The Journal
OF Research
ON THE LEPIDOPTERA
Volume 42 2003 (2010)
ISSN 0022 4324
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journal of Research on the Lepiilojjlera
42: 1-4, 200.4 (2010)
Differences in thermal responses in a fragmented landscape; temperature
affects the sampling of diurnal, but not nocturnal fruit-feeding Lepidoptera
Danilo B. Ribfjro' - and Andre V. L. Freitas'**
'De|)artamento de Zoologia, Iiistituto cle Biologia, Univer.sidade E.stadiial de (4ini|jinas. (4’ 6109, 14083-970 Oampinas, SP. Brazil, tel.
-t-+.6.5 19-452 16.3 10
-Prog'iama de Po.s-Giadiiagao ein Ecologia, hi.sliluto de Biologia, Uiiiversidade Estadual de (’.anipinas, Brazil.
hlo(lhr@yahoo. com.br
-’DepartanieiUo de Zoologia, In.stiiuto de Biologia, Univer.sidade Estadual de Cam|tinas. UP 6109, 1,3084-970 Uainpinas, SP, Brazil, tel.
+-r55 19-452 16.3 10
Ab.stract. Weather is the primary determinant in hiittei lly activity, with tem|3eralnre one of the
key factors affecting the hiolog)’ and behavior of most Lepidoptera. Despite et idence about the
inllttence of temperature in Lejtidoptera capture jtatterns, few stttdies have analyzed microclimatic
characteristics. Most studies focused on broad geographic scales and historical climatic jtatterns.
The present stitdr contrasts the effect of local temperature on the capttire rates ol two groups of
ft iiit-feeding Lepidoptera, btttterllies (dittrnal) and noctuid tnoths (noctttrnal), iti a fragmented
landscape. Ten fragments with live traps each were sampled in sotttheast Brazilian Atlantic Forest
dttring eight days iti |tily-2005. We fotmd a jtositive relation between mean tem|teratiire and both
richness and abundance of captttred butterflies, but not the noctnid moths. These difleretices are
jtrobably a result ol the miothermic natttre of moths, making the moth assemblage less dependent
of solar radiation than butterflies. 4'he differences between moths and htittei flies coitld affect the
distribittion of these insects across fragmented latidsca|3es and sttggest that adult moths are |)robably
less sensitive to changes in the amottnt of solar radiation than adtilt btitlerflies,
Key word.s: frtiit-feeding btitterllies, Nym|3halidae, Noctitidae, temperatitre.
Introduction
Ehrlich (1984) stated that weather is the [triinary
determinant in btitterfly activity. Temperature is a key
factor affecting most Lepidoptera because it has direct
effects on larval behavior and performance, flight
activity and associated behaviors such as foraging
and territoriality (Broersma et al., 1976; Scriber &
Slansky, 1981; Hrdy el al, 1996; Shirai el al., 1998;
Kiilirt et al., 2005; Nabeta et al., 2005; Merckx et al.,
2006). Many btitterfly species are able to maintain
their body temperattire above ambient through
basking and/or shivering behaviors (Kemp, 2002),
such that individuals with higher body temperatnres
can be active for longer periods than their cooler
bodied counterparts (Dudley, 1991). On sunny days
some butterflies have been reported to fly for longer
periods and maintain higher body temperatnres than
on cloudy days (Shelly & Ludwig, 1985). Temperattire
*■ Corresponding author. Departamento dc Zoologia, In.stiluto cle
Biologia, L'niversidacle E.stadual de Ciampina.s. C.P 6109, 14083-
970 Campina.s, SP, Brazil, tel. -1+5519-35216310
baku@unicamp. br
Rereived: 5 March 2009
Accepted: 6 March 2009
is also known to affect the seasonal dislribtition
of some species (Turner et al, 1987), probability
of capttire in temperate regions (Yela &: Holyoak,
1997; Holyoak et al., 1997), and the abundance and
diversity patterns of both butterflies (Turner et al.,
1987; White & Kerr, 2007) and moths (Brehin et al,
2007; Choi, 2008).
Despite the evidence that ambient temperature
influences activity patterns in Lepidoptera, few
studies have analyzed the effect on a microclimatic
scale (e.g. Yela & Holyoak, 1997) . Most have focused
on broad geograjihic scales and historic climatic
patterns (e.g. Brown Sc Freitas, 2000; Menendez et al,
2007). However, anthropogenic activity is known to
prodtice major changes in microclimatic conditions
(Saunders, 1991; Vitonsek et al, 1997) which likely
in turn could affect the insects that occtipy a given
habitat.
Accordingly the present study attempts to test the
effect of local temperature in the capttire rates of
fruit-feeding butterflies and moths in a fragmented
landscape. Here we ask whether there are differences
in the responses of diurnal versus nocturnal
Lepidoptera to average temperature, linking
the possible differences with the effects of forest
fragmentation among these two sets of insects.
/. Res.Lepid.
0
D
m
0
Richness Abundance
Figure 1. Linear regressions between temperature and species richness and between temperature and abundance for both
butterflies and moths sampled with baited traps in a fragmented landscape in Brazilian Atlantic Forest, a) Linear regression
between mean temperature and richness of fruit-feeding butterflies; b) linear regression between mean temperature and
abundance of fruit-feeding butterflies; c) linear regression between mean temperature and richness of bait attracted moths; d)
linear regression between mean temperature and abundance of bait attracted moths.
Materials and methods
Field work was carried out in the Sao Liiiz do
Paraitinga municipality (Fig. 1), Sao Paulo State,
south-eastern Brazil (centered in 23°20’ S, 45°20’ W).
The original vegetation of the area was mainly a dense
humid forest (MME 1983); however, the process of
forest fragmentation drastically changed the plant
community cover across the region (Schmidt, 1949;
Petrone, 1959; Dean, 1997). Today, large parts of the
native vegetation has been removed with the resulting
landscape now being composed of small patches of
disturbed forest scattered in a matrix of farm fields
and abandoned pastures and including some patches
of Eucalyptus plantations.
Ten forest fragments were chosen at random for
sampling. In each fragment, five traps were arranged
along a linear transect for a total of 50 traps. Detailed
information of sampling methods and the study site
are given in Ribeiro ct al. (2008).
Butterflies (diurnal) andiioctuid moths (nocturnal)
were sampled during |une 2005. The traps remained
in the field for eight days and were visited at 48-hoiir
intervals. During each visit bait was replaced and
each captured individual was identified, marked and
released. Species not determinable in the field were
taken for later identification (following Ribeiro et at,
2008). All butterflies were identified to species level
and the moths (all Noctuidae) were discriminated as
morphospecies.
Ambient temperatures were measured with a niax-
min thermometer at each visit. The arithmetic mean
of the maximal and minimal temperature measured
during the period between visits (48 hours) was used
as mean temperature.
We use simple linear regression to test if there was
a relationship between abundance and richness of
butterflies and moths with mean temperature.
Results
A total of 233 individuals comprising 27 species
of fruit-feeding Nymphalidae and 475 individuals of
nine morphospecies of noctuid moths were captured.
42: 1-4, 2003 (2010)
3
The mean temperatures recorded during tlie study
period ranged between 1 1.5 and 21.()°(1. We found a
significant relation between mean temperature and
species richness (p < O.OOOl; R- = 0.362; N = 40; y =
0.2481x+ 14.84) (Fig. la) and individual abundance (p
< 0.0001; R" = 0.362; N = 40; y = 0,2481x + 14.84) (Fig.
lb) in our butterfly samples. In contrast, we did not
find a significant relation between mean temperature
in either richness (p = 0. 581 1; R- = 0.0084; N = 40; y =
-0.1608x+ 16.599) (Fig. Ic) or abundance (p = 0.8936;
R2= 0.0004; N = 40; y = -0.0079x + 16.094) (Fig. Id) of
the moth samples.
Discussion
We found a strong relation between microhabitat
temperature and richness and abundance in samples of
diurnal, but not nocturnal noctuid Lepidoptera. The
relation between butterfly capture and temperature
is likely the result of differences in daily activity of the
diurnal set of species compared with the nocturnal
noctuids. Despite the great variety of behaviors related
to thermoregulation in butterflies (Clench, 1966),
air temperature remains important in determining
butterfly activity (Douwes, 1976). Tbus we would
expect greater butterfly activity and capture rate
on hot rather than in cold days. Although weather,
especially temperature, is usually considered the most
important factor determining butterfly and moth
diversity (Holyoak et al, 1997; Yela & Molyoak, 1997;
Hawkins & Porter, 2003; Brehm et al., 2007; Menendez
et al., 2007; Choi, 2008), few studies demonstrate
significant relations between microhabitat conditions
with species richness and abundance of Lepidoptera
(e.g. Yela & Holyoak, 1997; Doha et al, 2008).
The differences found in diurnal versus nocturnal
fruit-feeding Lepidoptera are likely the result of the
latter being miothermic and therefore independent
of solar radiation to enable their activities (Daily &
Ehrlich, 1996). If the conclusion is correct, we would
expect that butterflies in the subfamily Brassolinae
should respond similarly to nocturnal moths, since
brassolines are not as dependent upon solar radiation
as other butterflies are (Siygley, 1994).
The degree of fragmentation has significant
influence on microclimatic conditions, as temperature,
humidity and amount of solar radiation (Saunders,
1991), with many studies of diurnal fruit-feeding
Lepidoptera reporting changes in the community
correlated with forest fragmentation (Ki'auss et al,
2003; Shahabuddin & Ponte, 2005; Uehara-Prado et
al., 2007). The change in microclimatic conditions
also affects the distribution of butterflies in forest
fragments, probably because fragmentation impacts
the activity of these insects by being beneficial to
heliophylous species that are more likely to displace
shade-loving species. Another important alteration
caused by microclimatic changes in temperature is
the effects upon life-history traits of butterflies by
changing daily fecundity and lifetime number of eggs
of females (Ktirlsson & Van Dyck, 2005) . However, the
same effect may be less important in moths because
they are not directly influenced by solar radiation
(Daily & Ehrlich, 1996) and suffer only the indirect
effects of the changes (e.g. alteration in leaf quality,
resource offer and so on).
Both .sample richness and abundance are positively
correlated with mean temperature in the present study.
Since trap capture is considered as a reliable measure
of activity and density in fruit-feeding Lepidoptera, we
can conclude that temperature had an undeniable
effect in butterfly richness and abundance. I lowever,
in view of the great importance of temperature in
determining the behavior and distribution of diurnal
Lepidoptera, other studies are necessary to verify if
this relation could be found in other habitats, with
different climates and land covers.
Acknowledgements
We es|)ecially thank ('.aria Pen/, and Niklas Walilberg lor
critically reading and connnenting tt]>on oitr mamtscript. W'e
also tliank tlie severtil land owners who permitted held work on
their |jroperties. DBR thanks FAPKSI’ tor ;i tellowship (grants
#03/ 1 1697-0, 07/.5089(>0). AVLF acknowledges the FAPESP (grants
#00/01484-1 and #01/05269-9), the Bra/ihan CNPq (lellowshi])
#300315/200.5-8), and the National Science Foundation (DEB grant
#0527441 ). This project is part ol BIOTA-FAPFSP program (grants
#98/05101-8 and #02/08558-6).
Literature cited
Bruim, G., R. K. Cot.WF.t.i. & J. Ki.uca;. 2007. The role otenvironment
and mid-domain ef fect on moth species richness along a tropical
elevational gradient. Globtil Ecolog)' and Biogeographv 16:
20.5-219.
Broersma, D. B., J. R. Barreei', & J. O. Sit.i.iNcs. 1976. Activity
and blacklight induced flight of black cutworm Le])idoptera-
Noctnidae and European corn-borer L.epidojttera-Pyralidae as
related to temperature and relative httmidily. Environmental
Entomolog)’ 5: 1 191-1 194.
Brown, K. S. Jr & A. V. L. Freit.vs. 2000, Atlantic forest hntterllies:
iiulicators for landscape consen'ation. Biotropica 32: 934-956.
Ciioi, S. W. 2008. Diversity and com|)osition of larger moths in
three different forest types of Sottthern Korea. Ecological
Research 23: 503-509.
Ci.ENCH, H. K. 1966. Behavioral thei inoregnlation in btitterflies.
Ecolog)' 17: 1021-10;34.
Daii.v, G. C. & P. R. EiiRt icii. 1996. Noctiimality and species
sttn'ival. Proceedings of The National Academy ol Science 93:
11709-11712.
Dean, W. 1997. A ferro e logo. A histdria e a devasttigao da Matti
Atlantica brasileira. Companhia das Letras, Sao Patilo.
Dot.tA,J., M. S. Dew, N. A. Ar,\vind& A. KfMAR. 2008. Adult butterfly
4
J. Res.Lepid.
coniinunities in ct)free plantations around a protected area in
the Western C'.hats, India. Animal Clonservation 1 1: 2t>34.
Douwes, I’. 1976. Activity in Heodes virgaurear (Lep., Lycaenidae)
in relation to air temperature, solar radiation, and time of day.
Oecoloo-ia 22: 287-298.
Duni.iiV, R. 1991. Thermoregulation in unpalatable Danaine
butterllies. Functional Ecology .'5: .503-506.
EiiRMOii, P. R. 1984. The structure and dynamics of butterlly
populations. Pp. 16(>2()I. hr. Vane-Wright, R. I. & Ackeiy, P. R.
1984 (Eds.). The biology of butterflies. London, Academic
Press Inc., 430 p.
Hawkins, B. A. & E. E. Porter. 2003. Does herbivore diversity
depend on plant diversity? The case of Clalifornia butterflies.
The American Naturalist 161: 40-49.
Hoi.voak, M., V. |arosik& I. Novak. 1997. Weather-induced changes
in moth activity bias measurement of long-term population
dynamics from light trap samples. Entomologia Experimentalis
et Applicata 83: 329-335.
Hrdy, I., F. Koc:ot'REK, J. Berankova, & j. Kuldova. 1996. Temperature
models for ]>redicting the flight activity of local populations of
Cydia fiinebmna (Lepidoptera: Tortricidae) in Central Europe.
Euro]>ean Journal of Entomology 93: 569-578.
K,\ri.s,son, B. & 11. Van Dyck. 2005. Does habitat fragmentation
affect temperature-related life-history traits? A laboratory test
with a woodland butterlly. Proceedings of The Royal Society
B. 272: 12.57-1263.
Kemp, D. L. 2002. Visual mate-searching behaviour in the evening
brown butterfly, Melanilisleda (L.) (Lepidoptera: Nymphalidae).
Australian Journal of Entomolog)' 41: 300-305.
Kraii.ss, j., I. Stefan-Dewenter & T. T.sc:harntke. 200.3. How does
landscape context contribute to effects of habitat fragmentation
on diversity and po]>ulation density of butterllies? Journal of
Biogeography .30: 889-900.
KOhre, Lh, J. Samietz&S. Dorn. 2005. Thermoregulation behaviour
in codling moth larvae. Physiological Entomology 30: 54-61.
Menf.ndez, R., a. GoN7,.Ai.E7,-ME(a.A.s, Y. Coi.i.iNOM.AM, R. Fox, D. B. Roy,
R. Ohef.mui.ler & C. D. Thomas. 2007. Direct and indirect
effects of climate and habitat factors on butterfly diversity.
Ecology 88: 60.5-61 1 .
Merc.kx, T, B. KARi.ssftN & 11. Van Dyc:k. 2006. Sex- and
landscape-related differences in flight ability under suboptimal
temperatures in a woodland butterfly. Functional Ecology.
20: 4.36-441.
MME-Minksterio 1),\.s min.as e enercta. 198.3. Projeto Radam Brasil.
Programa de Integrayao Nacional. Levantamenlo de Recursos
Naturals, Vol. 32. Publication Division, Rio de Janeiro.
N.abeta, F. H.. M. Naiv\i & Y. Kunimi. 2005. Effects of temperature
and photoperiod on the development and reproduction
of Adoxophyes liotimni (Lepidoptera: Tortricidae). Applied
Entomology and Zoology 40: 231-2.38.
