-export activity which has developed, JAPANESF MARKET Domestic landings in the period 1984-88 aver- aged about 30,000 t y''. Imports, during the pe- niod 1985-89 and in 1989 were 44% higher than they had been in 1985. The share of imports in total supplies to the Japanese market increased from 61% in 1970 ta 80% in 1980, while by 1988 it had reached 89%. For many years India had been the leading supplier to the Japanese market. In 1986 and 1987 Taiwan took the lead, but in 1988 exports from Taiwan dropped by 54% in relation to the previous year and in 1989 only §,900 t were exported. Indonesia and China assumed the lead- ing position in 1988. In 1989 Indonesia assumed the top position with exports to Japan of 52,000 t (34% more than the second largest supplier, Thailand). Notable increases in exports to the Japanese market in 1989 (compared to 1987) were achieved by Thailand, Indonesia, Philippines, Vietnam, and China. The growth in imports during the 1980's has been the result of increased demand, caused by, among others, rising incomes, favourable price levels, together with the movement of the popu- lation into urban areas, Since 1985 the strength of the Japanese currency in relation to the United States dollar has also substantially contributed ta Japan's strong import performance, Declining prices. have contributed to a signifi- ait MEMOIRS OF THE QUEENSLAND MUSEUM TABLE 10. Wild shrimp production (1,000 1) from selected countries in the Asian Region, Source: FAO Yearbook of Fisheries Stausucs and FISHDAB. Countr 19R4 1985 China Taiwan Indonesia Thialand Bangladesh India Vietnam Malaysia Japan Total “Estimated. cant change in the pattern of consumption. In 1982 institutional consumption was reported to account for over 75% of total usage, with the remainder consumed at home. By 1985 home consumption had increased (o 55% of the total usage. Because of increased retail sales the Japanese market was able to expand further in recent years, despite the fact thal institutional sales appeared to have reached saturation point. No major increase in Japanese import and con- sumption levels are anticipated. The gradually weakening yen, signs of reduced growth in the national economy, increasing competition from other food items, e.g. salmon and beef, and the already high levels of per capita shrimp consump- tion, are all factors that undermine confidence in the future growth of the Japanese market. UNITED STATES MARKET Domestic shrimp landings in the period 1985— 1988 averaged 162,300 t y"', live weight. Domestic catches of tropical shrimp have remained stable for many years, Coldwater shrimp landings declined in the carly 1980's, but have recently started to recover.and in 1988 accounted for 25% of the total domestic landings. Production {rom domestic shrimp culture is negligible. Imports increased each year during the period 1985-1988, and in the latter year were 40% higher in volume than they had been in 1985, In 1989 imports remained at the 1988. level. Imports slumped during the last quarter, when the market virtually collapsed due to an oversupply caused by dumping of Asian black tigers and white shnmp, deverted from the Japanese market. The share of imports in total supplies to the United States market increased from 53% in 1970 to. 55% in 1980 and by 1988 had reached 75%. For many years Mexico was the leading sup- 1986 1987 1988 1989* | plicr to the United States market, but this country has been unable to maintain its position. tn 1987 Ecuador took the lead, but in 1988 was narrowly overtaken by China. Most of the product sup- plied by China and Ecuador is cultured white shrimp and these two countries together ac- counted for 37% of the total volume of United States. imports in 1989, During 1989 imports from Ecuador dropped by 22% due to problems in their culture industry. The most significant factor in 1988 was the sharp increase in imports from China (+145%) in relation to the previous year, a position main- tained in 1989. [Imports from Taiwan (-53%) and Mexico (-23%) declined sharply in 1988 from the previous year, as a result of problems in culture production and Jower landings from cap- lure fisheries respectively, During 1989 Mexico maintained this level (+15%) but Taiwan lost more ground as its exports for the year dropped by another 57% compared (a 1988. Headless shell-on shrimp is the predominant product lorm for imports and in 1988 accounted for 71% of total imports, During the period 1985-88 imports of headless shell-on product grew by 54%, while peeled shrimp imports in- creased by 18%, In the period 1970-80 United States consump- tion of shrimp increased by only 995. In the period 1980-88, however, it grew by 78% asa result of the inercasing popularity of shrimp and improved availability, Sull, per capita consump- tion in L988 was a modest 1.1 kg (edible meat weight). The drop in price levels for the medium sizes (20-25 and 26-30) during 1989 was the result of a substantial increase in supply of these sizes, mainly cultured product from Ecuador, China and Southeast Asia, The large sizes (under 15) followed suit as the price gap widened. WORLD SHRIMP PRODUCTION 445 The prices for the smaller sizes held up rela- tively well in 1989 because of increased sales through retail outlets and the fact that imports of these sizes from Ecuador were much below nor- mal (and anticipated) levels. In recent years the pattern of consumption has changed. It is estimated that about 30% of shnmp is now sold retail, as compared to about 15-20% as recently as 5 years ago. Lower prices have enabled retail outlets to sell shrimp.at prices which make it attractive in relation to competing products, and which provide favourable profit Margins, The current United States market can be de- scribed as unsettled as nobody seems to have a clear picture of whal is happening. There is only scattered news on the production side, which is also mostly based on rumours, Asa result trading is generally for immediate use only al depressed price levels, There is definitely no clearly de- fined direction. The United States market can be expected lo have great potential in terms of an increase in imports although the current weaken- ing of the economy will probably have a negative impact on growth, The lower value of the dollar and higher interest rates are additional negative factors. On the other hand, anticipated higher fuel prices could have a negative effect on do- mestic landings, leaving more room for imports. EUROPEAN MARKET With a total consumption of over 250,000 t in 1988, live Weight equivalent, Europe follows Japan and United States as the third largest market forshrimp. Coldwater shrimp (Pan. borealis), which is the major product in the Western and Northern European markets, is mostly supplicd by coun- tries [rom the north Atlantic, Declines in catches by Norway and the USSR have been compen- sated for by relatively stable landings in Green- land, Tceland, Faeroe Island and Denmark. The proportion of coldwater shrimp in the (otal shrimp supply to the European market declined from 49% in 1982 to 41% in 1988, although it increased in absolute terms from &1,000 t to 106,900 t during the same period. Imports of shrimp into European countries in 1988 were 45% higher than they had been in 1985. The increases jn imports of tropical shrimp can also be ascribed. at least partially, to the strength of (he Enropean currencies in relation to the United States dollar and the slow growth in the supply of the preferred coldwater species. Price considerations may also have played a role in the growing importance of tropical shrimp, Contrary (0 the preference for coldwater shrimp in northwestern Europe, consumption in south- ern European countries, especially Spain, France and Italy, is primarily directed towards tropical shrimp, and one of the most preferred product forms is head-on shrimp from Africa, the Medi- terranean and Latin America. Despite consistent supply and price advantage Asian shrimp have not been able to make inroads in Spain and Italy, Quite the contrary can be said abou! Western Europe, which can be considered black tiger and chinese white territory by now. Little impact is expected from the opening up of the eastern European markets in the short term. Incomes are too low, Judging tram the economic preference and current per capita consumption, Europe offers the most promising growth potential. However, it should be kept in mind that shrimp does not occupy the same status and popularily in Europe a8 it does jn Japan and the United States. MINOR MARKETS There are a number of important and rapidly growing markets suchas Singapore, Hong Kong, Canada and Australia, In addition, the metropali- tan areas in developing countries harbour a sub- stantial number of wealthy people who do dine out frequently and like to consume shrimp. Their role in the world shrimp market will become increasingly important, For instance, Brazilian exporters indicate that they could scll the entire national production in the home market, and only export to carn hard currency, FUTURE MARKET PROSPECTS The sharp drop in world shrimp prices during the fourth quarter of 1989 has been 8 reminder to producers and traders that shrimp, like all traded commodities, is subject to fluctuations in price when the forces of supply and demand are out of balance or when a traditional trading pat- tern falls apart and uncertainty takes over. The rapid expansion in recent years of cultured shrimp production in Asia and Latin America caused a temporary oversupply on world mar kets. The sudden fall in prices was inevitable. Other factors that contributed to the dramatic weakening in market conditions during the last part of 1989 were; 1. the oversupplcd and temporarily saturated Japanese market 2, the gradual reduction in prices since early 1988 3. the increasing competition among ex- porters 4. the switch from a supply to a demand driven market 5. the marketeers in major markets not being ready for the new demand driven market situation. Tn considering the future market prospects for shrimp over the next five to ten years it 1s impor- tant to maintain a focus on Jong term trends and underlying market forces, and to avoid being overly influenced by the recent dramatic events of 1989. To a certain extent this recent crisis has already been overcome, although at considerable cost. During most of 1990 the major markets actually experienced a shortage of certain spe- cies and sizes, as a result of production problems and sustained high consumption. Overall demand for shrimp over the next de- cade will depend mainly on such factors as population growth rates; increases in disposable income; prices of shrimp; prices of meat, fish, poultry and other substitutes for shrimp; and consumer tastes and preferences. Forecasts of changes in demand for shrimp depend upon an- ticipated changes in these factors and on the responsiveness of shrimp consumers to these changes. The World Bank predicts that the population growth rate in industrialised countries during the 1990’s will be about 0.3% annually, while that of developing countries will be about 1.8% an- nually. Overall, the world population is pre- dicted to grow at annual rate of approximately 1.4% during the 1990's, Although total popula- lion growth will affect overall shrimp consump- tion, it will largely depend on the increase in the number of people who can afford to buy shrimp, how much theirdisposable income will grow and how much of this total disposable income will be spent on seafood (i.e. shrimp). The World Bank forecasts that the real Gross Domestic Product (GDP) in the industrial and developing countries will increase at average annual rates of 2.6% and 4.9% respectively over the present decade. This suggests a weighted average growth rate of GDP worldwide of ap- proximately 3.5% and an average per capita in- MEMOIRS OF THE QUEENSLAND MUSEUM come growth rate of about 2% annually in the 1990's. Estimates of the income elasticity of demand for shrimp vary widely from market to market. In our opinion overall income elasticity of demand for shrimp will be less than 1.0. Using the estimate of slightly less than 1.0 as the future income elasticity of demand for shrimp, a world- wide population growth rate of 1.4%, an average growth rate of per capita income worldwide of 2%, and other factors remaining constant, shrimp demand should rise at an estimated annual rate not exceeding 2.5%, up to the year 2000, With total world shrimp production in 1988 estimated at approximately 2.45 x10° t with demand expected to continue to grow at about 2.5% annually, the total world production for shrimp will have to rise to about 3.2 x10° t by the year 2000, It is not expected that there will be any significant increase in landings of shrimp from capture fisheries, A certain proportion of the required supplies will come from reduced post-harvest losses because of better handling and improved yields through new processing technologies and product development. Nevertheless, the major share of the additional supplies will have to come from culture opera- tions which will have to grow from the 1988 level of about 560,000 t to about 1.3.x10° tin the year 2000. This implies an annual growth rate of cultured shrimp of about 7% over the period until the year 2000. Thus production will have to continue to increase at the 1985-90 rate, result- ing in a cultured shrimp production at the year 2000 of 1.5 x10" L Such a growth rate of cultured shrimp output appears highly unlikely without either a significant rise in real pond bank prices and profit margins approaching 1988 levels, or a major breakthrough in culture technology that will substantially lower production costs, and/or increase output. Therefore our forecast is not one of an over supplied market, although there may be periods of excess supplies, e.g. because of temporary favourable natural conditions. Price levels to the producer/exporter will very much depend on marketeers in major markets successfully pro- moting shrimp as a tasty, healthy, and valuc- for-money food item, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM a7 ANALYSIS OF CATCH STATISTICS FROM THE DEEP-WATER PRAWN (HALIPOROIDES SIBOGAE) FISHERY OFF NEW SOUTH WALES, AUSTRALIA, The deep-water trawl fishery Tor Toya) red prawns (Hali- poroides sibogae De Man, 1907) has developed quite re- cently (mid 1970s) off New South Wales, Australia. Temporal and spatial trends in catch, fishing effort and catch-per-unit effort (CPUE) were analysed using landing statistics. from fishermen’s cooperatives (1978-1985) and data from a recently introduced logbook system (1985 1988). Fishing effort and CPUE were standardised using (i) a method derived from Gulland or (ii) log-linear regression lechniques depending on the quality of data which diftered between areas and periods of time. Regression techniques also allowed identification of factors influencing the vuria- bility of CPUE. Time of fishing (in terms of three month period) and engine power of vessel explained 79.4 and 20.66 of the variability of CPUE accounted for by the regression model, respoctively. Fishing effort was concentrated within small ranges of latitude (1°) and depth (100 m), Economic and logistic fac- tors, rather than differences in prawn abundanve, may be responsible lor this geographic concentration ot the tishery. Suggesting that the royal red prawn stock isnotexploiéd over AN APPRAISAL OF TRAWLING AS 4 TOOL FOR STOCK ASSESSMENT AND DEVELOPMENT OF HARVESTING STRATEGIES IN SOUTH AUSTRALIAN PENAEUS LATISULCATUS FISHERIES. South Australian prawn fisheries are based on a single fenaeid species Penaeus latisulcatus. Over the last decade, prawn landings in Spencer Gulf have ranged from 1.4 to 2.3 thousand tonnes with a current export value of S50 millon. ‘There has been a marked increase in larger prawn grades of the catch attributable 10 refinement of harvesting strategies. The Spencer Gulf fishery is limited entry (39 vessels) with controls on gear, Vessel physical characteristics, amount and direction of effort, Large scale survey sampling is undertaken in conjunction with industry for stock assessment and for development of real time harvesting strategies. The main objectives of the research are: lo develop strate- gies which minimise the risk of recruitment over-fishing and lo optimise the value of the catch. This paper is a brief zppraisal of trawl sampling methodology und ils application to management. Trawl sampling is systematic over a wide scale and is primarily based on stratified sampling plans. Inherent prab- lems associated with sampling are apparent. Sampling hus a number of functions which in tum require different sampling plans, Owing to environmental gradients. sampling variance can be minimised by sampling across rather than along the gradient However, cross sampling has practical restrictions: its full distriburion, The absence of obvious temporal and spatial variations in CPUE indicated that royal red prawns caught off centril and southern New South Wales belonged to the sume stock which was available throughout the year. This apparent temporal and spatial stability of CPUE con- trasted with the great variation in CPUE generally observed for coastal prawn species revealing an important difference in the population dynamics between coastal prawns species and deep-water royal red. prawns. From 1979, annual landings have been stable at about 300-350 tonnes and there is al present no apparent reason for concern for the state of the royal red prawn stock off New South Wales. However, the availability of catch and effort data in the present study was limited in space and time. To better understand the relationship between fishing patterns and trends in abundance of prawns it would be necessary to 1) extend the area covered by logbooks, which is limited presently to centfal and southem New South Wales, and 2) conduct stratified fishing surveys outside the main distribu- Lon of the fishery, P. Baelde, Fisherves Research Institute, NSW Agriculture and Fisheries, PO Box 21, Cronulla, New South Wales 2230, Australia. furthermore. information is lost relating (o spatial size struc ture Which is necessary for closure delineation. Mixed sum-~ pling plans and the value of strategic ‘spot’ surveys provide a Solution to the problem. The information obtained from survey sampling is used in conjunction with fishermen's log book data for evaluation of ihe effects of fishing, parameter estimation and development of sequential harvesting strategies. The application of survey dala 0 ‘optimal’ harvest simulation incorporates a harmonic growth model which enables predictions of biomass and value at different regions in the Gulf, Resulis show that natural mortality bas a large influence on model predictions, Information indicates that biomass and biovalue Lrends differ depending upon the size composition of the population. However, over all regions, both biomass and biovalue decrease from June to February. Hence, effort reduction from June to March has two advantages: it reduces reproductive depletion attributable to fishing and results in increased value of catch. The work demonstrates the impurtance of the participation anid coopermtion of fishermen in research and management. N.A, Carrick and ©, Moore, South Australian Department of Fisheries, GPO Rox 1625, Adelaide, SA 5000, Australia. R.L, Carrell, CSIRO Biometrics Unit, Private Bag 2, Glen Osmond, South Australia 5064, Australia MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 448 THE BIOCHEMICAL COMPOSITION OF NATURAL FOOD OF PENAEUS ESCULENTUS HASWELL (PENAEIDAE; DECAPODA) The development of artificial diets for penacid prawn aquacullure has been almost entirely an envpirical process. largely driven by the need to provide a diet |hat gives good growth al minimum cos!. Some of the early work was done by Kanazawa et al. (1970) and Deshimam and Shigeno (1972) who formulated artificial diets for Penaeus japonicus based on the composition of the short-necked clam. Tapes (=Venerupis) philippinarum. Penaeus japonicus grows well ona diet of this clam, but it is not normally eaten in the wild, A more logical approach would be to formulate a diet based on the composition of the natural food of the prawn, Was- senberg and Hill (1987) studied the diet of juvenile Penaeus esculentus in seagrass beds and found that ihe main prey items were small pastropods, bivalves and Crus{acea. We have analysed and compared these prey animals together with lwo commercial prawn feeds. Materials and Methods The most abundant known prey of juvenile Penaeus eseu- len(us (i.e. 3 species of gastropod, 2 bivalves, 4 crustacea. a polychaete, and ripe and green seeds of Zostera capricorm) were collected from an intertidal seagrass (Zostera capri- corni) bed in Moreton Bay, Queensland. Collections were made in September, February and May when juvemile P. eéscuilentus were present, Proximate analyses (water content. ash, lipid, protein and carbohydrate), lipid class, fatty acid and amino acid analyses were carried out on each of the prey species and on 2 commercially produced prawn feeds, one formulated for P. monadon and the other for P. japonicus. Results and Discussion The natural diet contained high levels of ash from the shells and exoskeletons of the prey animals so comparisons with the commercial] diets, which contained much lower levels of ash, have been made using the ash-free dry weights. Protein content of the prey animals ranged from 52-76% of ash-free dry weight, lipid 10-20% and carbohydrate 6-21 %. Zostera seeds. which are ealen seasonally, contained 9% protein, 4% lipid and over 60% digestible carbohydrate. Using the % numerical composition dita of the prey animals of the prawns (Wassenberg and Hill, 1987) and the weights and proximate analyses of representative animals, a profile MEMOIRS.OF THE QUEENSLAND MUSEUM of the natural diet of the prawns was calculated, The profile. expressed in terms of the ash-free dry weight, indicated that the natural diet of the prawns contained 66% protein, 13% lipid and 21% carbohydrate. The protein contents of the commercial feeds were 51% and 77% of the ash tree dry weight, 8% and 16% for lipid and 41% and 8% for carbohydrate. Amino acid composition was fairly uniform in all species and similar to the commer- cial feeds, Cholesterol was above 4% of ash-tree dry weight; phospholipids ranged from 22-80% of total lipid. Saturated fatty acids were mostly less than 45% of total fatty acids and polyunsaturated fatty acids ranged trom 24-56% of the lotal, The Zostera seeds contained no fatty acids with a carbon chain length greater than 18, The commercial feeds had a similar saturated fatty acid profile to the prey animals but differed in the mono- and polyunsaturated fatty acids with highér concentrations of CL8:1w9 and C18:2w6 and with a lower concentralion of C20:4wé6, reflecting the presence of vegetable oils. P, esculentus is a relatively