Petrone, P. 1959. A regiao de Sao Luiz do Paraitinga: estudo
de geografia luimana. Revista Brasileira de Geografia 21:
239X336.
Ribeiro, D. B., R I. Prado, K. S. Brown Jr., & A. V. L. Freitas.
2008. Additive partitioning of butterfly diversity in a
fragmented landscape: importance of scale and implications
for consen,'ation. Diversity and Distribution 14: 961-968.
Saunders, D. A., R. J. Hobbs & .R. Margui.es. 1991. Biological
consequences of ecosystem fragmentation: a review.
Gonservation Biology 5: 18-32.
Schmidt, C. B. 1949. A vida rural no Brasil: a area do Paraitinga-
uma amostra representativa. Boletim de Agricultura. Numero
unico. Secretaria da Agricultura do Estado de Sao Paulo, Sao
Paulo.
ScRiBER, J. M. & F. SianskyJr. 1981. The nutritional ecology of
immature insects. Annual Review of Entomology 26: 183-211.
Shahabuddin, G. Sc C. A. Ponte. 2005. Frugivorous butterfly species
in tropical forest fragments: correlates of vulnerability to
extinction. Biodiversity and Conservation 14: 1137-1152.
SiiELi.Y, T. E. & D. Ludwig. 1985. Thermoregulatory behavior of
the butterfly Cafisto nubila (Satyridae) in a Puerto Rican Forest.
Oikos 44: 229-233.
SiiiR.\i, Y., Y. Kosugi, & I. Noguchi. 1998. Effects of sex, mating
status and temperature on flight activity of the Oriental tea
tortrix, Homona magnanima (l.epidoptera: Tortricidae). Applied
Entomology and Zoology 33: 413-418.
Sryc.ley, R. B. 1994. Shivering and its cost during reproductive
behavior in owl butterllies Caligoiind Opsiphanes (Ntyuphalidae:
Brassolinae). Animal Behaviour 47: 2.3-32.
Turner, }. R. G., C. M. Gatehoiese & C. A. Corey. 1987. Does solar
energy control organic diversity? Butterflies, moths and the
British climate. Oikos 48: 195-205.
Uehar.a-Pr.4do, M., Brown Jr., K. S., & A. V. L. Freita.s. 2007.
Species richness, composition and abundance of fruit-feeding
butterflies in the Brazilian Atlantic Forest: comparison beftveen
a fragmented and a continuous landscape. Global Ecolog)' and
Biogeography 16: 43-54.
ViTousEK, P. M., H. A. Mooney, J. Lubchenco &J. M. Melillo. 1997.
Human domination of earth’s ecosystems. Science 277: 494-
499.
White, P. |. T. &J. T. Kerr. 2007. Human impacts on environment-
diversity relationships: evidence for biotic homogenization
from butterfly species richness patterns. Global Ecolog}' and
Biogeography 16: 290-299.
Yela, J. L. & M. Hoi.yoak. 1997. Effects of moonlight and
meteorological factors on light and bait trap catches of noctuid
moths (Lepidoptera : Noctuidae). Environmental Entomology
Vol. 26, lY 6, pp, 1283-1290.
journal oj Ri'searrh on Uw IjjndojHm
42; 5-12, 2003 (2010)
Use of sound and aerial chases in sexual recognition in Neotropical
Hamadryas butterflies (Nymphalidae)
Onildo }. Marini-Fii.ho' -^ and Woodruff W. Benson'^
‘Dep. Biologia Animal, Universidade Estadual de Oampinas, C. R. 6109, 13083-970 Oam|)inas, SP, Brazil
-Instituto Ohico Mendes de Oonsei vacjao da Biodiversidade, EQSW 103/104, Bloco D, 1- aiidar. Setor Sudoeste. CEP: 70670-350.
Bra.silia, DF, Brazil
0. m a ri ni @gm a il. com
'14ei3. Biologia Animal, Universidade Estadual de Campinas, C. P. 6109, 13083-970 Camjtinas, SP, Brazil
Abstract. Neotropical Hamadryas butterllies are notorious for the clicking noise they produce in
flight. Tests of the sotind production cajtacitv of nine species of Hamadryas and observations on
aerial interactions of six .s|tecies showed that, among the three species grotips, onh males of the
jeronia grotip produced sounds, whereas females of all species and males of the jcbrna and laodamia
gron|ts never did so. .Vlost of the aerial interactions occurred during mid-day, generally initiated by
males in exploratory flights. Chasers were always males. Male.s engaging in chases with other males
continnallv nroduced clickine sotmds dnrinsi: the interactions whereas males chasing females usnallv
restricted their auditory displays to the initial jt
of both sexes of six species of Hamadryas, m;
observed, with one single male participating it
females and male.s of //. jeronia. There was no i
successfully defended a feeding jterch and the n
is probably involved in finding mates, while at
dominance hierarchy among male Hamadrya.s.
Key words: agonistic interactions, behavior,
connntmication, sexual recognition, sound.
Introduction
Butterflies couununicate by means of a variety
of stereotyped acoustic, visual, chemical, and
tactile signals (Swihart, 1967; Wickman & Wikluud,
1983; Boppre, 1984; Silberglied, 1984; Bernard
& Remington, 1991; Lees, 1992). Among these,
acoustic signaling is relatively infrequently cited
in the literature (Swihart, 1967). The Neotropical
Hamadryas (Hiihner, 1806) butterflies, a tight-knit
group containing 20 species (Jenkins, 1983), are
famous for their production of loud clicking sounds
during aerial chases (Bates, 1865; Darwin, 1871;
Swihart, 1967; Otero, 1990). Adult butterflies feed
on tree sap and rotting fruits, and individuals of both
sexes may display and fight to defend feeding sites
from congeners (Marini-Filho, 1996). Ross (1963)
classified Hamadryas ‘pugnacious,’ although he did
not obseiwe site fidelity or other evidence for territorial
behavior. //mMadryzo butterflies are capable of hearing
sounds produced by other conspecific butterflies and
consider that once these sounds are produced during
social interactions, these are probably involved in
conspecific communication (Yack et at, 2()()0) . Yack et
Received: 27 Aj>ril 2009
AccejHed: 1 May 2009
lia.se of the pursuit. In a cage contaiuiug 24 iiulividuals
‘s were involved in 100% of the aerial interactions
1 57% of them. The most chased iudividttals were
elatioti between the ntimber of times an individual
utiiber of aerial chases initiated. Sound prodttctiou
■rial chases may be used in the establishment of a
btttterflies, comiminicatioti, Hamadryas, acoustic
al, 2000 also discuss that the po.ssible origin of sound
production in the Papilionoidea btUterllies could
be derived from bat-detecliou in the basal clade of
Hedyloidea moths, thus being a degeneration ofthe.se
former structures.
Although Seitz (1913) reported that almost all
Hamadryas [members of the genus Agmrnia and
jWidromia (genus Hamadryas Stcnsn Jenkins, 1983)]
make sound on llight, species typical ofden.se tropical
forests (e.g. H. chloe, H. alicia, H. rosandra and H.
Jenkins, 1983) apparently do not ttiake
sounds. Otero (1986), based on the observation that
males of //. jeronia intensely produce sound when
pursuing other Hamadryasm flight, whereas H. j'ebrua
were ‘mute’ and performed a spiral flight, argues that
the behaviors represent alternative means of sexual
recognition in the genus. Hamadryas were placed by
Jenkins (1983) in three species groups (subgenera)
based mainly in wing venation differences (note that
species names preceded by * are possible exceptions):
(1) jeronia species group (subgenus Hamadryas) ,
including H. jeronia, H. gualemalena, H. il)litliim.e,
H. ej)inome, H. fornax, *H. alicia, *H. rosandra, H.
amphinome, H. belladonna, //. arinome, (2) yf/zrR// species
group (subgenus Ageronia), including H. februa, H.
amphichloe, H. glaiiconome, H. honorina, H. allanlis, II.
chloe, H. albicornis; and (3) laodamia species group
6
/. Res.Lepid.
(subgeniis Peridromia) , including H. laodamia, H. arete,
//. veiutina.
The mechanism of sound production by Hamadryas
is still subject of controversy. At least seven different
places on the thorax, abdomen and fore wings have
been proposed as sound-producing organs (Jenkins,
1983; DeVries, 1987; Monge-Najera & Hernandez,
1991; Swihart, 1967). Otero (1990) presents good
evidence that Hamadryas feronia produce percussive
sound through the striking of the wings. He points out
that the structures responsible for the loud snapping
sound are the swollen veins at the distal end of the fore
wing discal cell. These modihcations also occur in the
Australian Hecatesia moths and were called castanets
by Bailey ( 1 978) . Some Satyrinae species in the genus
Pharneuptycliia and Euptychoides also seem to have
identical structures a.ssociated with sound production
(Kane, 1982; Murillo-Hiller, 2006). According to
Otero (1990), castanets were only observed in the
males of the sound-producing pnvnia. species, while
males and females of H. fehrua in Venezuela do not
show these structures. The swellings of the snb-costal
venation of the forewings have also been supposed
to be associated with sound production by Monge-
Najera and Hernandez (1991), however, these authors
pointed that swollen snb-costal veins occur in all
Hamadryas species they dissected {amphinome, feronia,
gualemalena, glauconome, and fehrua) independent
of sex. Further studies made by Yack et al. (2000)
contradicts the percussion mechanism arguing that
sound can be produced by a single forewing, thus
pro])osing a wing deformation mechanism for the
production of sound. This ‘flip-flop’ changes the side
of the wing concavity as shown in the photographs
])resented by Monge-Najera et al. 1998.
In the present study we evaluate the sound
production capacity of nine species of the genus
Hamadryas and analyze the hypotheses related to the
possible functions of sound production and aerial
chases in sexual recognition. After determining which
species and sexes are capable of producing sounds, we
use behavioral and morphological data to conjecture
if ( 1 ) aerial interactions with sound production are
used for sexual recognition between Hamadryas, and
(2) aerial interactions are related to the establishment
of a dominance hierarchy between the males present
in the feeding arena.
Study sites and methods
But ter flies were captured using standard Van
Someren-Rydon butterfly traps baited with a mixture
of fermented sugarcane juice and banana (DeVries,
1 987) . Traps were set several times from 1992 to 2090
along the edges and interiors of forests and woodlands
at eight different localities: Linhares Forest Reserve
(tropical semi-deciduous forest), Linhares, ES, Brazil
(19°04’ S; 40°08’ W); Santa Genebra Forest Reserve
(subtropical semi-deciduous forest), Campinas, SP,
Brazil (47°04’ S, 22°50’ W); Brasilia Botanical Garden
and Agna Limpa Reserve (tropical cerrado savanna
and galleiy forest) , Brasilia, DF, Brazil (15°57’ S; 47°56’
W); Pipeline Road (tropical evergreen rain forest),
Gamboa, Panama (09° 10’ N, 79°51’ W); the restinga
dry-forest of Praia das Neves (semi-deciduous tropical
dune forest) ES, Brazil (21°18’ S, 41°02’ W) ; Ecological
Station of the University of Minas Gerais (upland
tropical semi-deciduous forest), Belo Horizonte, MG,
Brazil (19°43’ S, 43°57’ W) ; Serra da Canastra National
Park (cerrado savanna and gallery forest) , MG, Brazil
(20° 14’ S, 46°33’ W); and the cerrado woodlands of
Fazenda Jatoba, Correntina, BA, Brazil.
We tested freshly captured butterflies for sound
production capacity by holding the hind wings dosed
over their backs with forceps and passing the fore
wings below the hind wings, so that the fore wings
were free to beat and produce their typical clicking
sound (Otero, 1990).
Data on flight interactions were obtained from
butterflies kept in an outdoor cage (4x6 m at the
base and 4 m in height containing the trunks of two
trees) set in a plantation of native trees in the Linhares
Forest Reserve. This area was regularly used by at least
five Hamadryas species. Caged butterflies permitted
observations on butterfly social behavior during a
period of Hamadryas scarcity between June 1993
and March 1994. Observations of flight interactions
were all from October 1993 on 24 caged butterflies,
comprising 13 males (m) and 5 females (f) H. feronia, 2
m atid 1 f H. amphinome, 1 m H. iphthime, 1 f //. arinome,
and 1 m H. laodamia (Table 1).
Butterflies were fed with fermented banana and
sugarcane juice every morning. Each butterfly was
individually numbered on the hind wing underside
with India ink or marked with highly visible colored
spots on the upper side of each fore wing to indicate
its sex and species. For each interaction, the species
and sex of both individuals and which of them was
the chaser and the chased were recorded. Sounds
produced and, when possible, the individual
responsible for it were also recorded. Nomenclature
is based on Jenkins (1983).
The non-parametric statistic Chi squared was
used to test the heterogeneity of the interactions
among the sexes while the binomial statistic (Z) was
used to compare the distributions of probabilities
of interactions among individuals of the same sex
or species and those of different sex or species.
42: 5-12, 2003 (2010)
Table 1 . Observed and expected [ ] number of aerial interactions from 24 caged Hamadryas butterflies kept in an outdoor cage
(A/= 129 interactions). Expected values of the main diagonal were calculated as [n(n-^)/N] x 129, while the other elements were
calculated as {if/N) x 129. FR = H. feronia, AM = H. amphinome, ARI = H. arinome, IP = H. iphthime, LA = H. laodamia.
FR m (»?=13)
FR/(fi=5)
AM m (n=2)
AM/(>j=l)
ARI/(j!=1)
IP III (»!=1)
LA III (;/=l )
FR m
91 [55]***
28 [23]
1 [9|**
0 [5]*
2 [5]
6 [ 5]
0 [ 5]*
FR/
0 [7]***
0 [-/]*
0 [2]
0[2]
1 [2]
0 [2]
AM m
0 [ /]
0 [ /]
0 [i]
0 [1]
0 [i]
AM/
0 [0]
0 [0]
(» [9]
ARI /
0 [0]
« [0]
IP m
0 [0]
Hypothe.sis te.st.s Lor .sample proportion vs. hypothesized value: * = P < 0.05, ** = P < 0.01, *** = P < 0.001.
Spearman rank correlation was used to assess the
relationship between two discrete variables describing
the number of events observed.
Results
Sound production. The sound production tests
carried out with recently captured butterflies showed
that only males of the five species of the yrrortm group
(sub-genus Hamadryas'. H. feronia, H. iphthime, H.
epinorne, H. amphinome, H. arinome) produced sounds
under the test conditions (Table 2). These were also
the only species in which one can perceive .swollen
veins in the middle of the proximal border of the
males’ forewings. The feronia group females and
individuals of both sexes of the laodamia (H. laodamia
and H. arete) and februa {H. februa and H. chloe) groups
never produced sounds in the hand tests (Table 2)
nor in the flight cage. Males of//, feronia, H. epinorne
and H. iphthime (/eroruVegroup species) produced most
.sounds, whether in flight interactions, when perched
over food, or while walking on tree trunks. Data
a.ssembled from the literature (Table 3) suggest that
there may be variation in sound production capacity
of some species; however, since many Hamadryas
species have veiy similar color patterns, these results
need confirmation.
Flying chases. Of the 104 observed flight
interactions in which the departing points of the
participating individuals were observed, 74 occurred
between two H. feronia males and 23 between a male
and a female H. feronia. The other 7 interactions
involved a male H. feronia and another species. The
most frequent interactions between two males were
initiated by a flying chaser (64%), while the most
frequent interactions between a male and a female
were between perched individuals (39%) (y- = 58.7,
d. f. - ?>, P < O.OOOl). Aerial chases occurred almost
exclusively during periods of intense sunshine, mainly
from 1 130 h to 1330 h on hot windless days. Hamadryas
males commonly made exploratory flights ca. 1.5 to
2.5 m high, surrounding the two trees inside the cage.
Such behavior normally stimulated other individuals
in the cage to fly.
When encountering a perched individual, flying
Hamadryas of the feronia-growp frequently made a
pendidar flight display. This display comprised a
.semicircular flight with constant .sound production for
5 to 10 s, 10 cm below the perched individual, which
could be of either sex. Some perched individuals
did not respond to the display, but others took flight
after or ahead of the displaying individual. When
this happened with two males, a chase was normally
initiated with one or both butterflies vigorously
producing sounds during the first 10-20 s of the
interaction. During a chase both individuals flew
rapidly and performed complex aerobatic maneuvers
which included downward spiral fliglits, fast dives-
and-rises, zigzags, and sudden, momentary (<1 sec)
perches.
Twenty-five percent of the aerial chases (n = 27)
began when an individual walked on the trunk and
found and touched another individual. Apparently
individuals walking on trunks after feeding were
deliberately looking for other Hamadryas w\d\ which
to interact (and not for food). Another 33% of the
aerial chases (n = 35) began with a perched butterfly
darting after a hovering individual, and 18% of the
cha.ses (n = 19) began with a flying butterfly provoking
a perched individual to fly using the pendular display.
The other 24% of the aerial interactions (n = 26) were
initiated when two individuals met in flight; these
occurred mainly during the hottest hours when many
butterflies were flying. Interactions between more
than two butterflies were not considered.
s
/. Res.Lepid.
Table 2. Number of individuals producing sound in the hand tests carried out with males and females of nine Hamadryas
species in Brazil and Panama.
Species group (Siibgenus)
Species
Sex
Number producing
sound
Number soundless
Percent individuals
producing sound
febma {Agmmi(i)
m
0
21
0
I
0
18
0
chlod'
m
0
3
0
I
0
2
0
laod a m id ( Peri d ro in id)
Idoilnmid-
m
0
8
0
I
0
4
0
ari’tr
m
0
1
0
I
0
1
0
feronia ( Haniadryds)
feronid'-
m
35
7
83
f
0
26
0
iphihimr- ^
m
39
9
95
f
0
20
0
cpinomr-
m
17
1
94
I
0
15
0
amphinomr' '■ “
m
18
3
86
I
0
19
0
drinomr
m
5
0
100
I
0
5
0
1 ) .SV«,v(( Jenkins (1983). Butterflies front: (2) Linhares, ES, Brazil; (3) Campinas, SP, Brazil; (4) Balboa, Panama; (5) Brasilia, DF,
Brazil; (6) Praia das Neves, ES, Brazil; (1) Belo Horizonte, MG, Brazil; (8) Serra da Canastra National Park, MG, Brazil; (9) Faz,
Jatttba, Correntina, Bahia, Brazil.
Table 3. Summary of published reports of sound production in Hamadryas butterflies based on field observations (FO) and
manual tests using Otero’s (1990) hand test (OHT). References; (1) Jenkins (1983); (2) Ross (1963); (3) Monge-Najera and
Hernandez (1991); (4) Otero (1990).
Group/Species
Sex
Locality
Method (FO/OHT*)
Sound production
Ref.
felmid species Group
II. amphichlop
P
Dominican Republic
FO
Yes
1
//. chloe
p
? (dense rainforest)
FO
No
1
II. fcbrun
P
Mexico
FO
Ye.s
9
II. pdmia
???
???
FO
Yes
3
II. februd
m and /
Venezuela
FO/OHT
No
4
II. guatemdlend
P
Mexico
FO
Yes
9
pronid species Group
H. feronia
m
Venezuela
FO/OHT
Yes
4
II. feronia
/
Venezuela
FO/OHT
No
4
42: 5-12, 2003 (2010)
9
Of the 129 aerial chases with interacting individuals
of known sex, among 17 ni and 7 f, 76% (n = 98) were
between two males, which was more than expected (Z
= 3.097, P < 0.001 ) , 24% (n = 3 1 ) with a male chasing a
female (Z = -0.600, P > 0.05), and none with a female
as the chaser, which was less than expected (Z = -3.802,
P< 0.001) (Table 1). Hamadryas feronia \yAi'\\c\p'Aied
in all interactions, generally chasing a conspecific
(90.1%, n = 120). Only 8 aerial interactions (6.2%)
involved other species, and 7 of these were between
H. feronin'cmd a male H. iphthime (Table 1).
Chases between two male H. feronia occurred in
a higher frequency than was expected (Z = 6.409, P
< 0.001), and those involving a male and a female
H. feronia occurred in a smaller frequency than was
expected (Z = -2.721, P < 0.005) (Table 1). Chases
involved fast flights and much sound production.
These interactions nsnally ended with one of the
individuals perching while tlie other continued flying.
Interactions between a male and a female nsnally
began with some sound production by the chasing
male in a short period of fast flight, after which the
male followed the female in a slow flight with little or
no sound production until she perched. Frequently,
the male would alight behind and court the female
(described below). Individuals that were chased a
lot seemed to avoid interactions and apparently flew
less during the periods of greater exploratoi^ flight
activity.
The majority of the cha.ses were carried out by only
a few individuals (Fig. la) , with one H. feronia (no. 89)
performing no less than 57% of all chases (33 of the
58 chases by identified individuals). The next most
active males initiated only four chases each. Three of
the ten most chased individuals were females, but the
frequency distribution of clia,sed butterflies was much
more uniform than the frequency distribution of the
chasers (Fig. lb).
Sometimes more than two /-/rt/wr/rfr'yrw engaged in
aerial interactions. These interactions tended to be
intense, long lasting, and difficult to keep track of the
individuals. Most involved three or four individuals,
but a few had up to seven. These happened when
individuals met during exploratory flights in the
hottest hours of the day and perched individuals
joined the flying party. Some of these interactions in
which all individuals cotild be identified consisted of
two or more males chasing a female.
All Hamadryas species of both sexes may defend
feeding sites through displays and physical interactions.
However, there was no relation between the success
of an individual in defending a feeding site and the
number of times it chased after other individuals.
Only one individual seemed to be efficient in both
Figure 1. Frequencies of aerial chases of identified
Hamadryas individuals in a flight cage (n = 58). A) Chases
effected by a chasing individual. B) Chases suffered by
a chased individual. Individuals are represented by a
species/sex/number code: AM = Hamadryas amphinome,
API = H. arinome, FR = H. feronia, IP = H. iphthime, m
= males, f = females, and the capture number of the
individual.
tasks (f/. feronia no. 89). Of the species engaging
in aerial chases, H. amphinome did much better
at defending feeding sites than at chasing other
Hamadryads (Table 1; Fig. 2, Spearman correlation,
N = 14, R = 0.25, t, = 0.90, T= 0.39). Individuals
of other species participated in le.ss chases than was
expected (Table 1).
Courtship. In the cage, six observations were made
on male H. feronia cotirting females perched on a
tree trunk. All of them around noon. Usually a male
perched 5 to 10 cm behind a female and facing her
and remained 1 to 5 min slowly opening and closing
10
J. Res.Lepid.
Figure 2. Relation between the number of times
individuals successfully defended food and the number
of aerial chases initiated by the same individuals. AM =
amphinome, FR = feronia, IP = iphthime.
his wings while slowly approaching the female by
taking a few steps at a time. The female responded
to this approach with similar wing movement. When
the male got close (< 1 cm), she usually walked 15
to 100 cm down the trunk. If the male touched her
with his wings or legs, she usually flew to another tree
trunk or to the cage walk The male either followed
her to the new perch or quit after some unsuccessful
attempts. After this he would fly around the trees
apparently looking for another individual with which
to interact.
The first author once observed a much longer
courtship in H. epinom.em a reforested area containing
Joannesia princeps (Euphorbiaceae) and Senna nmltijuga
(Leguminosae). The butterflies behaved essentially
like the H. feronia described above, differing principally
in that when they changed perches they usually flew
over a much larger area (about 20 x 20 in) from 1 to
7 Ill high (canopy height), and usually perched higher
up (4-6 m) than did the caged H. feronia.
Discussion
Our results, added to the observations of Jenkins
(1983), Otero (1988) and Yack et al. (2000), indicate
that sound production capacity in Hamadryas is
restricted to the males of tiie feronia species group,
with the possible exception of H. amphichloe, which
belongs to the februa species group. Monge-Najera
and Hernandez (1991) allude to one population
of sound producing H. februa which disagrees with
our data and those of other workers. Species of the
feronia group are unique in their possession of swollen
wing veins associated with sound production (Otero,
1988 and our observations), and the rare reports
of sound production in the februa group (Monge-
Najera & Hernandez, 1991; Ross, 1963) may result
from identification errors. The five populations of
H. februa tested in the present study did not produce
sound, as is the case of the Venezuelan population
studied by Otero (1988, 1990), which contrasts with
the results of Monge-Najera and Hernandez (1991)
and Ross (1963).
Hamadryas feroniais monomorphic, suggesting that
sound production or other non-visual cues may be
related to the discovery of females for mating. The
absence of sound production and the presence of
sexual color diinoiq)hism in the laodamia species group
suggest that sexual recognition between individuals
of this group may have a visual component, since
butterflies that possess sexual color dimorphism
are supposed to recognize each other visually
(Silberglied, 1984), although there is little evidence
for this. The absence of both sound production and
color dimorphism in the species of the februa species
group suggests that chemical signals may be used for
determination of gender.
All the species mentioned by Jenkins (1983) and
Otero (1988) in which sound production has not
been noted belong either to the laodamia or februa
species groups. Species of the februa group have been
reported as capable [H. amphichloe, and H. februa) or
incapable of producing sounds {H. chloe (Jenkins,
1983) and H. februa (Otero, 1988)]. This suggests
that there may exist different mechanisms of sexual
recognition between species of the same group or that
the dogma that has developed in relation to the sound
production capacity of the whole group Hamadryas has
been due to misidentifications of flying individuals
because of their great similarity. In the past, this
genus had a very confusing taxonomy, comprising
about 100 species. Jenkins (1983) synoiiymized more
than two thirds of these, leaving only 20 species and
21 subspecies in the genus Hamadryas. Probably
many reports prior to the revision of Jenkins (1983)
contain identification errors, which may have added
to the confusion about the sound production capacity
of each species.
Jenkins (1983) recorded two copulations for
Hamadryas, one at 1130 h {H. amphinome) and the
other at 1400 h (H. velutina). Most of the aerial
interactions and courtship behavior in the present
42: 5-12, 2003 (2010)
Study occurred around noon, simultaneously with
the majority of the flight interactions. The sounds
were produced at will during flight interactions by
male butterflies. Haviadryas feronia has been proven
to hear the sounds in the same acoustic range they
produce (Yack et ai, 2000) . Therefore, these situations
may be used to promote sexual recognition which
apparently takes place quickly at the very beginning
of chases carried out by males after females. Thus,
males initiating chases shift to courtship behavior
almost immediately upon approaching a female or
proceed in aerial pursuit when finding a male. Some
moths {Hecatesia thyridion) and Satyrinae butterflies
are among the few Lepidoptera known to produce
high frequency sounds, similar to those produced
by Haviadryas males, which are voluntarily used in
intraspecific communication while in courtship flight
(Bailey, 1978; Kiine, 1982; Murillo-Hiller, 2006). Thus,
it seems difficult to ascertain what role the clicking
sounds play in Haviadryas' behavioral repertoire.
We conjecture that the clicks are used as an early
recognition of sexual partners and that sound intensity
may also be used by females as a means to assess the
male’s htness, as bigger healthier males may produce
louder clicks. Behavioral experiments are needed to
provide evidence for either hypotheses.
Although Haviadryas butterflies of both sexes
defend feeding sites, the aerial chases observed here
do not seem to be associated \vith resource defense
or to territoriality (Ross, 1963). Food was provided ad
lihituvi in two localized spots in the flight cage and the
majority of the individuals had ceased feeding when
aerial chases reached a climax (Marini-Filho, 1996).
With the exception of one very successful male, males
that had the greatest success in defending feeding sites
were different from those that initiated aerial chases.
W'hile H. feronia was the species that performed the
majority of the aerial chases, H. aviphinotne was the
one that defended the feeding resource more fiercely.
This is consistent with their size difference, as body
size determines to a great extent the winner of those
interactions (Marini-Filho, 1996).
Aerial chases apparently play two intimately
related functions: the discovery of receptive females
and the establishment of dominance hierarchies for
mating priority, although we did not consider this
during the experiment. Dominance hierarchies may
be the result of natural selection over intraspecihc
differences in flight capacity or other fitness-related
character, promoting the individual spacing in natural
populations and enhancing the mating chances of
hierarchically superior individuals (see Rutowski etal,
1989), the priority order being generally established
through previous agonistic encounters (Archer, 1988:
,1 14). The establishment of dominance hierarchies
may come about by the recognition of the individual
aggre.ssiveness by the butterflies present in the .same
feeding area (usually one or a few tree trunks oozing
fermenting sap). It is unlikely that monomorphic
butterflies as other monomorphic insects are able
to visually recognize others of the same or similar
species (Ewing, 1984). Males and females of most
species of the groups feronia and februa have a cryptic
marbled color pattern, making them difficult to be
recognized in flight. It is more likely that after a series
of aerial chases the individuals present in the area can
recognize behaviorally that there are other individuals
more aggre.ssive a,ssuming then a submissive attitude,
either evading chases or refusing to fly during the
period of most aerial interactions. Possibly the most
chased Haviadryas were receptive, while non-
receptive females would not stay close to the food
source during the period of aerial chases, and would
otherwise be looking for suitable host-plants for their
larvae if they could have left the cage.
These results may also help the definition of the
Haviadryas phylogeny once it seems that there is a
high agreement between the ability to produce .sounds
observed on the males of the feronia species group
and the inability to produce sound in the other two
species groups {laodaviia And februa). The ability of //.
aviphkhloeio produce sound must be checked by hand
test and further considered with the morphologic
factors to find if it is an exception from this pattern
or in fact more associated to the feronia species group
than to the februa species group.
Acknowledgements
We thank the direction and staf'f'oftlie Linharcs Forest Preserve
for essential logistic stijtport dtiring this study. We are grateltil to
Andre V. 1.. Fieitas, Carla M. Penz. Rogerio P. Martins, Dottglas
Yanega, Robert Srygley and .Stanley Rand Ibr discussions and/or
critical cotnnients on earlier drafts of the inaiuiscript. Sttidy grants
to 0|M-F were |)rovided by Coordenadoria de Aperfeicoainento de
Pessoal de Nivel Sttjterior (CAPES) and tbe Smithsonian Tropical
Research Institute. Financial support for this sttidy was |>rovided
by FAPESP to WWB.
Literature Cited
Archkr, J. 1988. The behavioural biology of aggre.s.sion. Cambridge
University Press, Cambridge.
B.vii.i'.v, W. J. 1978. Resonant wing systems in the Atistralian
whistling tnoth Hecatesia (Agarasidae, Lepidoptera). Nature
272: 444-446.
B.vtes. H. W. 1865. Ciontrihtitions to an insect fauna of the Amazon
Valley. Lepidoptera-Nymphalinae. Journal of Entomology 2:
311-315.
Bernard, G. D. & C. L. Reminoton. 1991. Color vision in Lycaena
htitterflies: spectral timing of receptor arrays in relation to
12
J. Res.Lepid.
beliavioral ecolog)'. Proceedings of the National Academy of
Sciences (USA) 88; 2783-278?/
Boppre. M. 1984. Chemically mediated interactions between
butterflies. In: Vane-Wright, R.I. & P.R. Ackery (eds.), The
biology of butterflies, Symposium of the Royal Entomological
Society of London, no. 11, pp. 259-275. Academic Press,
L.ondon.
Darwin, C. 1871. The descent of man and selection in relation to
sex, Vo!. 1. John Murray, London.
Jenkins, D. W. 1983. Neotropical Nyniphaiidae 1. Revision of
Hamadryns. Bulletin of the Allyn Museum 81: 1-146.
K.,\ne, S. 1 982. Notes on the acoustic signals of a Neotropical satyrid
butterfly. Journal of the Lepidoptertsts’ Society 36: 200-206.