slow growing prawn in both aquarium sysiems and in aquaculture ponds. The reason for this could be some response la environmental condilions in caplivily or an unsuitable diet. The difterences between the proximate and fatty acid profiles of the natural diet and the commercial feeds formulated for other penacid species sug- gesls thal growth of P, esculentus may be improved by altering the formulation of the feed towards that of the natural diet. Literature Cited Deshimaru, QO. and Shigeno, K. 1972. Introduction to the artificial diet for prawn, Penaeus japonicus. Aquacul- ture 1: 115-133. Kanazawa, A., Shimaya, N., Kawasaki, M. and Kashiwada, K, 1970, Nutritional requirements of prawn — |: Feed- ing on an artificial diet, Bulletin of the Japanese Society for Scientific Fisheries 36; 211-215. Wassenberg, T.J, and Hill, B.J. 1987. Natural diet of the liger prawns Penaeus esculentus and Penaeus semisulcatus. Australian Journal of Marine and Freshwater Research 38: 169-182. W. Dall, D.M. Smith, and L.E. Moore, Division of Fisheries, CSIRO Marine Laboratories, 233 Middle St, Cleveland, Queensland 4163, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM SPAWNING CONTROL OF THE JAPANESE SPINY LOBSTER The Japanese spiny lobster, Panylirus japonicus. is a very important crustacean in Japan. In this Study, the nature of their breeding was investigated as a basis for potential aqua- culture of (his species, The normal breeding season around tzu Peninsula, Japan, is trom June to August Incubation period was variable and temperature dependent, At normal water lemperature on {zu Peninsula in 1989, the ineubation period was two months, Phyllosams larvae were seen toward the beginning of August. Lobsters were maintained in running sea water aquaria, 142 x 142 x 84 cm, with a capacity of 1,000 L and were fed short-necked clams or fish. Body weight and carapace length of lobsters Were 70-440 g and 39-80 mm in females, and 65450 g and 41-80 mm in males. Beginning in 1983, animals were held at normal, ambient water lemperatures ur Al constant temperatures of 20°C and 25"C Paired mature lobsters were transfered lo smal) glass aquana for observations of copulation and spawning, The mature female lobster grooms the pleapods with the filth leg before copulation. Body weight and carapace length of lob- sters in copulation were 125-310 g and 52-70 mm in females. and 210-360 g and 59-75 mm in males. Males were larger than females among copulaling pairs. Copulation and spawning were observed early in June. Copulation generally occurred al night to early morning. The pre-copulatory phase of the courtship lasted 1.5—3 hours. In EXPERIMENTAL CARAPACE INCREASE IN THE LOBSTER (ffOMARUS AMERICANUS) FISHERY ON CAPE BRETON ISLAND, CANADA The Gulf of St. Lawrence lobster population has histori- cally been very productive, landing hall uf the landed weight of Jobsters in Atlantic Canada, While the fishery has ex- perienced fluctuations over the last hundred years, landings ig the past fourteen years have steadily increased with the exception nfareas in eentral Northumberland Strait, The Gulf of St. Lawrence lobster fishery captures 75% of lobsters at the commercial ‘canner’ size (63.5 ta 80.9 mm) and 15% at the commercial ‘market’ size ($1.0 mm and greater}. The lobster population of the southern Gulf of St La- wrence experiences a wide seasonal range of temperature, a range of 0'-20"C is possible al a depth of 10 metres, Under these conditions, some lobsters moult twice a yeur, Femule lobsters become functionally mature al a smaller size (77-80 mm) than in other areas on the Atlantic coast. Recent studies on fecundity haye shown that Gulf lobsters carry more egas ata given size than lobsters from other regions. In 1987 we promoted wn experimental legal carapace size increase programme on (he west coas! of Cape Breton Island, The purpose was lo determine experimentally whether an increase in minimul legal size would enhance yield as predicted by the current models. Over four years the legal carapace size was raised by steps of 1/16" from 2 1/2" wm 2 3/4" (63.5 |] 700 mm), The fingl increment was 249 copulation, the male embraced the female, belly to belly, for about 20 seconds. With a vigorous, extension of the male's abdomen, spermatophores were discharged and deposited on the fomale's sternum and werestored externally, Frequency of copulation was between one and four times at night. Within 10-]30 minutes after final copulation, spawning, or oviposition began, During oviposition, the female lobster usually assumes a vertical position that will guarantee pus- sage of the eggs [Tom the oviducl opening to the ventral side of the abdomen where the cggs wre eemented tw the pleopads. Ovipasition required 30-50 minutes, Thirty to 550 thousand egps were deposited. Egg size was abour0,5 mm in diameter, In lobsters held a 20°C and 25°C in the laboratory, spawning was observed in March and April, 1.5-2 months before the sturt of normal spawning season and spawns in animals held al normal water temperatures. The eggs hatched early in May and June. Our observations suggest that spawning, of the Japanese spiny lobster can he controlled by changes in the water lemperature of the rearing aquaria This may be of great significance in the polential aquaculture of this species. Yoshiakt Deguchi and Haruo Sugite, Department of Fisheries, Nihon University, Takyo, Japan, Fred I, Kamemoto, Department of Zoology, University of Hawali, Honolulu, USA, completed in 1990, During the carapace size increase peo- gramme the size [requency distributions of lobsters caught im the commercial fishery were monitored in the area and in udjacenl control areas. Lobster lagging programmes were completed in [954 and 1988 in the experimental zone to Jetermine if any changes in movernent or growth would occur, To date, the size frequency distributions show only aslight increase in percent frequency for lobsters released during the first three years of the project and presently reaching the new legal size. The expetiment will be pursued over a period of five sears in order lo contrast benefits, if any, of the minimal size increase in the experimental area with the control areas, ALOIS POIDL I Hime iL ts NOL possible to identity any benefits resulting from the carapace size increuse despite the madel predictions, Landings increased considerably more in one control area than in the experimental arew, The ag returns to date do nol show significant differences in the growth or Movement pallens as seen before the carapace increase programmy, It presently appears very difficult to distinguish any changes generated by the minimal size increase from changes generated by natural environmental causes, These fesults are similar to those encountered by meteorologists controming predictive modeling and chaos Gerard ¥, Conan and Donald R. Maynard, Department of Fisheries and Oceans, Gulf Regions, PO Box 5080, Manaion NB, Canada MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 450) MANAGEMENT AND ENHANCEMENT OF THE STOCK OF PENAEUS ORTENTALIS KISHINOUYE IN THE VELLOW SEA AND THE BOHAI SEA Penaeus oricntalis is 4 large, lemperate, migratory species occurring between tatitudes 33°30'—4)°00'N, [Loverwinters (December to March) in waters of 60-A0) ra depth in central and southern areas of the Yellow Sea, and spawns from carly May to eutly June around estuaries af the Yellow Seaand the Bohai Sea. As the shrimp fishery. is intensively exploited, recruitment is related to Spawning stack, as well as factors such as rainfall, runoff and salinity. The vear class yields of the shrimp in the Bohai Sea have shown periodic fluctuation in recent years, The average yield Was. 26,5801 in the late 1950s 19,391 (in the 1960s. 30.430 tin the 1970s, 19,2071 in the early 1980s, The maximum yleld of 50,653 t occurred in 1979 and a miniraum yield of 6,429 t occurred in 1984. Although the average yield in the early 1980s was similar ta (he 1960s, since then the shortage of spawning stock has led to a decrease of year class recruil- ment, The management ot shrimp fishery in the Yellow Sea and the Bohai Sea involves two strategies. 1, The protection of spawning stack and postlarvac so as to increase year class recruitment. A regulation forbids their capture along the migration route and in the spawning grounds, In addition, there are regulations which prolect postlarvae and juvenile shrimps in the Bohai Sea. This pro- lection includes closed aréas and closed periods tor the use of nets that could damage postlarvae and juvenile shrimp, and prevention of damage to postlarvae and juvenile shrimp by pumping water for pond culture, Sall-making anu other in- dustrial Usage. 2. The management of the autumn fishery i ihe Bohai Sea, or the problem of how to utilise and allocate the resources after a year class has matured. Before 1987, the open dates of the autumn shrimp fishery in the Bohai Sea were Septem- ber 5 for drift nets, September 15 for moator-sailboats equipped with trawls, and October 5 for motorstrawls. From the beginning of the 1988 autumn fishing season, all trawlers have been excluded from the Bohai Sea. and only ships equipped with shrimp drift nets, are permilled lo fish in the guluron lishing season in the Bohai Sea, The major problems of the autumn shrimp fishery tavolve the huge fishing power employed, high fucl use and poor economic efficiency, Beyond a certain level, fishing mortal- ity (F) does not increase linearly with fishing power, This is due to the limited shrimp fishing areus in the Bobai Sea and over-concentralion of fishing vessels. When the number af fishing vessels is beyond a certain limit, Fuel consumption rises while fishing coefficient (q), production rate and profit decrease, The numbers of al] major types of nets used in the autumn shrimp fishery in the Bohai Sea and the shrimp catch differs greatly from vear to year. From the 1960s to the early 1970s, MEMOIRS OF THE QUEENSLAND MUSEUM shrimp catch was largely made by bottem trawls of motor- sajlboats and motor-trawlers, In late 1970s, owing \o an earlier Opening date, the shrimp drift net fishery developed rapidly and shrimp yield from drift nesis increased. By L9S0s, they began 10 dominate shrimp fishery, capturing mare than 80% of the vield from 1986 to 1987, Shrimp Stack Enhancement Shrimp recruitment fluctuated from year to year, ranging trom 1.07 ¥ 10° (1985) to 1.40-x 10" (1961). The shrimp resource has had a low recruitment level particularly since carly 1980, Hence, the release of hatchery rewred larvae can be expected (o enhance the shrimp resources in the Bohai Sea and increase yields. Postlarvae. 30-50mm in length, are regarded as the best size (ecologically and economically) lo release. There are many shrimp hatcheries and farms along the coast of the Bohai Sea thal are capable of providing seed for release. The waters around the estuaries of the Yellow River, Haihe River and other rivers in the Bohai Sea are ideal release arcas with suitable conditions (good water quality with abundant food, and few predators) for shrimp survival. The best release time is when the sea water is muddy atrer strong winds, an the ebb, and when watcris nor being pumped by power plants and salt works. Postlarvae are easily caught by predators immediately afer being released as the larvae ure weak and stressed by new environmental conditions. Proper selection of release time and sites is therefore of great importance to minimise natural and made-made mortality. Peterminarion of the optimal quannty of postlarvae tor release in a specific sea waters ix a complex problem. The optimal quanuty depends on the ecological capacity and natural recruitment abundance in the specific waters, Artifi- cial releases can considerably affect ecological balance, in lerspecifi¢ relations and population succession. By using an annual shrimp resources estimation model, the shrimp num~ ber required lo maximise catch in the Yellow Sea aod the Bohai Sea was estimated to be 1.2 billion (food iy a major limiting factor to increase of shrimp recruitment). Since 1984, commercial shrimp posttarvae releases have been carned out in the Bohai Sea, the Yellow Sea and the east China Sea, Good results have been obtained; recapture: Tate was estimated asc. 10%. In the East China Sea, where the original P. orientalis population was very small, 4 natural stock large enough for fishing has grown up after many years of releases, In the inshore waters of the Yellow Sea, where previously natural shrimp populations were small and annual recruitment showed large fluctuation, recruitment has steadily risen after a series of large-scale seed releases. There is Stil] a great potential for artificial seeding the Bohai Sea. The release numbers will be increased in years to come to reach the ecological capacity of the region. Jingyaa Deng, Yellow Sea Fisheries Research Institute, Qingdao, Shandong 266003, China. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSELM EVALUATION OF SEASONAL CLOSURES AS A MEANS OF OPTIMISING YIELD FROM A MULTI-SPECTES PRAWN FISHERY Seasonal closures have been used ts a means of Optimise vield (rom Queensland's multi-species coastal prawn fisher- ies, Field studies and a log book data base have demonstrated that the fishery is supported by six penagid species. four ot which ure significant contributors to the fishery. Species composition has varied significantly across distances as litle as 1U0 km, and both the timing and strength of reeruumient has varied during the two years (1989- ]990) in which sam- pling look place, A deterministic model, based upon Thompson and Bell's (1934) yield model, has been used as an iniial means of estimating yield (weight of prawn and dollar value) from a given recruitment sequence. The model allaws for variable focruitment liming, Species composition and nyoriality, Te has the advantages of being mathematically simple, Nexible in respect ol variability in inpul parameters, and readily adapted fo either spreadsheel or microcomputer programming. Input parameters have been estimated from data obtained in tag- ging und field sampling programmes (Gribble and Dredge. 1991), or from published literature. There is a wide range of seenarios under which the model can be run, By varying growth and mortality parameters, polential vield from the fishery can be established across normally acceptable ranges of these parameters. The major role of the model was to test the value of yield under 4 seasonal closure regime of management. Under a conventional scenario of constant fishing mortality, Output from the mode) suggests that closures had little positive or fegalive effect upon vield fram the fishery. Im econaniic terms, the clasure would thus appear to be of lintle benefit to THE WHITE SHRIMP [PENAEUS SETIFERUS| FISHERY IN THE CAMPECHE BANK, MEXICO The whille shrimp Pendeus setiferies (Linnaéus, 1767) is amongsrthe most economically important penacid species in the southwestern Gulf of Mexico, with more fhan 1000 tonnes caught annually, It supports three different fish eries in the area: am artisanal estuarine fishery, a drift nel fishery. offshore and the industrial (raw) fishery. Relation- ships between these fisheries were analysed using yield per recrult models. Interaction between sequential fisheries (esiuarine artisanal versus marine fisheres) is relatively low, as tho estuarine fishery on white shrimp is small. Neverthe- less, artisanal estuarine exploitation could exert a negative effect on the marine white shrimp fishery if the fishing effort increases inshore. Parallel offshore interaction (drift net and trawling fisheries) is stronger, since the types of gear used in the artisanal marine fishery are very efficient at catching white shrimp, This fishery is selective on large mature shrimp, Catches of the parallel fisheries are inversely related However, the investment, costs and benefits of the drift net fishery make (his activity highly profitable and competitive with the industrial trawl fishery, A simulation model of the effect of the (hree Fisheries suggesied thal (he 1984 fishing eHort was nearing the critical reproductive biomass. 43) industry. However, log book data clearly indicate that imme- diately following the cessation of closures, the fishery under goes a heavy pulse af etfort, which diminishes ws the fishing: season progresses, Under such a regime of fishing mortaliry, the model suggests thal yield ik increased as a consequence of the closures, This is achieved as a consequence of higher exploitation rates of the stocks. The subsequent output fren reduced spawning stocks remains (o be delermined. The variability of recruitment dynamics In this tishery indicates that seasonal closures are unlikely to optimise yield unless carried Gul on a tegional basis, in conjunction with @ deiuiled sampling programme. The authors intend to investi- gale the spalial dynamics of the fished species and incar- porale these dala into an evaluation of spatial closures as ai alternative Means. of Optimising the fishery, Literature Cited Gribble, N.A, and Dredge. M.C,L. 199) Preliminary results foracentral Queensland cousial prawn fishery, Memoirs nf the Queensland Museum 34:453 Thompson, W.F, and Bell, FLH. 1934, Biolugical statistics of the Pacific habital fishery. 2. Effects of changes in intensity Upon total yield and yield per Unit Of Year, Report af the Intemational Fisheries (Pacific Habirat} Carmrssion &: [-19, MCL. Dredge, Fisheries Branch, Southera Fisheries Centre, PO Box 76, Deceprioy Bay, Queensland 4508, Avwstratia, NA. Gribble, Fisheries Branch, Q@DP, Fisheries Laboraiory, Gibson Sireet, Burnett Heads, Queensland 4670, Australia. The white shrimp spawns throughoe! the year, resulting in continuous recruitment. However, seasonal variations in re- cruitment result in periods of low and high abundance. The telationship between spawning and recruitment did nat show a Significant correlation (C.2>P>{.01) when analysed as bi- ological years. This lack of correlation is attributed to the effect of environmental factors, as Well as inter-annual vari- ability of recruitment strength in the main. cohorts throughout the year. A Ricker Stock-tecruitment relationship (P>0.001) Was established fordominant cohorts in the 1973-1984 study period. The explained variance increased from 70% to 84% when the model included the rivers® discharge during the previous recruitment month and during the spawning pertod four months prior. The river discharge has both negative and positive effects on recruitment. Its increase during spawning time can restrict the habitat available tor successful estah- lishment of shrimp postlarvac, but on the positive side, adrop in salinily can ingger juvensles ta migrate to sea, The recruit. ment level depends largely upom the carrying capacity of critical nursery habitats. White shrimp adopt an opportunistic strategy to efficiently exploit the seasonal variations In estuarine carrying capacity associated with river discharge. A. Gracia, Instituto de Ciencias del Mary Limnologia, Apdo, Postal 70-305 México, D.F, 04510, Méxicn. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum COMMERCIAL RECIRCULATING SEA- WATER SYSTEMS FOR HOLDING ROCK LOBSTERS IN TASMANIA, AUSTRALIA Annual production of southern rock lobsters (asus novae- hollandiaé) in Tasmania is usually about 1750 ~2250 | with a landed value of $29.2 million in 1987/58. While the majority are sold chilled or frozen, 4 proportion ure held in land-based tanks prior to domestic or export sale al a pte- jium pricé as live product. In this paper technical aspects which could have influenced mortality in these systems are discussed. Lobsters may be stressed, prior lo reaching the holding facility, by being kept ou! of water for up to five hours in inadequately cooled vans during road trinsport, Severe swelling occurs around joints and many rock lobsters have ta be processed instead. Loss of limbs also reduces product value, Tdeally, a land-based facility should have a continuous seawaler supply with a salinity of more than 27% and flow-through holding tanks a+ large amounts of orgunic matter are released soon after stocking. Accumulation of organic matter in biofilters leads io excessive oxygen demand and ammonia production by heterotrophic bacteria and sul- phide production in any poorly exchanged areus (Furteath, 1990), Recirculating systems are used at most facilities and successful inland units rely almost totally on these systems, They are akin wo soft crab or freshwater crayfish shedding systems in that the animals are not fed (Malone and Burden, 1988; Munthe ef al., 1988) and water should flow through the holding tank, physical filter, biofilter and comling system in that order. The holding tank is usually a simple fibreglass or concrete tank of 1m depth, Rapid sand filtration is preferred over dscron filter media although overloading of sand media with organic matter can occur despite backflushing. A sep- arate biofilier tank, containing shell grit tor bulferng capac- ity, is preferred to reduce accumulation of organic malter within the biofilter. Three key environmental variables inMuencing biofilira- tion efficiency are; large salinity fluctuation, water lempera- ture and dissolved oxygen Jevels. Technical problems including inappropriately insulated buildings and inadequate cooling sysiems have hindered iemperalure contro) in Tasmanian systems. Operators usually aim to operate the systems at 10-12°C thereby reducing ammonia production, Ideally the reduction to 6°C, prior ta londing of rock lobsters into export packs, should be done in separate 4ystoms ay the temperature reduction could disrupt biolilter function, The capacity for maintaining dissolved oxygen levels at 2 mgL- : throughout the biofilter. along with flow rate, surface area of medium and bacterial populations, will determine the amount of ammonia that can be converted to nitrate and hence the biological loud that the biofilter can accommodate (Manthe er al. 1988). Biofilters which contain partially exposed media and are supplicd will) Seawater via gentle suttace sprays may be adopted. Alternatively, ifthe biofilter medium is fully submerged, airlift pumps should be included to enhance oxygenution of the biolihee (Marthe ef al, 185). MEMOIRS OF THE QUEENSLAND MUSEUM The holding tanks are usually aerated with very turbulent surface generate removable organic foam, and may be aug- mented with occasional inpuls of oxygen especially after stocking of rock lobsters as oxygen demand is high, Al- though separate aeration systems are rarely !ncluded in the designs for holding tanks, they should be used as they en- hance circulation near the lank bottom and help ensure that waler is well oxygenated before entering the biofilter, Operators may maintain a small population of rock Job- sters or fish in the holding systems to help establish or maintain appropriate bacterial populations ¢.g. Nitroso- monas and Nitrobacter, prior to bringing rock lobster densi- fies up 1 commercial levels in the holding tanks (about 60 kg m’*). Alternali vely, commercially available bacteria may be added. However, the bivlogical load should be increased progressively, i.e, no more than 1()% per day (Malone and Burden, 1988). Even when high bacterial densities have become established (up to six weeks aller initiation of biofit- ter), sudden increases im loading will exceed the capacity of the biofilter thereby leading to stressful levels of ammonia and nitrile, Unfortunately, as large numbers of rock lobsters become avallable, the holding systems are subject to sudden changes in loading and often pH, ammonia and nitrite levels ure notadequately monitored, However, operators are reduc- ing losses by minimising holding periods for tock lobsters within their systems, Ata research level, more information is needed on biofiltur design, appropriate biological loads, maintenance of bacterial populutions and toxicity of am- monia dnd nitrite, The use of chemical sources of ammonia and nitrite for conditioning biofilters appears promising (Manthe and Malone. 