Lees, D. C. 1992. Foreleg stridulation in male Urania moths
(Lepidoptera: Uraniidae). Zoological Journal of the Linnean
Society 106: 163-170.
M.\rini-Fii,h(), O. J. 1 996. Defesa de reciirsos alimentares e interagoes
aereas entre borboletas simpatricas do genero Hamadryas.
Master’s tliesis, Lhiiversidade Estadual de Campinas, Brazil,
ix -h 73 pp.
Monc;e-NA|Era, J. & F. Hern.andez. 1991 . A morphological search for
the sound mechanism of Hamadryas bulterflies (Lepidoptera:
Nymphalidae). Journal of Research on the Lepidoptera 30:
196-208.
M(>n('.e-N.4|er.-\, J., F. Hernandez, M. 1. Gonz.-vlez, J. Soley, J. Araya
& S. Zoi.i.A. 1998. Spatial distribution, territoriality and
sound production by tropical cryptic butterflies (Hamadryas,
Lepidoptera: Nymphalidae): implications for the ‘industrial
melanism' debate. Revista de Biologia Tropical 48: 297-329.
Murii.i.o-Hii.i.er L. R. 2006. A noise producing butterfly, Yphthimoides
castrensis (Nymphalidae, Satyrinae) from south Brazil. Journal
of the Lepidopterists’ Society 60: 61-64.
Otero, L. D. 1988. Contribucidii a la historia natural del genero
Hamadryas (Lepidoptera: Nymphalidae). Tesis Doctoral,
Universidad Central de Venezuela, Macaray. viii + 108 pp.
Otero, L. D. 1990. The stridulatory organ in Hamadryas
(Nymphalidae): preliminary observations. Journal of the
Lepidopterists’ Society 44: 285-288.
Ross, G. N. 1963. Evidence for lack of territoriality in two species
of Hamadryas, Nymphalidae. Journal of Research on the
Lepidoptera 3: 207-229.
Rutowski, R. L., j. Ai.cock & M. C.arey. 1989. Hilltopping in the
pipevine swallowtail butterfly (Battus philenor). Ethology 82:
244-254.
Seitz, A. 1913. The macrolepidoptera of the world. Alfred Kermen,
Stuttgart.
Sii.BERca.iED, R. E. 1984. Visual communication in sexual selection
among butterllies. In: Vane-Wright, R. I. & Ackery, R R.
(eds.). The biology of butterflies, Symposium of the Royal
Entomological Society of London, no. 11, pp. 207-223.
Academic Press, London.
SwiiLART, S. L. 1967. Hearing in butterflies (Nymphalidae: Heliconius,
Ageronia). Journal of Insect Physiology 13: 469-476.
Wickman, R O. & C. WiCKi.UND. 1983. Territorial defense and its
seasonal decline in the speckled wood butterfly (Pararge argeria) .
Animal Behaviour 31: 1206-1216.
Yack, J. E., L. D. Otero, J. W. Daw.son, A. Suri.ykke & J. H. Fuliard.
2000. Sound production and hearing in the blue cracker
butterfly Hamadryas feronia (Lepidoptera: Nymphalidae)
from Venezuela. The Journal of Experimental Biology 203:
3689-3702.
Journal of Research on the Lepidoftera
42: 13-20, 2003 (2010)
Ecobiology of the common castor butterfly Ariarfwc merione merione (Cramer)
(Lepidoptera: Rhopalocera: Nymphalidae)
Janaki Bai Atluri'*, Samatha Bodapati', Bhupathi Rwalu Mataia', Sandhya Deepira, Devara' and
SUBBA Reddi Chiiakaia-
‘Department of Botany, Andhra Lhiiversity, Visakhapatnam - 530003, Andhra Pradesh, India
-Department of Environmental Sciences, Andhra University, Visakhapatnam - 530003, Andhra Pradesh, India
jhalluri_adit'(a007@\ahoo.com
Abstract. We describe the life histoiy of the comtnon castor butterfly, Ariadne merione merione, monthly
occurrence and seasonality' of eai ly stages and larval performance in terms of food consnmjition
and ittilization, and the length of life cycle. Onr study was conducted during 2002 itt the Andhra
University campus at Visakhapattiam (17'’42' N, 82°18' E), South India. Field study itidicated
that A. merione merione wna in continitoiis flight and reproduction, with highest densities of earlv
and achtlt stages occurring during June - Se|)tember, the time of the entire South-West monsoon.
Occurrence of the early stages was positively, but non-significantly correlated with rainfall, relative
humidity, tetnperatnre and day-length. Multiple regression analysis showed that the effect of any
combination of weather parameters on the rejtroductive activity was less than 40%. The Sotith-West
monsoon period jtrobably infhienced the reprodttetive activity by promoting fresh growth of the
larval host plant, Ririnus ronimunis, which in turn sup|rorted development of early stages. Ariadne
merione meiionew’-As. exemplified by a life cycle of 27.4 ± 3.57 days (eggs 3-4, larvae 1 3-18, and pupa 6-9
days) permitting a maximum of 8-9 overlapping generations per year. The values of the tuitritioniil
indices across the instars were A.l). 87.02-95.50%; E.U.l. 3.80-20.90%; E.U.D. 4.00-24.08%, measured
at 28°U in the laboratoi-)'. These relatively high values, at least partially explain the ecological success
of A. merione merione 'm the urban environment.
Key words: castor butterfly, Ariadne merione, life history, po|)itlatioti index, mttritional indices.
Introduction
Of the estimated 20, ()()() - 30, GOO sj^ecies of
butterflies occurring globally, at least 1,500 species
occur in India. Several field guides for the identification
of the Indian btitterflies are available (Wynter- Blyth,
1957; Haribal, 1992; Gay et al, 1992; Gunathilagaraj
et ai, 1998; Kunte, 2000 and the references therein).
A list of the works giving the descriptions of the life
histories was given by Pant and Ghatterjee (1950),
of which those of Bell (1909 - 1927) are important.
However, review of these early works indicated that
for many species data, particularly on the duration
and phenology of early lifestages, are either absent
or incomplete. Haribal (1992) noted that the life
histories of nearly 70% of the Indian species require
description. We began sttidies to address the sittiation.
Here we describe the life history of Ariadne merione
merione (Gramer), the common castor butterfly, of
the Oriental region. It is a sj^ecific pest of the castor
^Corresponding author
Received: 24 July 2008
Accepted: 20 August 2008
seed jjlant Jiicinus communis (Nayar el ai, 1976) and
the larvae also feed on the stinging nettles Tragia
involucrata And T. Jduhenetti (Euphorbiaceae) (Ktmte,
2000). Because reprodtictive efficiency dej^ends on
life style and feeding pattern (Boggs, 1981; Slansky &
Scriber, 1985; Muthnkrishnan Sc Pandian, 1987), we
also studied larval performance with resj^ect of food
tuilization by feeding them on a daily stij3|)ly of pieces
of fresh leaf of the castor j^lant.
Materials and methods
The sttidy was conducted dtiring the year 2002
in the Andhra Lhiiversity campus (168 ha) at
Visakhapatnam (17°42’ N, 82°18’ E) situated in the
east coast of India. The natural plant commtmity
of the camjius was searched for the distribution
and reproductive activity of the common castor
btitterfly Ariadne merione merione (Cramer). Adult
btitterflies were seen mostly near the larval host plant
Ricinus communis Linnaetis. Once located detailed
observations were made at 10 sites in order to observe
the flight activity and abundance of adtilLs, the period
of cojiulation and ovijiosition, following which we
collected fresh eggs to study the life history and the
duration of early stages. After oviposition, the leaf
14
J. Res.Lepid.
with egg(s) was collected in Petri dishes (15 cm x 2.5
cm depth) and brought to the laboratory. The piece
of the leaf with the egg was then placed in a smaller
Petri dish (10 cm x 1.5 cm depth) the inside of which
lined with moistened blotter to prevent the leaf from
drying. Five such samples were placed in a cage
covered with wire mesh. The laboratory temperature
was 28 ± 2° C and relative humidity 80 ± 10% with
normal indirect sunlight conditions that varied in
duration between 12h during November/Jamiary and
14h dnring june/july. The eggs were then examined
at 6h intervals daily for recording time to eclosion.
The larvae were subsequently reared on a weighed
quantity of fresh leaves supplied daily. The time of
each moult was noted. The morphological characters,
body measurements, body weight of each instar and
the faeces egested were taken daily. The prepiipal
behavior of the final iiistar, pupal particulars and the
time of adult eclosion were also recorded. Larval
performance in terms of food utilization indices were
calculated as described by Waldbauer (1968) as:
arbitrary scale of rare, less common, and common.
The relation between the monthly distribution of
early stages and prevailing rainfall, relative humidity,
temperature, and day-length was assessed by statistical
correlation and multiple regression analysis using
Minitab Statistical Software 14, 2003.
Results
Adult stage (Fig. la, b)
Both male and female adults were nearly identical,
characterized by their reddish brown colored wings
bearing black colored wavy lines. Copulations
occurred during mid-day, mostly between 1100 -
1500 h and lasting for more than one hour. Adults
were found feeding on spoiled flowers of Lantana
camam, overripe, fallen and damaged fruits of Annona
squamosa, Syzygiuni cumini and Artocarpus heterophyllus,
and the sap oozing from wounds in the tree trunks of
Citrus aurantifolia.
Food c{>nsuinpti()ii index (C'.l.)
Relative gnjwth rate (Ci. R.)
Approximate digestibility (A. D.)
F.tliciency ol conversion of
digested food (E. C. D.)
Egg stage (Fig. Ic)
Wl. of foofl consumed
Wt. of instar X No. of feeding days
Wt. gained by the instar
Mean wt. of instar x No. of feeding days
Wt. of food ingested - Wt. of faeces
- X 100
Wt. of food ingested
Wt. gained bv the instar
- X 100
W't. of food consumed * Wt. of faeces
Gravid females lay eggs singly on the under surface
of the leaves of the castor plant mostly before mid-day,
between 0900 -1200h. Females spread their wings
during egg laying, depositing 1 to clutches of 15.
There was no bias for the age of the leaf. During one
survey old leaves had 1-7 and young tender leaves 1 -
3 eggs. The eggs were round, 0.80 - 0.90 (0.83 ± 0.04)
mm in diameter. At oviposition they were white, the
color changing to light brown before hatching. Wlien
first laid eggs appeared soft in texture, but within 6 -
10 seconds they became hairy. They hatched in 3 - 4
days. Soon after hatching, larvae ate their egg-shells.
Each larva passed through five distinct instars over a
period of 13 - 18 days.
Ff ficicncy ol conversion of
ingested food (E. C. 1.)
Wt. gained bv the inslar
- X 100
Wt. of food ingested
To determine the developmental success of each
of the early stages, a number of eggs were placed in
Petri dishes in each month and the number of larvae
hatched, pupae formed and the adults eclosed were
recorded. To record the different early stages on the
natural host plant, one plant at each of the 10 study
sites was thoroughly searched at 10 day intervals eacli
month and the early stages found were enumerated
and pooled for each month. During the same visits,
the (light frequency of adults was also noted using the
Larval stage (Fig. Id-h)
Instar I lasted for 2-3 days. Larvae were 1 .8 - 2.0 ( 1 .9
± 0.08) mm on Dl, growing to a length of 2.50 - 3.00
(2.80 ±0.21) mm and width ofO.30- 0.50 (0.43 ±0.09)
mm before moult. Body was somewhat rectangular in
siiape, but slightly narrowing posteriorly. Its color was
pale brown immediately after hatching, later turning
brownish green with three brown colored horizontal
bands on dorsal side. Head was very minute, and
brown. Instar II also lasted for 2-3 days and attained
a length of 3.30 - 4.00 (3.73 ± 0.30) mm and width of
0.60 - 0.90 (0.73 ± 0.12) mm. Whitish green spines
with branched ends appeared over the entire body.
Head was brown with a pair of brown horns. There
42; 13-20, 2003 (2010)
15
were no changes in other characters seen in instar I.
Instar III lasted for 3-4 days. Developing to a length
of 6.00 - 8.00 (7.00 ± 0.81) mm and width of 1.10 -
1.50 (1.36 ±0.18) mm. Dorsally they had a yellowish
green broad stripe with brown edge longitudinal to
the body. The body spines present on the three brown
horizontal bands were also brown. Head was 1 mm in
size, blackish brown in color with white markings. The
head horns were 0.80 - 1.00 (0.90 ± 0.08) mm long
and branched. Legs were clearly visible. The larva
did not move much, but moved its head continuously
when disturbed. There were no changes in other
characters from previous instar. Instar IV also lasted
for 3-4 days, growing to a length of 1 0.00 - 1 5.00 ( 1 2.00
± 0.21) mm and a width of 1.50 - 2.00 (1.73 ± 0.20)
mm. Body became green in color. The dorsal stripe
turned iDiown with yellowish cream edges. The three
black horizontal bands began to disappear. Head was
blackish brown in color, square shaped and measured
1 .00 - 2.00 ( 1 .53 ± 0.41 ) mm in diameter. There were
three triangular white markings on the head. The
head horns were reddish brown in color and measured
2 mm in length. Segmentation was clear. Body spines
were green in color, arranged in four lines on each
side of the body on all the segments. The legs were
green. Instar V also lasted for 3-4 days. When full
grown the larva was 23.0 - 30.0 (25.6 ± 0.32) mm long
and 2.20 - 3.00 (2.73 ± 0.37) mm wide. Body was dark
green. The dorsal stripe changed to orange with black
edges showing numerous small white to cream colored
spots. The dorsal three horizontal bands disappeared
completely. Head was 2.00 - 3.00 (2.56 ± 0.41 ) mm in
diameter. It had prominent white triangular markings
with black border two present above and one below.
The horns became orange in color, with black tips,
and measured 3.00 - 4.00 (3.60 ± 0.43) mm in length.
Light and dark green crossed lines developed on both
lateral sides of the body. The color of spines changed
to brown with black tips and with yellow to orange
colored spots at their base.
Pupal stage (Fig.li)
During the prepupal period of 1 - 2 days the full-
grown larva stopped feeding, turned brown and its
lateral crossed lines changed to brown and white. The
body contracted and the larva attached itself to the
substratum with its posterior end hanging downwards.
It measured 20.00 - 25.00 (22.60 ± 0.20) mm in length
and 3 mm in width. The pupal stage lasted for 5-7
days. The brown color changed to black with pupal
maturation until adult eclosion. It measured 15.00
- 17.00 (16.00 ± 0.08) mm in length and 6.00 - 7.00
(6.46 ± 0.41) mm in width at the broadest end. The
anterior end was narrow. At the broadest point both
lateral sides were curved inwards, between which two
pointed projections appeared on dorsal side. Average
pupal weight was 202.3 mg.
Development success and population index
Hatching success varied between 40 and 100%,
being highest duringjune to September. Both larval
and pupal development success varied between 50 and
100%, (Table 1). The numerical frequency of eggs,
larvae, pupae recorded on the host plants and adult
abundance, along with the prevailing weather data
are given in Table 2. The three early stages and adults
could be found under natural conditions throughout
the year. However, the period ofjune and September
provided the highest frequency of all stages, with peak
numbers in July. Correlation between the counts of
early stages and monthly average temjterature, average
relative humidity, total rainfall, and average day-length
was positive, but non-significant, the coefficient values
being 0.566, 0.333, 0.468, and 0.521 respectively.
The four weather variables jointly influenced the
distribution of early stages to the extent of about 40%,
as indicated by multiple regression coefficients, R-
0.216-0.396 (Table 3). Other combinations including
temperat lire /rain fall-/ day-length, temperature/
Table 1 . Hatching, larval and pupal development success of Ariadne merione merione in the laboratory.