1987). We were able (o condition a Hepical marine binlilter in 18 days without a bielagical load by using commercial bacteria and chemical sources of am- monia and nitrite (NHwCl and NaNO), Literature Cited Forteath, G.N.R. 1990, ‘A handbook on recirculating sys- lems [or aquatic organisms’. (Fishing Industry Training Board of Tasmania: Hobart). 72Zp. Malone, R.F_and Burden, DG, 1988, ‘Design of recirculat- ig soft crawfish shedding systems”. (Louisiana State University: Baton Rouge), 749, Manitke, D.P. and Malone, R.F., 1987. Chemical addition for accelerated biological filter acclimation in closed blue crab shedding system, Aquaculuiral Engineering fi: 227- 236. Manthe, D.P., Malone, R.F. and Kumar, 8.1988. Submerged rock filler evaluslion using ad oxygen consumption criterion for closed recirculating sysiems. Aquaculiural Engineering 7: 97-111, Greg 8B, Maguire and G, Nigel R, Forteath, National Key Centre for Teaching and Research in Aquaculture, University of Tasmania, Box 1214, Launceston, Tasmania 7240, Australia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSELIM PRELIMINARY RESULTS FROM ASTUDY OF A CENTRAL QUEENSLAND COASTAL PRAWN FISHERY As pari of an evaluation of seasonal closures. an ongoing. ssudy is being carried out to determine the species composi- lion, spatial and temporal distribution, recruitment, growth, and mortality in the multi-species penseid prawn fishery in the Bowen—Mackay region. Analysis of OFMA and a restricted number af research log books show that tiger, king and banana praws are the domi- nant commercial species ‘groups’ caught in the region, Bananas and tigers are laken in large numbers inshore throughout the region with the kings coming from the ncar reef and inshore at Mackuy.In 1988 and 1989 fishing effort peaked immediately alter the seasonal closure ended and dropped to a very low level by the following December. Results from night-time research trawls show both spatial and inter-annual differences in species composition and re cruimment timing. In January-May 1989 the heer prawns, Penaeus esculentus and P. semisulcatus comprised 4). 3% and 31.4% respectively of commercial species caught at the Bowen site. At Mackay, 100 km to the south, the catch consisted of 60.3% P. esculentus and only 4% P. semisulea- res, Banana prawns #, mereulensis, were caught al borh sites but numbers were highly variable. Western king prawns, P. fetisulcatus, were most abundant off Mackay. Endeavour prawns Metapenaeus ensis and M, endeavouri made up the remainder of the catch at hoth sites. In 1988/89, P. eseulentus displayed a single prolonged recruitment apparently peaking in late spring and summer. P. semisulcatus appeared lo have two recruilment pulses, one im spring and a second jn late summer to early autumn. P. lantsulearus appeared to have ome spring/suramer pulbe while LABORATORY VALUATIONS OF THE EFFECT ON THE EASTERN ROCK LOBSTER, JASUS VERREAUXT (H. MILNE EDWARDS), OF TAGGING WITH EXTERNAL OR INTERNAL TAGS OR MARKINGS Three lypes of anchor tag (Joggle, T-anchor and dart) and a mark (V natch In the right uropod) were assessed under controlled conditions for the effects.of tagging on the mor- talily im custern rock lobsters (Jesus verreauxt) In each of six pens ing 1 x 10°L pool were five lobsters (75-120mm C.L,) from each sex chosen at random, An equal number of untreated lobsters were placed in two remaining pens, After 84 weeks the experiment was lerminaled, The null hypothesis thal there was no difference bétween treatments ia lobster mortality OF tag and mark loss was tested using the y” test. We found no difference in mortality between lobsters that were tagged or marked. The mortality among untagged con- tral lobsters was greater however than thal of he tagged or marked lobslers. There were na differences between external lag lypes in the number of tagged Jobsiers that lost their tag- None of the marked Jobsters lost their mark. We found no differences in apparent mortulily (mortality plus tag loss) between lobsters tagged with different types of external tags. The apparent mortality among marked lobsters was less than that among (hose tagged with extemal taps. In another experiment in thesame pool, 40) lobsters.chosen at random were lagged with visual implant tags and placed 453 P. merguiensis displayed a number of possible recruitment pulses. In 1989/90. the recruitment pulses of all species appeared to be reduced and delayed. Von Bertalanffy growth paramelers have been esilmated for the (wo liger prawn species from tagging studies. The pattem of fag recaptures supgest a slow dispersal rather than definite migration of these prawn. The pattern of fishing cffort as shown tn the research logbooks was relatively even with areas of peak effort matching the areas of highest tag recapture. Further lagging studies ot the king and banana stocks are being carried out at present. Net sclection was investigated using the “allernate haul’ method te compare the 39 mm stretch mesh nets used in the research trawls with both a 19 mm mesh and the commer- cially used 52 mm mesh, A similar technique was used to compare the teseatch beam trawl gear with the industry standard olfer board pear These dala have beon used as parameter estimates for a preliminary vicld per recruit model of this fishery, described in acompanion paper (Dredge and Gribble, 1991), Literature Cited Dredge, M.C.L. and Gribble, N.A. 1991. Evaluation of sea- sonal closures as a moans of optimising yeild from a muln-species prawn fishery, Memoirs of the Oucens- land Museum 34: 451. NA. Gribile. Fisheries Branch, ODPL Fisheries Lebaratory, Gibson Street, Burnew Heads, Queensland 4670, Australia. MCL. Dredge, Fisheries Branch, Southern Fisheries Centre, PO Bax 76, Deception Bay, Queensland 4508, Australia, in a pen adjacent to one containing an equal number af untagged conirals, The experiment was terminated after 48 weeks, The null hypothesis that there was no difference ip mortality between lobsters lagged with visual implant tags or untagged controls was lested using the 7“ lest, Na differences in mortality between tagged and untagged lobsters were found. However. 43% of the tagged lobsters lost their (ag. We concluded that no one type of external tag tested was better than the others, In o field marking experiment we would expect a greater proportion of lobsters tu survive and retain their mark up 10°84 weeks than if wsimilat experiment were done using the types of external tag lesied it our experiment, The visual implant tag has potential especially for experiments under controlled conditions. Hawever, lag- ging techniques need io be improved so that the rate of tzg loss can be reduced. Acknowledgements We are prateful to the Fishing Industry Research and Development Council for funding this work, Dr R. Buckley (University of Washington) pravided us with visual implant tags and demonstrated the lagging technique. 5.5. Montgomery, T.H. Butcher and P. Brett, NSW Agriculrure& Fisheries, Fisheries Research Institute, P.O, Box 21, Cronulla, New South Wales 2230, Avsrralia, MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 454 RECRUITMENT AND STOCK ENHANCE- MENT OF THE CHINESE SHRIMP, PENAEUS ORIENTALIS KISHINOUYE (DECAPODA, CRUSTACEA) Hatchery reared juvenile Chinese shrimp, Penaeus orien- talis, have been restocked into Chinese coastal waters since the early 1980s so as to increase natural stocks, Surveys of the physico-chemical and biological environments have been conducted, to take advantage of natural productivity and resources. The data obtained from Jiaozhou Bay area in the Yellow Sea. during 1981-1988 indicated that the released shrimp grew quickly, migrated out of the Bay to the shallow open sea, and could thus be fished during the autumn shrimp- ing season before the start of the over-wintering migration to the deeper part of southern Yellow Sea. The recruitment of the Chinese shrimp in the Yellow Sea is unimodal (in contrast with multimodality of tropical spe- cies) and occurs from June to September with a peak in July and August. The recruitment in July constitutes over 40-50% of the annual recruitment. The total number of shrimp esti- mated using ELEFAN (Electronic Length Frequency Analy- sis) for August of 1981-1988 was indicative of the annual MEMOIRS OF THE QUEENSLAND MUSEUM stock size and might be used (o evaluate and predict the effects of our restocking experiments. The stock size of the shrimp in the Bay was increased to more than 25,000 (41,500 in 1985) for years of commercial restocking (Table 1), which was about 4.5 times the maximum stock size estimated for non-stocking years (1981). The success of the releasing experiments is also reflected in the 2-4 fold increase of local shrimp catch compared with 1981. The average survival rate of the released juvenile shrimp Was estimated between 32,0-35,6%, Based on these figures and data on biological productivity and availability of natural food organisms (mainly benthic animals), the authors recom- mend that 70-100 x 10° juvenile shrimp be released for Jiaozhou Bay area, Juvenile shrimp have been released in different parts of northern, eastern and southern China Sea based on the find- ings of these and other similar experiments. To date promis- ing resulls have been achieved from these stockings. ALY. Ciu, YA. Cui, F.S. Xu and J.H. Xiang, Institute af Oceanology, Academia Sinica, Qingdao, China, TABLE 1, Density and stock size of Penaeus orientalis in Jiaozhu Bay in August 198]—1988 10° ind. Commercial release 10° ind. Experimental release 10° ind, Avetage density, ind-km- Stock size 14,110 1,335 8.396 66,209 103,716 75,725 5,181 63,125 EFFECT OF DIETARY PROTEIN ON SEXUAL MATURITY AND EGG PRODUCTION IN THE ECONOMICALLY IMPORTANT RIVERINE PRAWN. MACROBRACHIUM NOBILIT The effect of dictary protein on sexual maturity and egg production was studied by feeding juvenile M. nobilii on one or the other of five isocaloric diets containing 10, 15, 25, 35 or 50% prolein for 4 maximum period of 460 days. The juveniles altaimed sexual malurily on atlaining a body weight of 600 mg after 321, 280 and 240 days, when fed on 15, 25, 35 and 50% protein diet, respectively. Thus the high protein diets (>35%) advanced the onsetof maturation. Those fed the 10% protein diet died before reaching sexual maturity. The interspawning period was 45, 33, 24 or 21 days when the prawns were fed with 15, 25, 35, or 50% protein diet respec- tively. During the experimental period, prawns fed a high protein diet underwent § adult moults, carried 5 clutches and produced an average of 4375 eggs. compared to 5 adult moults, 3 clutches and production of 2088 eggs by the group fedon 15% protein diet, Energy content of the eggs produced by the groups fed >35% protein diet was 0.76 J/egg, which is significantly more than thal (0,69 J/egg) spawned by the prawns fed on the 15% protein diet. TJ. Pandian and S. Murugadass, School of Biological Sciences, Madurai Kamaraj University, Madurai 623 O21, India. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM CONSEQUENCES OF THE MORTALITY OF DISCARDED SPANNER CRABS (RANINA RANINA) IN A TANGLE-NET FISHERY — LABORATORY AND FIELD EXPERIMENTS In response to evidence of decreasing catch rates, the effects of disentanglement from commercial tangle-Iraps on the mortality of undersize, discarded spanner crabs, Ranina ranina (Linnaeus), was examined for a fishery in New South Wales, Australia, Firstly, the amount of damage sustained by discarded crabs was quanlified, Three main methods of dis- entanglement were used by commercial fishermen: careful removal, causing no damage; quick removal, where any entangled dactyli are broken off (average 3,95 dactyli per crab); and the fastest method whereby crabs are pulled off and entangled limbs and dactyli are broken off (average 2.9 dactyli and 0.8 limbs per crab), The effects of these various kinds of limb damage on the mortality of undersize R. ranina were tested in an aquarium experiment in which replicate crabs were damaged in the ways described above and com- pared to undamaged controls. In addition, a similar (though @ -211M85 @ 4 DACIYLI © -t DACTYLUS O - CONTROLS PERCENTAGE MORTALITY (5.6) DAYS FIG. 1, Mortality of damaged spanner crabs in aquana, shorter-term) experiment was performed in the field using enclosures buried in the substratum near the commercial fishing grounds. The results showed quite significant rates of mortality due to disentanglement: 60-70% of crabs with one or more dactyli removed died within 50 days, whilst 100% of crabs which lost whole limbs (after being pulled off nets) died after 8 days. The data also show that 75% of crabs that are caught by commercial tangle traps are less than the minimum legal size, and that sexual dimorphism in this species means that 85% of females ate smaller than this legal size. The resulis have implications an the effect of this mortality on subsequent exploitable stocks, the fecundity of the popu- lation, the usefulness of current size restrictions and the need for a better method of capture. Steven J. Kennelly, Fisheries Research Institute, N.S.W Agriculture and Fisheries, PO Box 21, Cronulla, New South Wales 2230, Australia, al un 4 40 o 30 < ~ o = 2 peal U < B 10 U & 2 t= CAREFULLY QUICKLY PULLED OFF REMOVED REMOVED FIG. 2. Mortality of damaged spanner crabs in the field over 24 hours. ALTERNATIVE AERATION SYSTEM FOR INTENSIVE PRAWN PONDS Anallernative aeration system was designed and used for intensive prawn production in the Souther Philippines. Four ponds were used for two crops with a stocking density of 23-39 post-larvae per sq.m, Dissolyed oxygen, salinity and temperature were monitared. D.O. fluctuated from 3.5-10 ppm; salinity from 15-25 ppt, and temperature froma minimum of 27°C to a maximum of 32°C. Readings on nilrales, H2S and ammonia were not taken. Survival rates after 130 days of culture for pond No. 2 were 79% (firs! cropping) and 85% (second cropping). Pond No. 1 had low survival rates due te the failure of the blawer (human error) to operate at the scheduled time. Artificial aeration such as the Air-lift System appears (o be feasible in high inlensive prawn farming. The cost of installation and maintenance appear to be the key io its adoplion- The results of the wo croppings in each pond showed that this artificial aeration system working hand in hand with a good waler system, will give good harvest results. The sys- tem appézrs to be able to maintain a D.O. level above the 4 ppm needed for ideal rearing. Considering the cost of materials, energy (power) con- sumption, maintenance and acquisition costs of major equip- ment, this alternative has great potential for larger scale application in the aquaculture industry. WM. Sanguila, Seafarm Pty Lid, PO Box 166 Cardwell, Queensland 4816, Australia. N.C, Mendoza, Mindanae State University, Department of Marine Science, Philippines. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 436 THE LARVATRON: A COMPUTER CONTROLLED APPARATUS FOR REARING PLANKTONIC ANIMALS Traditionally, workers studying the physical and biologi- cal requirements of plunktoni¢ animals have used manual methods tor feeding the animals and maintaining the specific experimental conditions in each container (Kuban er al, 1985; Diaz, 1987), However when factorial experiments are involved, with large numbers of experimental conditions, there are many problems with this approach. Changing the water, monitoring, and sdding (ood. is labour intensive, and this limits the feasible size of the experiment. There may be prodients in temperature or light intensity within en- vironmental cabinets or water baths, which can cause varia- tion in growth and survival of the experimental animals, Manual handling during walet Changes may myure some animals and contribuie to varfation in results. For these reasons, experimental results cun be variable and difficult lo repeat (Wilkenfeld ef a/,, 1983), Therefore we have developed a method ot automating the ongoing maintenance of larval cultures used in large-scale factorial experiments The new system has the following advantages: minimal labor requirements: no variability due to manual handling: no position effects; and complete flexibility in experimental design, sifice the treatments are specified only by software, All operations of the Larvatron are controlled by a personal computer. The rearing vessels travel around a circular track. driven by an electric molor, One tenth of the culture medium in euch vessel is withdrawn and replaced on each circuit Experimental conditions in each rearing vessel are delined mi a compuler file and (he quiture medium is made up ws it is required foreach resring vessel, with (he appropriate salinity, \emperature and food concentration. Extensive monitoring and error-checking procedures are included in the computer software, This prototype was tested in two experiments MEMOIRS OF THE QUEENSLAND MUSEUM Studying gawih and survival of penaeid larvae, while salin- ity, lemperature, food density and larval density were varied. In tavourable experimental conditions, survival to Mysis I was greater than 80%, In general, variation between repli- cates of 4 treatment was low and significant differences between treatments were evident, Now that the prototype has been tested successfully, we have commenced construction of a full-scale version of the Larvatron, capable of handling 200 experimental culture vessels. Acknowledgements M, Burford provided algal cultures for the experiments; R. Flynn and R, Kaden helped with construction, Literature Cited Diaz. G.G. 1987. Effect of environmental embryonic lempetature on larval development of Macrohrackium eoseabered (De Man). Journal of Experimental Marine Biology and Ecology 114: 39-47, Kuban, F.D., Lawrence, A-L. and Wilkenteld, 1S. 1985. Survival, metamorphosis and growth of larvae from four Penacid species fed six food combinations. Aquaculiare 47:151-162. Wilkenfeld J.S., Lawrence, A.L. und Kuban, F/B. 1983. Rearing penavid shrimp larvae in a smal scale system for experimental purposes’, Proceedings First Inter- national Conference on Warm Water Aquaculiure — Crustacea. Brigham Young University, Hawaii Campus, February 9-11, 1983. ChristepherJ. Jackson, Robert C, Pendrey and Peter C. Rathlisherg, CSIRO Division of Fisheries, PO Bax 120, Cleveland, Queensland 4103, Australia, DEEPWATER FISHERY FOR PRAWNS AND CARIDS OFF WESTERN AUSTRALIA Decpwate? prawns and carids have been fished commer- cially on the continental slope off acrihwestern Australia since 1985, The fishery operates by licence ender a Common- wealth Development Plat. Operating from Port Hedtand and Broome, the fishery (area 490,000 km) includes the waters from the 200 m isobath to the outer Australian Fishing Zone, Fishing ts hy demersal trawlers, with greatest catches in the 400-450 m depth range. Two spectes of earids and four species of penseids are caught, toralling 8501 in the 1987/88 logbook year. The red prawn, Aristaeomorpha faliacea (Decapoda: Aristeidae), dominates the catch in weigh) and commercial value. In 1987/88, 420 | of this species were caught, catch rates were usually between 25 and 75 kg hw! A, foliacea 1s caught in a limited area south of Rowley Shoals, in laree daytime aggregations. The size composition of the catch is being studied Ww determine growth rare and lite span. Males have a petasma which is recognised al >17 mm curapace length (CL); development of sperm ducts occurs at >21 mm CL. Fomale reproductive maturity is marked by the presence Of 4 Sperm plug (at >26 mim CL) and the caudal extension uf the ovarian lobes. Males in fteproductivé condition and females with sperm plugs are present throughout the year. The size-distribution of males is unimodal; that ot females is polymodal, with at least (hree recognisable year-classes. Females usually oumumber males in samples and alsizes >40 mm CL, females dominate the catch. Other commercial species aro disiribuled uver a grealer geographical area than A. foliacea, these include Aristeus virilis and Plesiopenaeus edwardsianus (Aristeidac), Penae- opsis eduardoi (Penaeidae), Haliporoides sibogae australis (Sulenoceridae) and the carid species Heterocarpus slbogae und Meterecarpus woodmasoni (Pandalidac). Deepwater prawn fisheries in other parts of the world use baited traps (¢.8. tropical Pacific Islands) and traw! nets (e.g, off Spain, north-west Africa, laly, and south-west India), By compurison with (hese fisheries, the slope of norlhwestem Australia provides favourable catch rates and a variety of commercial crustacean species. Acknowledgements This research Was funded by FIRDC Grant 88/74, VA. Wedley and S,L. Morris, CSIRO Marine Lahorateries, PO Box 20, North Beach, WA 6020, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM A CALANOID COPEPOD FOR INTENSIVE CULTIVATION Reliable provision of sultatle food for larvae has heen an ubstacle to successful cultivation af many marine fish species (Kahan et al, 1981/82; Bromage e7 af, 488), Small fish larvae require [ood which, as well as being nutritionally adequate and of appropriate size, elicits a feeding response by its active movement. Artificial foods do not, at present. meet all of these criteria (Wanalabe 1988), Nauplii of Ar- femia und some species of rotifers are used us live food lems hut copepods, especially copepod nauplii, may be more suitable for very stall fish larvae. Copepods are probably important natural food items for many fish, they are naturally rich in essential tatty acids (Stottrup ef a@/., LYRA) and ure’ abundant in many parts of the sea, Although cultivation of Marine copepods has been successfully achieved (Klein Breteler and Gonzalez, 1986) the animals aré not widely svailable at low cost. Our work with Gladioferensimparipes suggests that this species ys ideal for intensive low cose cultivation, Animals can be made available as live food, as ccotoxicological