Life cycle stage
Calendar nioiith.s
J
F
M
A
M
J
J
A
S
O
N
D
# eggs incubaled
4
4
5
4
5
10
17
10
6
7
5
0
# larvae hatched
2
3
2
3
3
10
17
8
5
5
5
4
# pupae formed
1
2
1
9
3
9
12
8
5
4
4
3
# adults emerged
1
1
1
2
9
9
11
8
4
3
3
3
16
/. Res.Lepid.
Table 2. Distribution of early stages of Ariadne merione merione on Ricinus communis and the associated weather
conditions.
Life cycle stage,
Calendar months
J
F
M
A
M
J
J
A
S
O
N
D
Eaiiy stages
7
7
9
8
24
42
117
61
33
21
14
16
Adults
❖
4:
**
Temperature (°C)
24.15
25.45
27.85
29.15
30.7
29.4
30.75
28.2
29.25
28.3
26.2
24.55
Relative humidity (%)
74
68
74
74.5 ,
71.25
77
73
80.5
76.5
74
62.25
69
Rainfall (mm)
014.1
000.0
000.0
085.2
015.1
143.2
075.4
143.5
023.5
118.4
007.8
000.0
Daylength (h)
1112
1148
1215
1312
1337
1316
1304
1322
1232
1224
1132
1105
* Rare, ** Common, *** Very common.
Table 3. Multiple regression of the counts of the early stages in relation to the prevailing weather parameters.
Constant (A)
X.
X.,
X3
X,
R2
-229.6
7.342
0.758
0.331
-153.7
6.336
0.139
0.369
-195.5
7.707
0.009
0.321
-7.1
0.338
0.239
0.216
-208.4
0.188
0.183
0.272
-146.2
0.118
0.138
0.297
-137
6.419
-0.270
0.152
0.370
-229.6
9.48
1 .094
-0.068
0.335
-87.7
11.88
0.220
-0.183
0.395
-121.1
-0.497
0.137
0.146
0.300
-101.3
12.21
0.301
0.211
-0.196
0.396
X| - Monthly average temperature; X„ - Monthly average relative humidity; - Monthly total rainfall; X^ - Monthly average
daylength.
Table 4. Food consumption, growth and food utilization efficiencies of Ariadne merione merione larva fed with Ricinus communis
leaves.
Instar
Wt. of food Wt. of faeces (mg)
Wt. gained by
GR
Cl
AD
ECD
ECI
number
ingested (mg)
larva (mg)
(mg/day/mg)
(mg/day/mg)
(%)
(%)
(%)
1
11
45.0 ± 10.03
2.0 ± 0.35
1.72 ±0.1 6
0.42
11.02
95.50
04.00
03.8
III
150.0 + 16.39
13.0 ±2. 16
10.85 ±0..59
0..34
04.80
91.30
07.90
07.2
IV
2,50.0 ± 05.65
25.0 ± 5.09
31.00 ± 1.65
0.36
02.90
90.00
13.70
12.4
V
925 ± 22.22
120.0 ±5.88
193.87 ±2.61
0.45
02.16
87.02
24.08
20.9
- ln(licate.s no data due to very small size of first instar.
42: 13-20, 2003 (2010)
17
Figure 1 . Photographs of the sequential stages in the life history of Ariadne merione merione. a) Adult pairing, b) Adults feeding
on the damaged fruits of Annona squamosa, c) Egg. d) Instar I. e) Instar II. f) Instar III. g) Instar IV. h) Instar V. i) Pupa.
18
J. Res.Lepid.
relative humidity/ rainfall, and temperature-rainfall
also liad similar to lower values.
Food consumption, growth and utilization
The data for the weight of food consumed and
weight gained by the larvae are given in Table 4. The
same data could not be collected for instar I due to its
small size with consequent danger in handling. The
amount of food consumed increased from instar to
instar, the proportion of total food consumed in instars
from II to V being 3.28, 10.94, 18.24, and 67.51%.
Thus, there was greatest consumption in instar V. The
weight gain corresponded to the food consumption
trend of the respective iiistars. The weight gain in
instar V was 81 .65% of total larval weight. The weight
of successive instars plotted against the food consumed
indicated a clear relationship between these two
parameters (y = 0.227 X and 18.383; r = 0.9963). The
values of growth rate (G. R.) decreased from instar II
to III and then increased to instar V, the values varying
between 0.34 and 0.45 mg/day/mg. Consumption
index (C. I.) progressively decreased from iiistar to
instar, the values ranging between 2.16 and 1 1.02 mg/
day/mg. Table 4 also includes the indices of food
utilization efficiencies A. D., E. C. L, and E. C. D. The
range of A. D. values was 87.02 to 95.5%, that of E.
C. I. 3.8 to 20.9% and E. C. D. 4.0 to 24.08%. While
E. C. I. and E. C. D. decreased, A. D. increased as the
larvae progressed.
Discussion
The year round occurrence of early stages on
the host plant Ridnus communis showed that Ariadne
merione merione breeds continuously, corresponding
with the usual pattern noted for most tropical
butterflies (Owen, 1971; Owen et ai, 1972). The
period of highest frequency from June to September
correlates with the South - West monsoon. Thus
rainfall appears to be the most important factor
promoting higher reproduction rates in A. merione
merione as is the case for both Catopsilia crocale
(Chirstopher & Mathavan, 1986) and Catopsilia
pyranthe (Atluri et ai, 2004a). However, statistical
correlation of the distribution and abundance of
early stages with the rainfall, though positive, was
non-significant. Precipitation during the South-West
monsoon likely had its influence on reproduction
via the host plant. During this season, the host plant
had its greatest fresh growtii, a resource needed by
the larvae for better performance due to the likely
higher levels of nitrogen and water content (Slaosky &
Feeny, 1977; Scriber, 1977; Mattson, 1986). Although
Figure 2. Relationship between food consumption
and growth in Ariadne merione merione on Ridnus
communis.
the host plant was available throughout the year, leaf
quality in terms of nitrogen and water content might
have varied through the year, hence the observed
trend in the pattern of reproduction of A. merione
merione. The work of Pullin (1987) on the growth of
larvae of Aglais urticae fed with foliage with different
water contents also suggested the likely variations in
the breeding success as being due to variations in
rainfall. Pollard et al. (1997) also examined a similar
relationship. The low incidence of early stages during
periods other than the South - West monsoon could
have been due to a decrease in mature egg number as
reported by Braby (1995) in the Satyriiie butterflies,
which also breed continuously.
Few other species noted at the study biotope
also reproduced all year, but at a higher rate during
different periods: Pachliopta arisolochiae April to May,
and October to November (Atluri et al, 2004b) , Papilio
polytes August to Februaiy (Atluri et al, 2002) , Graphiurn
agamemnon August to December (Veiikataramana et
al, 2003a), Eurema hecabe September to November
(Veiikataramana et al, 2003b), Euploea core November
tojaniiaiy (Veiikataramana et al, 2001). For most of
India, Wynter - Blyth (1957) rated spring as the most
favorable period, followed by post monsoon and South
- West monsoon. In the northern western Ghats,
Kimte (1997) observed highest flight activity during
late monsoon (August to September) and early winter
(October to November). These differences in the
phenology of butterflies suggest that different species
respond differently to the prevailing environmental
seasonality and exhibit different life history patterns.
Even different species of a genus may behave
differently as observed by Jones and Rieiiks (1987) in
tlie three species of the tropical Eurema they studied.
42: 13-20, 2003 (2010)
19
The overall effect of weather on population trends is
complex and difficult to predict, as also expressed by
Pollard (1988).
The characters of full grown larva observed in
this stndy substantiate those given in Bell (1910)
and Sevastopulo (1939) as well as pupal duration.
The total development time from egg laying to
adult eclosion was determined as 27.4 ± 3.57 days
at about 28°C, thus permitting a maximum of 8 to
9 overlapping broods per year. This behavior is in
line with the expectation of tropical butterflies to
have a short life cycle, and multiple broods over the
year (Owen, 1971). Since temperature influences
instar duration and the overall development time
(Mathavan & Pandian, 1975; Palanichamy et ah, 1982;
Pathak & Pizvi, 2003; Braby, 2003) , tlie brood ntun!)er
in other parts of A. nierione merione distribution may
vary from our records depending on the prevailing
temperattires. As no temperature extremes occur at
Visakhapatnam, especially at the Andhra University
site, the duration of life cycle did not vary much over
the overlapping seasons.
Adult feeding on the damaged and ripened fruit
helps them obtain proteins and carbon sources (Tevey
& del Rio, 2001 ), with such nutrient uptake improving
egg productivity (Fischer et al, 2004) . The larval food
also appears to be highly nutritional as indicated by
the observed values of assimilation efficiency (A. D.),
the efficiency of conversion of ingested food (E. C. 1.) ,
and the efficiency of conversion of digested food (E. C.
D.) into the body substance. The chemistr)’ of the leaf,
particularly its nitrogen and water content, influences
the assimilation efficiency (Pandian & Marian, 1986).
The castor leaves contain 2.54% nitrogen and 75.20%
water (Senthamizhselvan & Mnrngan, 1988). Hence
(he observed high A. D. value, mean 90.97%. Stich
high values are characteristic of the foliage feeders
(Slansky & Scriber, 1985) and indicative of their high
growth efficiency (Singhal, 1980). The values of E.
C7 D. and E. C. 1., particularly those of the last two
instars, are also relatively high (12.4%, 20.9%; 13.7%,
24.1%), thus respectively indicating tissue growth
efficiency and ecological growth efficiency, which
enabled A. merione nierione io thrive successfully in the
urban environment.
Acknowledgements
riie autliors thank Profe.ssnr Frances S. Cliew of tlie
De|3artinent of Biology of Tufts University. Medford, USA for
appraising ottr work. We also thank Mr. S. Naresh of the Andhra
University Statistics Department for help in the statistical analysis
of the data, and the Librarian, BNHS, Mtnnbai, for the supply
of literature. Two anonymous reviewers improved otir original
manuscript for which we thank them.
Literature cited
An.L Ri, f . B., S. B. VF.N'ivVtA Rvmana & C. Sriiiw Rmni. 2002. Autecology
of the common mormon htitterfly Papilio polyles {Le]jido])tera:
Rhopalocera: Pajtilionidae). Journal of Environmental Biology
23(2): 199-204.
Art.i'Ki, |. B., S. P. Vknk.\ta Ramana, & C. Suisiu Ri nni. 2004a.
Ecohiology of C.alopsilia pyranlhe, a trojtical pierid hutterlly.
(airrent Science 86(3): 4.57-461.
ATtx'Ri, |. B., S. P. Venk,\ia Ramana, D. Krishna Ri nni & SuititA Ri nni,
C. 2004b. Ecohiology of the common rose htitterfly /-’rtc/t/t'o/t/r/
arislolochiae (Lepidoptera: Rhopalocera: Papilionidae) .
Proceedings AP Akademi of Sciences 8(2): 147-154.
Brabv, M. F. 1995. Larval and adult food plants for some tropical
satyrine butterflies in northern Queensland. Australian
F.ntomologist 22( I ): .5-13.
Br.\bv, M. F. 2003. Effect of temperature on develo|)ment and
survival in Deltas iiigriria (Fabricius) (Lepidoptera: Pieridae).
Australian Journal of Entomology 42(2): 138-143.
Bttt.i,, 'L R. 1909-1927. The common hutterilies of the |)lains of
India. Journal of Bombay Nattiral History .Society vol. 19(1)
-vol. 31(4).
Bf.i.i,, T. R. 1910. The common butterflies of the plains of India.
72 Krgolis merione. Journal of Bombay Natural History Society
20: 319.
Btrc.os, C. L. 1981. Nutritional and life histoiy determinants of
resource allocation in holometaholous itisects. Atnerican
Naturalist I 17: 692-701.
Chris roi’tiFR M. S. M. & S. M vfhav.an. 1986. Population dynamics ofa
tr( ipical le|tido|3tcran CntopsiUa rroeale ( Pieridae) . Proceedings of
Indian Academy of Sciences (Animtil Sciences) 95(3): 303-324.
Fi.schfr, K., D. .M. O'Brifn & C. L. Boons. 2004. Allocation of larval
and adult resources to rejtroduction iti a fruit feeding butterfh'.
Functional Ecology 18: 656-663.
G.\v, T, 1. D. Ki Hi.MtLVR R J. C. Pt'NiniiA. 1992. Common butterflies
of India. Oxford University Press, Bombay. 67 pp.
Gunahiii.aoarai, K., T. N. A. PERfMAt. K. Javaicam &: M. Ganesh
Kumar. 1998. Field guide. Some .South Indian butterflies.
Nilgiri Wildlife &: Environment Association, Udhagamandalam,
India. 271 pp.
Haribai..\L 1992. The hutterilies of Sikkim Himalayas and their
natural history. Sikkim Nature (ionservation Foundation
(.SN(;F), Gangtok. 217 pj).
JttNF.s, R. E &• J. Ri INKS. 1987. Reproductive seasonality in the
tro|rical genus Eurema (Lepidoptera: Pieridae). Biotropica
19(1): 7-16.
Kuntf, K. 2000. Butterflies of Peninsular India. Utiiversities Press
(India) Limited, Hyderabad. 254|)p.
Kuntf. K. J. 1997. Seasonal ])atterns in hutterlly abundance and
s|)ecies diversity in four tropical habitats in northern Western
Ghiits. Journal of Bioscience 22: 593-603.
Leaky, D. J. & C. .M. Dei, Rio. 2001. It takes guts (and more) to
eat fruit: lessons from avian nutritional ecologv'. Auk 118:
819-831.
M.aih.aa'an, S. & T. J. Pandian. 1975. Effect of temperature on food
utilization in the monarch butterfh' Danaus chrysippus. Oikos
26: 60-64.
M.vnsoN, W. J. 1980. Herbivoty in relation to plant nitrogen
content. Annual Reriew of Ecololgv' and .Systematics 11: 119-
161.
Miniiab. 2003. Statistical SoftAvare 14.
Mu fhukrishnan.J. & T. j. Pandi an. 1987. Insect energetics, |5]3. 373-
511. In: Animal Energetics, Pandian, T. J. and F. J. Vernherg
(eds), Academic Press, Netv York.
Naaar, K. K., T. N. Ananth.akrishnan & B, V. D.aaid. 1976. General
and applied entomology. Tata McGraw Hill Company Lttl.,
NeAv Delhi. 590 pp.
20
/. Res.Lepid.
Owen, D. F. 1971. Tropical biiUoi flies. Clarendon Pre.ss, Oxford.
20,5 p.
Owen, I). K, |. Ov\t,n & 1). O. Cei.vnter. 1972. Sea.sonal changes in
relative abundance and estimates of species diversity in a family
of tropical butterflies. Oikos 2.S: 200-205.
F.M.\Ni(ai..\MV, S.. R. I’oNNUCii.wiY & T. Th.vnu.IiRXI. 1982. Effect of
temperattire on food intake, growth and conversion efiiciency
Eupterote mollip’ra (Insect: Lepidoptera) . Proceedings of
Indian Academy of Sciences (Animal Sciences) 91: 417-422.
P.vnuian T. |. & M. If M.\ri.\n. 1980. Prediction of assimilation
efiiciency in lepidopterans. Proceedings of Indian Academy
ofSciences (Animal Sciences) 95(6): 641-665.
Pan i , C. D. & N. C. Cii.vrrER|EE. 1950. A list of described immatitre
stages of Indian Le[)idoptera. Part 1. Rhopalocera. Indian
Forest Records (New' Series) 7: 213-225.
P,\iii.\K, .VI. & P. Q. Pi/A'i. 2003. Age specific stirvival and fertility
table ot Papilio demokus At different set of temperatures and host
plants. Indian Journal of Entomology 65(1 ): 123-126.
P()i,i.ARi), E. 1988. Teinjaerature, rainfall and bittterfly numbers,
joitrnal of Applied Ecology' 25: 819-828.
P01.1.ARI), E., J. N. Ce..vi()RE\-1)..\vie.s & |. A. Tiiom.as. 1997. Drought
reduces breeding success of the butterfly Aglais urticae.
Ecological Entomology 22: 31.5-318.
Pui.i.iN, A. S. 1987. C.bauges in leaf t]uality following clijjping and
I egrowtb in Urtira tiioicti, and consequences for a specialist insect
herbivore Aglais iirlirar. Oikos 49: 39-45.
ScRiiiER, J. .VI. 1977. Limiting effects of low’ leaf water content on
nitrogen utilization, energy budget, and lanal growth oi Hxlapliora
arropia (Lepidoptera: Saturniidae). Oecologia 28: 269-287.
SEN'riiAMi/,ii.sEi.v.4N, M. & K. .Vlt'RL'UAN. 1988. Bioenergetics and
rejrroductive ef ficiency of /l/rr/c/owe(/;/(rt cmitilalaF. (Orthoptera:
Insecta) in relation to food quality. Proceedings of Indian
Academy of Sciences (Animal Sciences) 97(6): 505-517.
Sev.vstopui.o, D. G. 1939. The early stages of Indian Lepidoptera.
Journal of Bomhay Natural Histoiy Society 41(1): 72-81 .
SiNGH.M., R. N. 1980. Relationships betw’een ecological efficiencies
of a herbivore and a carnivore insect. Indian Jotirnal of Ecology
7(1): 71-76.
Si.vnskvF. & j. M. Scriiser. 1985. Food consumjition and ittilization,
]3p. 8.5-163. In: Comprehensive Insect Physiology, Biochemistiy
and Pharmacology, Kerkuit, G. A. & L. 1. Gilbert (eds),
Pergamon, Oxford.
StAN.SKY, F. & P. Feeny. 1977. Stabilization of the rate of nitrogen
accitmulation b\ larvae of the cabbage butterfly on w'ild and
cultivated food jilants. Ecological Monographs 47: 269-228.
Venryia Rymana, S. P, |. B. Ati.uri & C. Si bba Reddi. 200 1 . Autecology'
of the common crow' butterfly. Ecology Environment &
Conservation 7(1): 47-52.
\'enk/\ta R.xmana, S. P., J. B. Atluri & C. Subba Reddi. 2003a.
Autecology of tailed jay butterflv Graphium agamemnon
(Lepidoptera: Rhopalocera: Pajiilionidae) . Journal of
Environmental Biology' 24(3): 29.5-303.
Venkata R,\mana, S. P., J. B. Ati.uri & C. Subba Reddi. 2003b. Biology
and food ittilisation efficiency oi Eumna hecabc (Lepidoptera:
Rhopalocera: Pieridae). Proceedings of the National Academy
ofSciences, India 73,B(1): 17-27.
W.M.DBAUER. G. P. 1968. The consutnption and utilization of food
bv insects, pp. 229-288. In: Beament, Treherne & Wigglesworth
(Eds.) , Advatices in insect physiology', Acadetnic Press, London
and New' York.
Wynter-Bi.vtii, M. a. 1957. Butterflies of the Indian Region.
Bombay Natural flistory Society, Bombay. 523 pp.
fournal of Research on the Lepidoftera
42: 21-33, 2003 (2010)
Larval feeding behaviour and myrmecophily of the Brenton Blue,
Orachrysops niobe (Trimen) (Lepidoptera: Lycaenidae)
David A. Edcif* and Hliib van Hambl'rc;
Scliool of Environmental Sciences and Development, North-West University, I’rivate Bag XOOOl. Potchefstrooni, 2.520, Sotith Alrica.
daveedge@xnets. co. za
Abstract. The larval feeding hehaviotir and myrinecophih' of the Brenton Bltie Orachrysops niohe.
an endangered polyommatine htitterfly from Knysna in Sotith Africa, were investigated by field
observations and captive larval rearing. The aerial and stihterranean parts of the Indigofera erecta
legtmie host plants were searched for O. niohe eggs, larvae and potential host ants. I’hird and
fonrtli instar larvae and ptipae were fotind in association witfi Camponotns baynei dwts on tfie host
plant rootstock. Ant colonies in viewable artificial C. baynei nests were sited near host jtlants
bearing nudtiple O. niobe eggs, bm no larvae were taken into the nests. Uannibalism was observed
between larvae raised in captivity on cm host plant. A third instar captive larva was enclosed
with a potted host plant connected to a similar artificial ant nest. The larva disappeared and was
later fotind feeding on the depleted plant rootstock, tended Itv the ants, and tfiis behaviour was
confirmed by field observations. O. niobe’s ant association is inferred to be obligate. Leguminous
Indigoferahosi plants have amino acid enriched rootstocks, wliich inav have pre-adapted the larval
digestive system to a cannibalistic or carnivorous lifestvle. I.arval growth characteristics are used
to compare African polvommatine genera and Orachrysops is intermediate fietween the facultative
myrmeco|thilous genera and the predaceous/parasitic Lepidochrysops species. A cladistic analysis
based on host jilants, ant associations and feeding behaviour leads to a hypothetical phylogenv
of the Af rican im i inecopliilotis jiolyoimnatines.
Keywords: myrmecophily, Orachrysops niobe. polyommatine, phytophagv', rootstock feeding.
Introduction
South Africa lias a wealth of niyrniecophiloiis
lycaeiiicls (Terblaiiche & van Hamburg, 2003), many
of which exhibit restricted ranges (endemism) and
are Red Listed species (Henning Sc Henning, 1989;
Henning et al, 2009). The phenomena of endemism
and rarity are believed to restdf from the narrow
environmental niches available to species that reqtiire
the overlapping jiresence of host plants and tending
ants (Pierce et al., 2002). Nearly all of the ohligately
myrmecophilous South African lycaenid butterflies
are in the tribes Aphnaeini and Polyouuuatiui (sensu
Pringle et al, 1994).
Orachrysops is a recently erected polyommatine
genus (Vari & Kroon, 1986), for which the life history
and myrmecophily of its 1 1 species and one subspecies
are little known. Clark and Dickson ( 1971) were otily
able to rear larvae of Orachrysops lacrimosa (Bethnne-
Bakei', 1923) to the end of the second instar, after
which the larvae died. Recent work on the two most
^Corresponding author
Received: 27 October 20()H
Accepted: 5 November 2008
endangered species in the genus has extended this
knowledge to all stages of their life history. Edge and
Pringle (1996) reported that the larvae oi Orachrysops
niobe (Trimen, 1862) were phytophagous in all instars
during captive rearing to the adult stage, and whilst
a dorsal nectary organ (DNO) was present no ant
association appeared to be necessary. Ln and Sainways
(2001; 2002a; 2002b) made field observations of
all larval stages and jDupae for Orachrysops ariadne
(Butler, 1898) and detected an apparently obligate ant
association with Camponotus natalensis (F. Smith).
Polyommatine larvae display a range of ant
associations, including predacious parasitism,
facultative mutualisms and myrmecoxeny (no ant
association). Larval diets vary from phytophagy to
entomophagy, or combinations thereof (Cottrell,
1984; Fiedler, 1991b; Fiedler, 1998; Pierce et al,
2002). Variation is evident within genera (e.g.
Maculinea) as well as between genera, with significant
implications for the ecology and population dynamics
of each species (Thomas et al, 1998). Consequently
extrapolations between even closely related species
can be misleading, and detailed field observations
as well as laboratoiy experiments are the only way to
establish with any certainty the laiwal diet and the exact
nature of the myrmecophily for each species (Thomas
et (d., 1989; Ehnes & Thomas, 1992).
99
/. Res.Lepid.
Materials and methods
Study site
riie study site was the Breiiton Blue Butterfly
Reserve (BBBR) at Breutoii-ou-Sea nearKuysnain the
Western (lape Province of South Africa. It has a total
area of 14.670 m-, is centred at co-ordinates 34®()4’2()”
S, 23-()2’()()” E, and lies at 90-115 metres above mean
sea level on a well-drained south-facing slope with an
average inclination of 1 in 3 (18°), vaiying between 10°
and 26°. The climatic, topographical and geological
featttres ol' the site and its vegetation communities
have been fully described elsewhere (Edge, 2005;
Edge et al, 2008a).
Field observations
All O. nioh('hos\ plants {ludigofera erertaThunhevg,
Eabaceae) were systematically searched for eggs
between November 2001 and April 2003 and all plants
with >5 eggs were searched repeatedly to detect the
j)resence of any larvae, pupae or ants, at various times
of day including the evening. The size, stage and
behaviour of any larvae discovered were recorded, and
samples were taken of ants for identification. Sizes
were meastired with a vernier scale using a hand lens.
Erom April 2002 not only were the leaves and stems
of the plants down to ground level searched, but also
some of tbe rootstocks were carefully excavated to a
depth of 2-4 cm.
Captive rearing on cut host plant
I lost plant sprigs bearing eggs were cut off and
placed in clear air-tight plastic containers 25mm
diameter x 55 mm high, with a drop of water
maintained in the bottom of the container to prevent
desiccation of the plant. The oviposition date (if
known), hatching date and all subsequent dates
and measurements were written on labels attached
to the container lids. If there were two or more ova
on a sprig, the larvae were separated into individual
coutainers on emergence. Every few days the contents
were carefully removed, the larvae examined and the
overall length (from the tip of the mandibles to the
end of the final segment for the first instar larvae,
and of the dorsal carapace for the second, third and
fourth instars) measured to an accuracy of 0.5 mm
with a vernier calliper. The containers were cleaned
otit with water and fresh cut sprigs of host plant were
inserted after careftilly transferring the larvae to the
new leaves. Erom the third instar onwards, the larvae
were transferred to larger flatter plastic containers 90
mm diameter x 50 mm high that would accommodate
larger pieces of host plant. Upon pupation, the pupae
were removed and placed on cotton wool under a
netting eclosion cage. Any adults emerging were
preserved as voucher specimens.
Artificial ant nests
Artificial ant nests similar to those used by Britton
(1997) 300 mm xl50 mm x 20 mm deep, with
labyrinthine passages, were made from wood with
sealed transparent tops, and covered by a detachable
hardboard lid to exclude light. Three queen right
colonies of the host ant Camponotus baynei Arnold
were collected on 5 October 2002, at a location away
from the BBBR, by breaking open decayed logs lying
on the ground under dense bushes. Each ant colony
was kept in a large plastic box 320 x 220 x 60 mm deep
with flnon (active ingredient: polytetrafluoroethylene)
coated walls to prevent escape, and the ants were
offered access into one of the artificial nests through
a translucent plastic tube. The ants quickly took up
residence in the artificial nests and feeding stations
were set up in the large plastic box where a 50%
v/v solution of sugar, plain water and chopped up
dead insects was provided. On several occasions a
third instar larva of O. riiobe on its sprig of host plant
was placed in the plastic box to observe any ant
interactions.
Two of these ant nests were slightly bitried (covered
with 10-20 mm soil) on 16 October 2002, close to
host plants on which a large number of O. niobeeggs
had been laid, to see whether butterfly larvae would
be taken into the artificial ant nest. Transhtcent
plastic tubing provided access from the ant nest to
the base of the host plant. The nests were inspected
every week until 27 January 2003, when one of the
nests was removed to the laboratory to prepare for a
captive rearing experiment (see below). The other
nest remained in the field until January 2004, when it
too was removed to the laboratory for another captive
rearing experiment.
Captive rearing with live host plant and ants
Two /. erecta plants were tratisplanted from the
field with their sitrrounding soil into pots I75mm
diatneter x 100 mm deep in December 2002, and
w'atered regidarly. An experiment was set up in
February 2003 with the two potted and caged /. erecta
plants, an artificial ant nest containing an ant colony
with brood of all stages, and one of the large plastic
boxes with atit feeding stations, all connected by clear
6 mtn diameter plastic tubes (Fig. 1 ). A 3“’ instar larva
42: 21-33, 2003 (2010)
23
Figure 1. Experimental set up for captive rearing with live host plant and ants
(7 mm long) was placed on each of the I. erecta plants
on 8 March 2003. The plants and the ant nest were
examined regularly to detect any larval activity and
any ant-larva interactions.
Morphology of the immature stages of O. niobe
Larvae were examined with a Wild M5
stereomicroscope at magnifications of tip to 50x.
The various stages were photographed under
magnification with a Nikon (loolpix E4600 digital
camera. Particular attention was given to the dorsal
nectary organs (DNOs), perforated cupola organs
(PCOs), tentacular organs (TOs) and the mandibles
of the 4"' instar larva.
Growth characteristics of O. niohe larvae and
comparison with other polyommatines
Data were obtained from Clark and Dickson (1971)
and Elmes et al. (2001) to enable a comparison to
be made between the growth patterns observed in
the early stages of O. niobe and other polyommatine
species.
Host plants recorded for other Orachrysops species
Data were obtained from variotis published sources
and from fellow lepidopterists of the host plants
recorded for the genus Orachrysops. Localities for
other Orrtc/try,5o/is species were \asited, the females were
observed ovipositing, and specimens were tiiken of the
host plants and sent to an expert for identification.
Ova of the Orac/nyvo/« species were collected and it was
confirmed that the larvae stirvived and fed on the host
plant on which they were laid. High magnification
photographs were taken of the eggs and the larvae
that hatched from them.
Results
Field observations - larvae and pupae
The 1*‘ and 2"'' instar larvae of O. niobe make 0.5
mm - 1.0 mm grooves in the epidermis and pali.sade
parenchyma of the glabrous uppersides of the leaflets
of I. erecta. When not feeding, the larvae descend to
the lowest part of the plant and rest on tlie stem in
a head-down position, making them very difficult to
find in the field.
The first 4‘'’ instar larva was discovered on 27 March
2002 at 15.50 pm on a cool, cloudy day. A vertical hole
abotit 8 mm diameter was alongside the rootstock of
this plant, from which several ants emerged. Down the
hole about 20 mm deep was a 4th instar larva, which
was careftilly removed for meastirement and found
to be 18 mm long x 4 mm wide, and then replaced
in the hole. A sample was taken of the ants and H.
G. Robertson of the South African Iziko Museum
identified them as Camponotus baynei Arnold. The
next day the larva had pupated (dimensions 12 mm
X 4 mm). A few days later the ptipa could not be
found, so possibly the attendant ants must have taken
it deeper underground.
Most of the subsequent observations were also
made later in the day and early evening, when the O.
^4
/. Res.Lcpid.
Figures 2-6. 2. O. niobe larval feeding marks can be seen on the 18mm diameter rootstock of I. erecta host plant, where 3
larvae were found at different times. 3. Rootstock of /. erecta showing feeding damage inflicted by larva of O. niobe (original
diameter of 6mm reduced to 2mm) (x20). 4. 2"'' instar O. niobe larva (2.5 mm long). 5. 3'"’ instar O. niobe larva (7mm long)
showing the head shield (Photos by D. A. Edge). 6. 4"' instar O. niobe larva (18mm long) showing an everted tentacular organ
(TO) on abdominal segment A8 (top right) (Photo by L. du Preez).
42: 21-33, 2003 (2010)
25
attendant ants appeared to be more active. On
two occasions two fully-grown 4‘'’ instar larvae were
found on the same I. erecta rootstock. In one instance
the C. originally in attendance were supplanted
by a Pheidole species (in large numbers), and the two
larvae could no longer be found. The ant attendants
were C. baynei in thirteen out of hfteen observations
made (seven 4'*' instar larvae; hve pupae and three
pupa cases) , with Camponohis berichti in attendance in
the other two cases.
Mature rootstocks of I. erecta are up to 18 mm
diameter (Fig. 2). The holes alongside the rootstocks
of I. erecta appear to be excavated by the C. ba^jnei-c\nis,
but these holes do not lead to ant nests. C. baynei was
only found to be nesting above ground in decayed
dead wood with holes bored out by a beetle larva,
and this was usually some distance away from the 1.
erecta plants.
Captive rearing with cut host plant
The size and duration of the early stages of O.
niobe during captive rearing on cut host plant are
summarised in Table 1. The few adults that were
reared were dwarfs, notwithstanding their rarity in
nature (Edge, 2008).