test organisms or for research, This contri- bution describes those aspeets of the biolugy of G, imparipes which makes the animal suitable as live food in aquaculture, Gladioferens imparipes is physiologically robust, Popula- hans occur in estuaries of southwestern Australia which are characterized by marked seasonal changes in sulinity and conspicuous vertical salinity discontinuities, Vigorous popu- lations. can occur both at low salinity (2 ppt) and in hypersa- line conditions (38 ppt.) and in the full range of temperatures (12-28°C) which occur In these estuaries. In culturing these animals, there is no need to maintain physical conditions within close limits. Wo have deliberately changed the salinity of our cultures trom 35 ppt to 5 ppe to rid the cultures ol harpacticoid copepods and we regularly separale G. un- paripes from other estuarine fauna by exploiting this toler- ance of rapid salinity change. G, imparipes feeds by fillering phytoplankton from water fn their natural estuarine habitat dense populations of the copepod follow high phytoplankton productivily when the seasonal run off ceases. In the laboratory, our copepod cul- twres have thrived on various small phytoplankton species which wre easily mainiained We have successfully used strains of yochrysts sp., Pavlova sp,, Phacodacn lum tricer- neufum and several unidentified estuarine species as food, Dense copepod cultures fapidly clear algal cells from the walter and cultures thrive if algae are added twice daily at densities such thal waler is cleated in u few hours and few old algal cells remain to contribute to teduction of water quality. G. imparipes is capable of rapid population growth This is typical of ecological pioneer species which exploit newly available resources, AL 22°C. females are able to reproduce c, 14 days after hatching, They then produce eve masses of 25-45 eggs al intervals of 2-4 days. Reproductive activity is affected by temperature and fond availability, beth of which can be easily manipulated in the laboratory. G, imparipes have been maintained in aur laboratory trough 28 generations in 18 months, Comparisons berween animals bred for 18 generations in the laboratury and firs| penerulion laboratory animals showed no diminution of re productive activity but a slight reduction in age at matunty for the 18th goreralion animals. 457 G, imparipes eggs are curried by females until mauplls hatch. An egg carrying female presents both a conspicuous visual larget und @ valuable food ilem io @ predator. For animals in cultiwation, We hyve developed s quick method for determining whether a population ts reproducing fo capacity, An index uf fecundity is obtwined by examining abou 15 living females and giving cach a score based on presence ur absence of an egg mass, size of the epg mass and Whether or fot (he ulérus is full of eggs. The index of fecundity hax been shown to relate closely tothe level ot food provided and therefore permiis us to'adjusi rations by bio- logical crileria. G, imparipes Naupli exhibit moderately strong photolactic behaviour, We have designed a trap to regularly remove nauplii from our culture containers. Nauplii are attracted oa a point source of light aad then removed [rom the cullure by siphon, An arrangement of air lift pumps and time swriches permits regular muitomalic Operation af (he nauplius trap. We have recorded duily production in excess of 20,000 nauplii from a 15 litre culture, G. imparipes nauplii have a mean body length of 128.5um on hatching. They grow through nauplius and copepodile slages lo ¢, BOO metasome length when mature. We have shown that nauplii can be taken as food by Dolphia fish (Coryphaena hippurus) and we have grown Sea Horses (Hippocampus angustus) (rom hatching to 40mm using, nau- plii, then copepodites and adults.as food, tris likely thatenher fish species would grow successfully on the same diet G. imparipes is ideally suited for relatively low cost inien- sive Cultivation and may, therefore, be useful in marine fish aquaculture, Achauwhergements Use of facilities at Curtin Universtiy of Teetnaligy is acknowledged. Literature Cifed Bromage, N.R,, Shepard, CF and Roberts, J, 1988, Farming systems and hisbandty practice, 50-102. In C.J. Shepard and NR, Bromape (eds) ‘Intensive Tish farming’, (BSP Professional Buoks: London). Kahan, D., Ublw, G., Schwenzer, D. aml Horowite. L. 1941/2. A-simple method for cullivating barpactiguid copepods and offering them tu lish larvae, Aquaculture 26. 303-310. Klein Breteler, W-C_M-and Gonzalez, $.R., 1986, Culture and development of Temora longicornis (Copepoda, Calanoida) at different conditions of temperature and food. In G. Schniever, H.K. Schminke and C.-t, Shih (eds) ‘Proceedings of the Second Intemational Confer- ence on Copepoda’. Onlawa. Canada, 1984, National Museums of Canada, Ottaws, Stolp, 1G. Richardson. K., Kirkegaard, £. and Pihl NJ. 1986, The Cultivation of Acariia tonsa for use asa live food source for fish larvae. Aquaculture 52: 87-96, Wanatabe, T. 1988, Nutrition anc growth, 154-197, In CJ, Shepard and NR. Bromage (¢ds)' Intensive fish tarm- ing’. (BSP Professional Books: London). RI, Rippingale and M.G, MacShane, School of Biology, Curtin University of Technology, Kemt Streets, Bentley, Western Australia 6102, Austratia MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 458 EFFECT OF ESSENTIAL AMINO ACID SUPPLEMENTATION OF CASEIN AND SARDINE POWDER ON THE PROTEIN REQUIREMENTS OF THE PRAWN, PENAEUS JAPONICUS Protein requirements of the prawn Penaeus japonicus has been extensively studied using purified diets based on casein (Deshimaru and Yone, 1978; Teshima and Kanazawa, 1984), but little work has been done on the essential amino acid balance required by prawn. Application of information on protein requirements to commercial practice will require an understanding of the effects of amino acid balance in the diet on growth. The present study investigates the effects on prawn growth of supplementing sardine powder and casein with essential amino acids. Material and Methods Seven purified diets containing varying levels of sardine powder, casein and crystalline amino acids were prepared. Diet 1 (control) contained 50% casein and a total of 53% amino acid. Diets 2, 3 and 4 contained 40, 35 and 30% casein, and this was adjusted to 50, 45 and 40% total amino acid tespectively using essential amino acids. Diets 5, 6 and 7 contained 50, 45 and 40% sardine powder and were adjusted to 50, 45 and 40% total amino acid respectively. Amino acids were added individually to adjust the essential amino acid profile of the diet to that of a standard diet based on the composition of prawn muscle. All diets contained 8% gluten- M and 3% CMC as binders. There were two replicates. Twenty juvenile prawns of 0.41-0.52g body weight were placed in 30L tanks with a recirculating salt water system. Water was maintained at 25+1°C and aerated continuously. Prawns were fed twice daily with a dry diet at 5—10% of body weight. Results and Conclusion Weight gain was increased (P<0.05) by supplementing the casein with essential amino acids (0.28g, 0.38g and 0.44¢ in MEMOIRS OF THE QUEENSLAND MUSEUM groups 4, 3 and 2 respectively), and by the lowest level of supplementation of sardine powder (0.36g) (Table 1). With the lower levels of sardine powder weight gain (0.20g) was less than for the control diet (0.27g). Food efficiency ratio was higher with the high level of amino acid supplemented diets, 0.27 in diet 2 and 0.25 in diets 3 and 5. Results showed a linear increase in the food effi- ciency ratio with level of total amino acids (r=0.98 and 0.97 in casein and sardine powder groups respectively). Protein efficiency ratios were increased by amino acid supplementation and were higher for diets based on casein (0.44, 0.48, 0.44 in groups 2, 3 and 4) than for those based on sardine powder (0.41, 0.29 and 0.20 in groups 5, 6 and 7). We conclude that growth was higher on casein than on sardine powder based diets. Addition of essential amino acid to diets containing casein and sardine powder increased the weight gain of prawns. The addition of essential amino acid improved the quality of the diet as measured by the food and protein efficiency ratios. Literature Cited Deshimaru, O. and Yone, Y. 1978. Optimum level of dietary protein requirement for prawn. Bulletin of Japanese Society of Scientific Fisheries 44(12): 1395-1397. Teshima, S. and Kanazawa, A. 1984. Effects of protein, lipid and carbohydrate levels in purified diets on growth and survival rates of the prawn larvae. Bulletin of Japanese Society of Scientific Fisheries 50(10): 1709-1715 H.Z. Sarac, Queensland Department of Primary Industries, Bribie Island Aquaculture Research Centre, P.O. Box 191, Bribie Island, Queensland 4507, Australia. A. Kanazawa, Kagoshima University, Faculty of Fisheries, Shimoarata, 4-50-20, Kagoshima 890 Japan. TABLE 1. Weight gain, food intake, food efficiency and protein efficiency ratio of the prawn, Penaeus japonicus as affected by protein source and essential amino acid level. Increase in Body (g) Food Efficiency Protein Efficiency g/prawn Ratio Casein 1(Control) 2 3 4 Sardine Powder 2 6 7 MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM ASPECTS OF THE BIOLOGY OF COMMERCIAL PENAEID PRAWNS IN TORRES STRAIT The Torres Strait Project, which is funded by the Queens- land stale government, was initiated in July 1985 to investi- gale the movement and distribution of the commercial prawn Species in Torres Strait and lo assess seasonal and area closures to ensure thal they are being applied in the most effective way. The findings of the research project are of international importance as the Torres Strait prawn fishery is jointly fished and managed by Australia and Papua New Guinea. Data from monthly otter and beam traw! samples taken between January 1986 and December 1989, and prawn lag- ging, are being used to investigate the life cycles of the brown liger (P. esculentus), endeavour (M. endeavouri) and red spol king (P. longistylus) prawns in Torres Strait, Due to tidal constraints in Torres Strait it was necessary to Use a daytime water jet beam trawl to sample the seagrass nursery areas on the Warrior Reefs. An unusual feature of the Torres Strait prawn fishery is that the juvenile seagrass nurseries are located on coral reef platforms (mainly the Warrior Reefs) rather than coastal estuarine mud-flats. Data indicate that brown tiger prawns move off the sea- prass nurseries on the Warrior Reefs into the shallow silty waters to the west of the reefs, ata very small size, then grow and migrate from the closed area west of the Warrior Reefs, eastward into the fishery. Spawning in brown tiger prawns in Torres Strait occurs year round with three distinct peaks of activity that vary considerably in intensity and duration between years. The yearly spawning pattern produces a series of age classes within each year that results in a complex pattern of recruit- ment into the fishery. Due to the complexity of the recruit- 459 ment pattern it is difficull to sel an optimal seasonal closure period. As the fishing fleet is highly mobile, a difference in closure timing (o thal in other areas could result in an extreme ‘pulse fishing’ effect that may negate any beneficial effect of the closure. Industry believes that the seasonal closure in Torres Strait opened (oo late this year thus missing the main recruitment into the fishery. Catches have been much lower than usual this year. Brown tiger