During the 2004 and 2005 captive rearing
experiments a number of new observations were
made. It was conhrmed that the first and second
instars (and presumably the third) normally consume
their shed cuticle, including the head capsule, after
ecdysis.
In April 2005 experiments were conducted
whereby pairs of well-fed fourth instar larvae were
placed in the same container with fresh host plant.
Within 24 hours in each case one of the larvae
disappeared and the survivor grew in size. In one
Table 1. Summary of the size and duration of the early
stages of O. niobe, reared on cut host plant.
Stage
Size
Duration
Ovum
0.6 dia X O.Snnn high
6 -7 days
P' instar
0.8 - 1 .5inm*
5 - 6 days
2'"' instar
1 .5 - 3. Omni*
8-12 days
3"‘ instar
3.0 - 7.5mm*
35 - 57 days
4"' instar
7.5 - 12.0mm*
26 - 61 days
Pupa
7.5 - 8.0mm
13 -23 days
Adult
10 - 13mm
L'p to 15 days
* For the larval instars the sizes are at the start and Hnish of
the instar.
instance the act of cannibalism was observed. Whilst
the prey larva was feeding on a host plant leaf, the
predator larva attacked it from behind and below,
through the soft ventral parts of abdominal segments
A7 and A8. After penetrating the integument with its
jaws, the predator larva sucked out the prey’s body
contents, eventually reducing it to just a skin and
head shield, which was also subsequently consumed
by the predator larva.
The prey larva thrashed about during the attack
trying to free itself, with the tentacular organs (TOs)
being very active. The predator lar%'a increased in
size from 9 mm to 1 1 mm before and after this attack.
The attacking behaviour appears to be calculated and
instinctive.
Artificial ant nests
Regular inspections of the artificial C. baynei ant
nests showed that the ant colonies remained healthy,
with stable abundances of adult ants and brood.
During the 1 03 days that the first nest was in place, no
larvae of O. niobe were observed inside the nest, nor
were any (). niobe larvae seen at all. The other nest
was in the field for 15 months and although the nest
remained active, no larvae were observed to come into
the nest. Both host plants had large numbers of O.
niobeeggs laid on them, and there is a high probability
that (). niobe larvae were in the immediate vicinity of
the nests.
Captive rearing with live host plant and ants
The two third instar larvae that were placed on the
two host plants could not be found after the first 24
hours. When the ants were given access to the plant,
they were observed crawling on the plant and on the
soil under the plant in the evenings, but no larvae
were detected. The larvae were also not seen in the
ant nest. Three months later, the plants were isolated
from the rest of the experiment and the soil around
the rootstock of the plants was carefully excavated.
Nothing was found around the rootstock of the more
healthy plant. The stems of the other plant were badly
withered and many were dead. A large hole (±20
mm) was discovered alongside the rootstock. The
plant became loose and it was lifted out of the hole.
A final instar O. nta/zclarva ( 1 5 mm long x 4 mm wide)
w'as clinging to the rootstock in a hunched position.
The rootstock was badly damaged (reduced to 2 mm
diameter from 6 mm).
This larva was observed for the next few months
with ants remaining in attendance at all times. Since
both the larva and the ants were photophobic, the
26
/. Res.Lepid.
larva was relocated to a vertical wooden box with a
red perspex translucent viewing window. The box
was filled with soil and a rootstock from a live plant
above was placed in a groove visible through the
window. Ants from the artificial nest were given
access, and were observed tending the larva and
imbibing secretions from the dorsal nectary organ
(DNO) . The larva mostly stayed on the rootstock until
it became clear that the larva was eating the rootstock,
cutting out deep grooves (Fig. 3). The length of the
larva was now about 18 mm. The larva eventually lost
interest in the rootstock, and accompanied by ants
made its way to the bottom of the box where the ants
had excavated a hole. The C. baynei ants continued
to imbibe secretions from the DNO, cover the larva
with soil when exposed to light, and occasionally
bodily carried the larva into deeper holes that they
had excavated. At no stage was there an attempt to
carry the larva into the ant nest, nor were the ants
observed to feed the larva by trophallaxis or any other
method. When the soil was excavated again on 5
August the larva had pupated (pupa 15 mm long),
still tended by the ants. The pupa was removed in
mid-October and placed under a hatching cage. A full
size male butterfly (forewing length 17 mm) eclosed
on 3 November 2003.
Morphology of the immature stages
The following features of the morphology of the
immature stages of O. niobe were not reported by
Edge and Pringle (1996). The 2'”' instar has much
shorter dorsal and ventral setae than the P' instar,
and already has active TOs (Fig. 4) . Tlie head shield
of the 3'^'* instar larva completely covers the head
(Fig. 5). The 4'’' instar larva frequently everts its
TOs (Fig. 6).
Comparative growth characteristics of
polyommatine larvae
The ratios between the lengths at the finish to the
lengths at the start of each larval instar are depicted
in Fig. 7. Note particularly the contrast between
the normally phytophagous taxa, Latnpides boeticus
(Linnaeus, 1767) and Euchrysops barkeri (Trimen,
1893), and the myrmecophagous species Lepidochrysops
palricia (Trimen & Bowker, 1887), Lepidochrysops
varinhilis (Cottrell, 1965) and Maculinea avion
(Linnaeus, 1767). The difference between O. niobe
reared purely on leaves cut from the host plant and
the same species reared on live host plant, including
rootstock and with ants in attendance, is also notable,
particularly in the 4’'' instar.
Host plants and ant associates recorded for other
Orachrysops species
The data currently available for the host plants
and known ant attendants for Orachrysops species are
summarised in Table 2. All host plants recorded so
far are in the genus Indigofera or the closely affiliated
genus Indigas trum.'And all ant associates yet known are
in the genus Camponotus.
Discussion
Phytophagy
The life histories of several Lepidochrysops species
have already been described:
L. patricia - by Clark and Dickson (1957).
L. variabilis - by Cottrell (1965).
L. methymna (Trimen, 1862) - by Clark and Dickson
(1971).
L. trimeni (Bethune-Baker, 1923) - by Claassens
(1972; 1974 and 1976).
L. ign.ota (Trimen & Bowker, 1887) - by Henning
(1983b).
L. plebeia (Butler, 1898) - by Williams (1990).
It was generally accepted from these observations
that the larvae of Lepidochrysops are mostly
myrmecophagous.
Clark and Dickson (1971) reared Orachrysops
lacriniosa (Bethune-Baker, 1923) as far as the start
of the 3"' instar, when the larvae died. When Vari
(1986) separated the genus Orachrysops from genus
Lepidochrysops Hedicke on adult morphological
Figure 7. Ratios between lengths at the finish and lengths
at start of larval instars for six polyommatine butterflies:
O. niobe 1 = reared on cut host plant; O. niobe 2 = reared
on live host piant with ants; E barken and L. boeticus =
Clark & Dickson 1 971 ; L. patricia - Clark & Dickson 1 957;
L variabilis = Cottreil 1 965; M. arion^ Elmes et al. 2001 .
SPECIES
42: 21-33, 2003 (2010)
27
Table 2. Host plants and ant associates recorded for Orachrysops species.
Orachrysops species
Indigofera host plant
Locality region
Camponotus ant associate
Sources
0. niobe (Trimen)
I. erecta Thnml>.
Brenton S. Cape
C. baynei Arnold
Williams, 19‘)(i; Lnbke et
at., 1997
(). firiftdne (Buder)
I. 7ww/;var. laxaW.
Bolii.s
Ivirlool KZN
C. nalatensis (F. Smith)
Ell K: Samways, 2001
0. tacrimosa (Betlume-
Baker)
I. nbscura N. F,. Br.
Cireylingstad Gauteng
Not known
Edge ]iersonal
observations 2004
(). tacrimosa (Betlmne-
Baker)
Indigastrum fastigium (E,
Mey.)
Verloren Valei
Mptimalanga
Not known
Edge persomil
observations 2004
(). brinkmarii Heath
I. dectinala E. Mey.
Kammanassie .S. Cape
Not know'll
Heath 1997
O. subraxnis G. A. & S. F.
Henning
I. woodiwAY. woodiiH.
Bolus
I. trislis E. Mey.
Wahroonga KZN
Camponotus sp.
Not known
Samways & I.tt, 2007
Lit, 2003
0. nasnlus nasulus G. A.
& S. F. Henning
1. elandsbergensis P. B.
Phillipson
I logsback E. Cajte
Not known
Edge personal
observations 2004
(). mijburghi G. A. & S. F.
I lenning
/. exiansiana Bnrtl Davy
Heilbron OFS
Not known
Pringe et at., 1994
(). near myburghi
I. dimidiata Woge\ ex
Walp. sensu stricto
Snikerbosrand Gauteng
Not know'll
Terblaticlie & FAlge,
2007
0. regalis G. A. & S. F.
Henning
I. accepta N. E. Br.
Wolkberg Eimjtopo
Not ktiown
Edge ]iersonal
observtuions 2004
(). warreni G. A. & S. F',
Henning
/. dimidiala \'ogel ex
Walp. sensn stricto
X'erloren \'alei
Mjttimalanga
Not ktiown
Edge personal
observations 2004
0. montanus G. A. & S. F.
Henning
I. di midiala Vogel ex
Wal|3. sensti lato
Golden Gate GFS
Not known
Edge jiersotial
observations 2004
N. B. All Indigofeni And Indigasirumphwu names deteriiiined bySchrire (200r)a)
grounds, the larvae of both genera were still assumed
to be myrmecophagous. Edge and Pringle (1996)
reared O. niobe larvae in captivity on host plant
cuttings without ants, and this discovery added a clear
biological jtistification for the separation of Orachrysops
fro m Lepid och rysops.
The O. niobe larvae reared on host j)lant cuttings
restdted in dwarf adtilts. In held observations P' and
2"^' instar larvae were nearly always fotind feeding on
the leaves of the host plant (with a single observation
of a P‘ instar larva feeding on the rootstock). 3”^
and 4''' instar larvae were always found tindergrotind
feeding on the rootstock attended by ants, and have
never been found feeding on the leaves. Rootstock
feeding in the Lycaenidae has only been recorded
once before. Jackson (1937) observed that the larvae
oi Eiiclirysops crawshayi crawshayi (Butler) fed “on the
fleshy otiter cortex of Cynoglossum coeruleum Hochst.
et D.C., Boraginaceae, always below the grotind; and
they are attended by many species of ants.” Rootstock
feeding in O. appears to be essential to produce
full size adults, since there is no evidence that the
diet of Orachrysops larvae incltides any ant provided
food. Rootstock feeding has also sidjsequently been
obseiA’ed in another Orar/ny.^e/As species (Terblanche
& Edge, 2007).
Rootstocks as a dietary source
Pierce (1985) noted that many myrmecophilotts
lycaenid larvae feed on nitrogen rich plants and
nitrogen rich parts thereof (such as flowers and
legtmie pods) . More recent work has questioned this
association (Fiedler, 1995; 1996), but the rootstock
feeding behaviour of the 3"' and 4"’ instar larvae of
O. accords with Pierce (1985), if the rootstock
is indeed protein rich. The rootstock of the legtime
I. erecta is a storage organ from which the plant can
resprout, storing carbohydrates and bearing nitrogen
fixing root nodules probably rich iu amino acids and
protein. Analysis of /. erecta leaves and rootstocks
showed that although their overall amino acid content
is quite similar (11600 nmol per g dry weight), the
rootstocks had more than double the content of
essential amino acids, particularly threonine, histidene
and allo-isoleucine. These amino acids could play
28
/. Res.Lepid.
an important role in the development of 4''' instar
larvae and pupae (e.g. threonine is important for
the synthesis of collagen, a basic constituent of the
more complex connective tissites generated in the
lepidopteran ptipal stage).
Cannibalism
Cannibalism by O. niobe larvae is another potent
source of protein. Freqtiently mtiltiple eggs are laid
on a single host plant (tip to 31 eggs were recorded),
so encounters between T', 2”'' and 3"' instar larvae
on the host plant (where attacks are most likely to
sncceed) must be quite freqtient. A larva grows rapidly
after it has successfully attacked and constmied one of
its siblings, and its sttrvival chances are considerably
enhanced. The habit that the larvae have of resting on
the lower thicker part of the stem no doubt protects
their vtilnerable ventral jjarts from such attacks. Laiwae
that stirvive long enotigh to reach and start feeding on
the rootstock are much better protected from attack,
since the thick dorsal integument (carapace) extends
down to the rootstock on both sides.
Morphological and behavioural adaptations of the
larvae of O. niobe
Cottrell ( 1984) described a ntimber of adaptations
of lycaenid larvae that enable them to ptirstie a
myrmecophilous life style. These adaptations have
great vahte in not only creating “enemyTVee space”
(At.satt, 1981 ), but also by providing access to a more
reliable nutritious diet restthing in more rapid growth
and larger adtilts (Pierce et al., 2002). A number of
these adaptations have been observed in the larx ae of
(). niobe. They have a thick, tough integument, which
defends the larvae from attack by the ants or from
conspecilic larvae. They have an onisciform body
shape with an expansion of the dorsal and dorsolateral
areas, which slope down to well-develo]>ed setadVinged
marginal ridges that can be brought in close contact
with the snbstrate, and seal off the ventral areas
inchiding the retracted head and legs. The ants (and
the larva’s siblings) therefore cannot gain access to
the softer ventral parts and vital organs when the larva
crawls or rests on a hard stibstrate.
(). niobe larvae have a dorsal nectary organ
(DNO) on the seventh abdominal segment in the
2"'', 3"'atKl 4''’ instars, producing a secretion that aids
myrmecojthily (Pierce, 1989; Fiedler & Maschwitz,
1989). 4’hey have tentacular organs (TOs) on the
eighth abdominal segment that appear to excite
the ants in attendance and draw them to the DNO
(C.laassens & Dickson, 1977; Fiedler & Maschwitz,
1987). The larvae of O. niobe '^ho have a number of
other adaptations not yet observed in other lycaenid
larvae, including powerful mandibles, which adapt
them for rootstock feeding and cannibalism, and an
ability to burrow in the soil - although the attendant
ants may assist this burrowing.
Larval shelter and overwintering
The sitbterranean, myrmecophilous lifestyle of
the larvae of O. niobe insulates them from extremes
of temperature and humidity changes; provides
protection from bres; and gives them access to a food
source (the rootstock) and a safe place to shelter
during the winter when the growth of the host plants
pauses.
Larval growth patterns
Dyar (1890) postulated that insect dimensions
increased by the same factor at each moult.
Phytocarniverous lycaenid larvae such as Maculinea
that parasitise ant colonies are exceptions to this rule
(Elmes et ai, 2001). Maculineei larvae show a normal
growth pattern during the first three instars, but after
adoption by their M-yrrairaant hosts, in the final instar
they increase in length by a factor of five, and by >50
times in mass (Elmes et al, 1991; Thomas & Wardlaw,
1992). Elmes et al. (2001) hypothesi.sed that these
growth patterns may have evolved to make the newly
moulted 3"* instar butterfly larvae approximately the
same size as the ant larvae at adoption and better able
to mimic the larvae of their ant hosts. Once in the
ant nest and accepted by the ants they could grow to a
larger size than other lycaenids becaitse of the readily
available, high quality food source.
In Eig. 6 it is clear that the phytocarnivorous
larvae of Maculinea and Lepidochrysops show similar
growth patterns. Whilst O. niobe larvae raised under
artificial (1) or natural conditions (2) have a higher
rate of growth in the third instar than any of the other
examples, in the final instar the growth rate of O. niobe
under natural conditions (2) is intermediate between
the phytophagous larvae {E. barkeri and L. boeticus) and
the phytocarnivorous larvae. Rootstock feeding may
be the key to the higher growth achieved in the final
instar relative to the normally phytophagous taxa.