prawns tagged in a closed area to the west of the fishery, moved to the eastern side of the fishery before being recaptured. This indicates that the season may have opened later than the optimal time to harvest that particular pulse of recruiting prawns. Data indicate that areas with high densities of undersized prawns are restricted to the western side of the fishery so an extension of the area closures may be a more appropriate management strategy than a total area seasonal closure. The whole system of area and seasonal closures for both Torres Strait and the east Queensland Coast are currently being reviewed at meetings involving representatives of industry, management and research. Future research will be aimed at inyestigating spawning and recruitment patterns of endeavour and red spot king prawns and using fisheries simulation models to assess various closure strategies for the Torres Strait fishery, The findings of the first three years of the project are detailed ina ODPI Information Series publication, 0190018, titled ‘Torres Strait Prawn Project: A Review of research 1986-88", Editor J.B. Mellors. C.T. Turnbull, Fisheries Branch, Queensland Department of Primary Industries, Northern Fisheries Centre, Box 5396 Cairns Mail Centre, Cairns, Queensland 4871, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum 460 THE FISHERY FOR ANTARCTIC KRILL (EUPHAUSIA SUPERBA) The catch of Antarctic krill in the Southern Oveun in 1989/90 was 395,470 tonnes. This represents 83% by weight of the total catch of all marine species from Antarctic witters: makes the operation for Antarctic krill the world’s largest single-species crustacean fishery; and puts the krill harvest among the world’s tap 30 fisheries by tonnage (FAO 1989). Antarctic krill are currently being caught predominantly in the Atlantic sector of the Souther Ocean: the Antarctic Peninsula, South Georgia and the South Orkneys but the area of operation of the krill fleets is likely to expand in the near future. Fish aré still being caught in the South Georgia, Antarctic Peninsulaand Kerguelen Island regions bul catches are low (104,405 tonnes in 1989/90) due to over-tishing, The krill fishery has displayed considerable catch fluctuations bul is likely to be the mainstay of the Southern Océan fishery in the foreseeable future. Estimates of the stock size of Antarctic krill range beiween 55 and 7000 million tonnes (Millerand Hampton, 1989), The krill population is circumpolar though certain areas are richer in krill than others. Evidence to date suggests that the krill population is not separated into stocks (Fevolden and Schneppenheim, 1989). The Soviet Union which has more than 100 large (9Um+) freezer trawlers operating in the Southern Ocean accounts for 76% of the krill catch. Japan takes 20% of the krill and Poland, S. Korea and Chile are responsible for the other 4%. Some additional countries may enter the fishery il the economic climate becomes favourable. Antarctic krill is caught in mid-water |rawls and processed on board freezer trawlers. Catches of between 3-10 tonnes per hour are dimed for lo ensure product quality and to avoid swamping the processing capacity of the vessel. Areas with eatch rates Of less than 50 tonnes per day are avoided. Krill spoil rapidly because of active proteolytic enzymes and are unfit for human consumption unless processed within 3 ours of capture, After 8 hours they are unfil for use in animal feed, Over 50% of the krill catch js now used for human consump- tion. Same of the Japanese catch is frozen whale and some is boiled then frozen. Most of the catch is peeled then frozen. Krill shells are extremely rich in fluoride and this migrates oul of the shell and into the flesh on death (Christians and Leinemann, 1980). Whole krill have very high Muoride levels because of this — upto 1800 ppm 4 times the EEC atlowable limit for animal feed — so peeling is the best approach to obfain a quality product, The yield of tail meat from krill produced by roller peelers is 10-25% of the wet weight of whale krill (Budzinski et a/,, 1985), Meal is produced from ‘the enecss low-quality krill. Consideration is being given to processes which can utilise MEMOIRS OF THE QUEENSLAND MUSEUM the waste material from the krill fishery. Valuable hy-pro- ducts which could be extracted from krill waste include; carolinoid pigments, chitin, proteolytic enzymes and vi- famins. The fishery is currently only marginally economic and the extraction of high value chemicals from krill wiste may increase the worth of the krill catch and encourage new entrants to the fishery (Nicol, 1989). Exploitation of the resources of the Southern Ocean is controlled by the Commission for the Conservation of Ant- arctic Marine Living Resources (CCAMLR) which meets annually in Hobart, Tasmania. Hs 20 members include all the nations involved in fishing in the Southern Ocean and all the Antarctic treaty signatories. CCAMLR first met in 1982 but it was not until the 1989 meeting of CCAMLR that manage- ment of the krill fishery made it onto the agenda. Manage- ment of the krill fishery is necessary since krill occupy the pivatal role in the Antarctic ecosystem and over-exploitation could have disastrous results. The information required to scientifically manage the krill harvest is not vet available. In ihe absence of such information it should still be possible to protect krill and their predators by introducing interim catch limits. Al present (hese limits could be set high enough that the fishing nations would have considerable room for expan- sion yet low enough that the Southern Ocean ecosystem would remain undamaged. Whether krill can be the first successfully managed fishery resource in the Southern Oceun will depend on the negotiations over management plans (hut lake place over the next few years. Literature Cited Budzinski, E., Bykowski, P. and Dutkiewicz. D. 1985. Possi- bilines of processing and markeling of products made from Antarctic krill, FAO Fisheries Technical Paper 268: 1-46. Christians, O. and Leinemann, M. 1980. Untersuchen uber fluor im krill (&, superba). Information fuer die Fischwittschatt & 254-260. FAO, 1989, FAO yearbook: Fishery statistics, catches and landings 1987. #4: 1-490. Fevalden, 8.E. and Schneppenheim, R. 1989. Genetic homo- geneity of krill (Euphausia syperba Dang) in the South- ern Ocean. Polar Biology. 9; 533-539, Miller, D.G.M-. and Hampton, I. 1989. Biology and ecology of the Antarctic krill (Euphausia superba Dana): a te- view, Biomass Sci. Ser. 9: 1-166. Nicol, $8. 1989. Who's counting on krill. New Scientist 1690; 38-41. Stephen Nicol, Australian Antarctic Division, Kingston, Tasmania 7050, Australia. MEMOIRS OF THE (QUEENSLAND MUSEUM BRISBANE © Queensland Museum PO Box 3300, South Brisbane 4101, Australia Phone 06 7 3840 7555 Fax 06 7 3846 1226 Email qmlib@qm.qld.gov.au Website www.qm.qld.gov.au National Library of Australia card number ISSN 0079-8835 NOTE Papers published in this volume and in all previous volumes of the Afemoirs of the Queensland Museum maybe teproduced for scientific research, individual study or other educational purposes. Properly acknowledged quotations may be made but queries regarding the republication of any papers should be addressed to the Editor in Chief. Copies of the journal can be purchased from the Queensland Museum Shop. A Guide to Authors is displayed at the Queensland Museum web site A Queensland Government Project Typeset at the Queensland Museum MEMOIRS OF THE QUEENSLAND MUSEUM AN ALTERNATIVE STOCK MANAGEMENT FOR SNOW CRAB, CHIONOECETES OPILIO (BRACHYURA, MAJIDAE), BASED ON THE PRESENCE OF A TERMINAL MOULT The snow crab, Chionoecetes opilio, is the most important commercial crab in Canada. In the southern Gulf of St Lawrence, the landings decreased drastically from 32.0001 in 1982 to 7880 1 in 1989, al which point the fishery was prematurely closed due toa high incidence of newly moulted ‘white’ crabs in the commercial catch. The description of a terminal moult in male as well as female crabs (Conan and Comeau, 1986) has generated a new interpretation of the life cycle of the species, This. new knowledge has important management implications for re- building the commercial potential of the stack. In the Gulf of St Lawrence, processors rely on hard shell terminal moult males which moulted one year or more prior to the short ten week fishing season. At an early state of exploitation, most individuals captured in the southern Gulf were inthe terminal moult phase. The catch resulted from the accumulation of 3 to 4 year classes of the terminal moult crabs. As the fishery developed, old terminal moult males were fished out and the proportion of individuals which had tecently moulted immediately prior lo the fishing season increased in the commercial catch. These recently recruited (called ‘whites’ by the fishermen) have a low commercial value and are mostly discarded at sea with a subsequent high fishery induced mortality. The harvest became based almost entirely on annual recruitment of newly moulted terminal moult individuals, Such a catch would have beer ultimately of low commercial processing quality and extremely sensi- tive to annual fluctuations of recruitment. The newly discovered patterns of life history are now being used for designing management strategies of the fish- ery. Newly moulted mules have no chance to mate before a complete hardening of their carapace. The mating of terminal moult males with hard shell multiparqus females takes place shortly after the spring moulting season and at the beginning 461 of the spring and early summer fishing season, therefore only the males which reached the terminal moult one year earlier can male efficiently. Management strategies were designed for avoiding the harvest of recent moulters, The catch would be optimised both in terms of yield per recruit and quality if only the males which have reached the terminal moultat least 12months earlier were harvested. This can be achieved cither by using traps selectively inaccessible to the less aggressive non terminal moult males, or by introducing a gauge identi- fying terminal moult males asa function of allometry of their larger claw size respective to carapace size. Using geostatistical mapping techniques subareas likely to contain high densities of recently moulted males can be identified during a prefishing period survey, The geographic concentrations of recently moulled males frequently differ from the concentrations of hard shell ones and specific zones can be closed selectively prior to the fishing season in order to protect the recent moulters. In order to rebuild the stock and stabilise the commercial landings, the protection of the annual recruitment of soft shell crabs as well.as catch limitations of hard-shell terminal moult crab are required, Tt appears that an age group reaches the terminal moull over a series of successive years, A major, still unresolved issue is to determine whether a non terminal C. opilio will opt for the terminal moult over a moult period. The answer would have major implications for management since many crabs reach terminal moult at a size smaller than the existing minimal legal size. Literature Cited Conan, G.¥. and Comeau, M. 1986. Functional maturity and terminal moult of male snow crab Chionoecetes opilio, Canadian Journal of Fisheries and Aquatic Sciences 43(9): 1710-1719. M. Moriyasu and G.Y. Conan, Science Branch, Department of Fisheries and Oceans, Monoton, NB. Canada,