Specialisation of Orachrysops associations
All the known host plants of the Orachrysops genu?,
are in the genus Indigofera or the very closely affiliated
genus Indigastrum (Table 2). Monophagy is common
in the localised species and allows such species to
42: 21-33, 2003 (2010)
29
Table 3. Ant associations of southern African polyommatine butterflies.
Key to third column [coding adopted from Fiedler (1991a)]
0 = No ant relationship (myrmecoxenous)
1 = Very few ant associations reported (weakly myrmecophilous)
2 = A varying proportion of larvae attended by ants (moderately myrmecophilous)
3 = Most if not all mature larvae ant-associated (steadily myrmecophilous)
4 = Larvae dependent on ants as commensals or parasites (obligately myrmecophilous)
** = DNO -r TOs
* = DNO only
= PCOs only
( ) = hypothetical
? = likely but not confirmed
Genus
Known ant a.s.sociates
Degree of
myermecophily
Sources
U ra n oth a u ma Butler
?
a
Ps/’udon/KYuiub/i Stem|)tfer
(0/1)
t'-g
Carireus Butler
(O/D*
a, c
Harpmdymts I leron
(0/1)*
c
Brephid'tum Scudcler
(1)**
c
Oraidium Bethune-Baker
(1)?
g
Tuxenlius Larsen
(1)**
c
ZiiUlia Eliot
(1)**
g
Ziziila Ghapman
(1)**
c
Actizera Ghapman
c
Lrploles Scudcler
Indeterminate
\
1
Zizina Ghajnnan
(2)^*
c
Cupidopsis Etarsch
a, c
Eirochrysops Bethuue-Baker
9**
c
Lampides Hubuer
('.ampoiiotii.s
Plagioli’pis
9^1:*
c, f
Zizeeria Ghapman
Papinoma
c, f
Azanus Moore
Pheidole
a, c. f
Chilades Moore
Pheidote
3**
c, f
Ihniru.s Moore
Plairiolepis
Monomorium
c, f
Euchrysops Butler
Monomorium
3:tc:tc
a, c
Oral hrysops Vari
Canipoiiiitiis
4**
i
Erpidochrysops I ledicke
Camponotus
4**
b, c, d. e
Sources: a = Jackson. 1937; b = Gottrell, 1965; c =
1991a; g = Pringle el at.. 1994; h = Williams, 1999;
Glark & Dickson. 1971; d = Glaaseus,
i = Lu & Samways, 2901.
1974 & 1976; e = Henning,
1983a; r= Fiedler,
avoid direct competition and co-exist at a locality
(e.g. O. lacrimosa and (). warreni at Verloren Valei and
O. subravus and O. ariadne at Wahroonga - Samways
& Lu, 2007).
Although only two ant associations are known as yet
for Orachrysops species, the ants concerned, C. baynei
and C. natalensis have some ecological similarities
(both are primarily nocturnal ants). C. baynei is only
found in fynbos or thicket and nests in dead wood
above ground level (Edge et at., 2008b), whereas C.
natalensis can be found in fynbos as well as grasslanrl
and nests in the ground (Lu & Samways, 20()2a).
Ant associates of South African polyommatines
The records of known or hypothesised ant
associations within the South African polyommatines
[members of the tribe Polyonnnatini as dehned by
30
/. Rfs.Lepid.
Eliot ( 1973) J are listed in Table 3. (Sotirces: Claassens,
1974, 1976; Clark & Dickson, 1971; Cottrell, 1965;
Fiedler, 1991a; Henning, 1983a; Jackson, 1937; Lu &
Samvvays, 2001; Pringle et al, 1994; Williams, 1999).
The coding system used in the final column has been
adopted from Fiedler (1991a).
Idle close affinities between Orachrysops and
Lepidochrysops wotild have always made a species of
Camponotus the most likely host ant for Orachrysops,
and this has now been confirmed for two of its species.
However, with only 1 1 out of 126 Lepidochrysops
species ant associates known (Pierce et al, 2002) and
2 otit of 1 1 Orachrysops ant associates known, there
is insufficient evidence to conclude that Camponotus
species are the only ant associates for both genera.
Nature of the ant association of O. niohe
3’'* and 4''' instar O. larvae were almost always
tended by the same ant, C. bayncL O. niohe s congener
O. ariadnehds only been fotind in association with one
ant (C. natalensis) (Lu & Samways, 2001). Cottrell
(1984) considered that relationships specific to one ant
species tended to be obligate. Even when more than
one ant species interacts with the larvae, in obligate
relationships one ant species is the most sticcessful
host (Thomas et al, 1989). Facultative relationships
by contrast tend to be formed with several species of
ant, even from different genera (Fiedler, 2001).
The larvae of O. niobe did not enter into ant nests
either in the field (artificial nests) or in the laboratoiy
The nests of the attendant ants found to date are
relatively remote from the plants on which O. niohe
feeds, but the plants need to be within the foraging
range of worker attendant ants so they can find the
larvae.
No trophallaxis or other feeding of the larvae by
ants has been observed. The larvae are rootstock
feeders in the later instars, and appear to need the
assistance of the ants to access the rootstock. After
pupation, clear access to the surface through a hole
or tunnel is necessary for the eclosed adult to escape
and expand its wings. Ants have been observed both
in captivity and in the field repositioning pupae and
their assistance may be essential to place the pupa in
a safe position to eclose. The balance of evidence is
therefore that O. niobe is obligately dependent on an
ant association with C. baynei.
Phylogenetic origins of Orachrysops and
Lepidochrysops
Various atithors have proposed phylogenetic
hypotheses regarding the origins and evolution of
lycaenid ant associations (Hinton, 1951; Eliot, 1973;
Fiedler, 1991b; Pierce et al, 2002). Hinton (1951)
believed that the possession of a DNO was a primitive
feature in the Lycaenidae, and that its absence was a
Figure 8. Hypothetical cladogram of the myrmecophilous polyommatine genera of South Africa based on genus of ant associates,
larval feeding behaviour and host plant families and genera.
Polyommatine genus Azanus Chilades Tarucus Euchrysops Orachrysops Lepidochrysops
AFRICAN POLYOMMATiNI
42: 21-33, 2003 (2010)
31
derived condition. Fiedler (1991b) pointed out that
the lycaenid subfamilies that were apparently more
primitive on other morphological considerations
(Poritiinae, Miletinae and Curetinae) were not
generally ant associated; whereas the more advanced
subfamily Lycaeninae [sensu Eliot (1973) = Theclini
+ Aphnaeini -i- Lycaenini + Polyommatini] contained
most of the myrmecophilous lineages. Within
Lycaeninae sensu Eliot Pierce ei al. (2002) predicted
that the Aphnaeini and certain subtribes of Theclini
would be shown to be basal and that Lycaenini and
Polyommatini were derived groups.
In Table 3, southern African polyommatine genera
are listed in ascending order of their degree of
myrmecophily. A tentative cladogram of the steadily
myrmecophilous polyommatine genera (denoted as 3
or 4 in Table 3) , based on genus of ant associates, lanal
feeding behaviour and host plants is presented in Fig.
8. Azanus and Chilades are associated with Pheidole
ants, which are the dominant ants in some habitats.
Tarucus is associated with a few ant genera, including
Camponotus. The genera Oreic/irysops, Euchrysops
and Lepidochrysops are predominantly Camponotus
associated. Ornchrysops has evolved rootstock feeding,
cannibalism, an obligate ant relationship and
specialisation on Indigofera. Euchrysops has a looser
ant association, and normal phytophagy, with the
exception of A. crawshayi. This interesting taxon has
genitalia similar to Euchrysops (Stempffer, 1967), facies
similar to Harpend.yreus, and larval behaviour with
features found in Orachrysops. It is of note that this
species has been placed in different genera by various
authors (by Butler in ScoUtantides\ by Aurivillius in
Harpendyreus Awd later Cupido\ by Jackson in Cyclirius;
and finally by Stempffer in Euchrysops) .
The larvae of Eepidochrysops are phytophagous
in the first two instars, and myrmecophagous in the
last two instars (they feed on the ant brood). This is
considered to be the closest ant relationship (Fiedler,
1998), with the larvae being treated as if they were ant
brood within the ants’ nests. It is here hypothesised
that the larvae of the common ancestor of the three
genera Euchrysops, Orachrysops, and Lepidochrysops
could have had rootstock feeding habits, which
physiologically adapted them to a higher protein diet.
Furthermore, the cannibalistic behaviour of O. niobe
larvae may have evolved in the common ancestors.
This wovdcl have enabled them to develop a taste
and a need for insect protein, a trait that could have
evolved in a sister lineage into the myrmecophagous
behaviour of Lepidochrysops larvae.
A higher protein diet may have made closer ant
associations possible because of the enhanced ability
to produce nutritious (high protein) secretions from
the DNO (Pierce, 1985). This would have enabled
the larvae to attract more ant attendants and given
them the opportunity to evolve more advanced
chemical camouHage and signaling skills (Fiedler,
1991b; 1998) . Such adaptations would have generated
further selective advantages in these butterfly lineages,
residting in more complex ant associations and
greater interdependence of the butterllies and their
ant associates.
Conclusions
O. niobe is a specialised organism, being
monophagons and having an obligate relationship
with a single ant species. Its habit of rootstock feeding,
which may be shared with other Orachrysops species,
distinguishes it from nearly all other afrotropical
polyommatines. A close phylogenetic relationship
between the genera Orachrysops, Euchrysops and
Lepidochrysops is inferred from a cladistic analysis.
Acknowledgements
(^apeNature is thanked ft)i' allowing access to the BBBR to
conditct research. The Green IVitst’s financial sn|t])ort is gratefully
acknowledged, and North West Lhiiversity kindly provided
a stereoinicroscope oti loan. Dr. Brian Schrire of the Royal
Botanic Gardens, Kew identified the Indigofera and Indigaslnim
specimens.
Literature cited
At.saii, B. R. 1981. Lycaenid butterllies and ants: selection for
enemy-free space. American Nattiralist 1 18: 638-6.'i4.
Bruton, D. R. 1997. Atit trajt nests enable detection of a rare and
localised butterfly, Arrodipsas myrmccophila (Waterhouse anti
Lyell) (Lepidt)]ttera: Lycaenidae) in the field. Menutirs of the
Miisetim of X'ictoria 56: 38.3-387.
Ct.vvssitNS, A. j. M. 1972. Lepidochrysops trimeni (Bethnne-Baker)
(Lepido|)tera: Lycaenidae) reared from larvae foitnd in the
nest of Camponotus maeulatusYAh. (Hytiienoptera: Formicidae).
Journal of the Entomological Society of South Africa 35: 359-
360.
Ci.vvssENS, A. |. M. 1974. Methods etnployed in the snccessfnl
retiring, tinder artificial conditions, of two Gape species of
Lepidochrysops (Lepidoptera: Lycaenidae). Journal of the
Entomological Society of South Af rica 37: 387-.392.
CiA-tssKNS, A. |. M. 1976. Observations on the myrmecophilous
relationships and the parasites of Lepidochrysops methymna
nuihymna (Tiimen ) and L. trimeni (Bethnne-Baker) (Lepidoptera:
Lycaenidae). Jottrnal of the Entomological Society of South
Africa 39: 279-289.
Claassens, a. j. M. & C. G. C. Dicicson. 1977. A study of the
myrmecophilous behaviour of the immattire stages of Aloeides
thyra (L.) (Lepidoptera: Lycaenidae) with special reference
to the function of the retractile tubercles and with additional
notes on the biology of tbe species. Entomologist’s Record and
Journal of Variation 89: 225-231.
Ci.ARR, G. G. & C. G. G. Dickson. 1957. The life-history of
Lepidochrysops patricia (Trim.) (Lepido|Dtera: Lycaenidae).
32
/. Res.Lepid.
lounial of the Entoinoloi>ical Society of South Africa 20(1):
I 11-117.
(ii .VRK, G. G. & (1. G. G. Dickson. 1971. Life histories of tlie Sotith
African lycaeiiid Ittitterflie.s. I’tirnell, Cape Town.
Co ri RKt.i., G. B. 1965. A study of the A/ct/ty?«t;('/-grotip of the genus
I .I'pidorhrysops l iedicke (Lejtidoptera: Lycaenidae). .Memoir of
the Entomological Society of Sotithern Africa 9: 1-1 10.
GoriRi i.i,, C. B. 1984. A|)hyto]tliag}' in hutterllies: its relationshijj
to myrmecophily. Zoological Jotirnal of the Linnaean Society
79: 1-57.
Dt.\R, 1 1. G. 1890. The ntimber of motilts of lepidopterotis larvae.
Psyche 5: 420-422.
Encr., D. A. 2005. Ecological factors infhiencing the stirvival of the
Brenton Bine butterfly, Oracltiysops niobe (Trimen) (Le]>idoptera:
Lycaenidae). North-West University, Fotchefstroom. (Thesis
- D. Phil.)
Enor., D. A. 2008. Adult behaviour of Orach ijsops itiohe (Trimen)
(Le|)ido|ttera: Lycaenidae). Metamorphosis 19(3): 116-126.
E.ih;e, D. a., S. S. Gii.i.iers. &: R. F. Tr.RittANCHE. 2008a. Vegetation
associated with the occtirrence of the Brenton Bine bntterfly.
South Af rican Journal of Science 104: 505-510.
Edoe, D. a., M. G. Roberison & H. V.an H.VMiiURt.. 2008b. Ant
assemblages at jrotential breeding sites for the Brenton Blue
btilterllv Orarhrysryps (Trimen) (Lepidopteni : Lycaenidae).
African Entomolog)' 16(2): 259-262.
Eix.e, 1). A. & E. 1.. Prinoi.e. 1996. Notes on the natnrtil history
of the Brenton Bine Orachry.sops niobe (Trimen) (Le]tidoptera:
Lycaenidae). Metamoiphosis 7(3): 109-20.
El lot, J. N. 1973. The higher classification of the Lycaenidae
(Le]rido|5tera): a tentative tirrangement. Btilletin of the British
.Vlnseiim (Nattiral Llistory) Entomolog}' 28: 37.3-516.
Femes, G. W. & |. A. d'noM.vs. 1992. Comjrlexity of species
conservation in managed habitats: interaction between
MacuHnea butterflies and their ant hosts. Biodiversity
Conservation 1(3): 155-169.
Femes, G. W., j. A. Tiiom.vs, M. I,. Mt'N(;uiR..\ & K. Fiedeer. 2001.
Larvae of lycaenid btitterflies that |tarasitise ant colonies |trovide
exceptions to normal insect growth rules. Biological |oin nal
of the Linnaean Society 73: 259-278.
Femes, Ci. W., J. G. W.vrde.wv & |. A. Tiiom.vs. 1991. L.arvae of
Maculinea rebeli, a large-bhie btitterfly and their Myrmira host
ants: patterns of cateipillar growth and stirvival. Journal of
Zoology 224(1): 79-92.
Eieoeer, K. 1991a. European and northwest African Lycaenidae
and their associations with ants, [otirnal of Research on the
Lepidoptera 28(4): 239-257.
Fiedeer, K. 1991b. Systematic, evohttionary, and ecological
implications of mvrmecophilv within the Lycaenidae
(Insecta: l.epidojjtera: Papilionoidea). Bonner Zoologisches
Monographien 31: 1-210.
Fiedeer, K, 1995. Lycaenid butterflies and jjlants: is myrmecophily
associated with partictilar host plant preferences? Ethology,
Ecology and Evolution 7: 107-132.
Fiedeer, R, 1996. llo.st-|)lan( relationships of lycaenid btitterflies:
large-scale patterns, interactions with jtlaiit chemistry, and
nuittialism with ants. Entomologia Experimentalis et Applicata
80: 259-267.
Fiedeer, K. 1998. Lycaenid-ant interactions of the Maculinea lype:
tracing their historical roots in a comparative framework.
Jotirnal of Insect Con.servation 2: 1-1 1.
Fiedeer, K. & IVfAsoHwrr/, U. 1989. Etinctional analysis of the
niyrnieco])hilotis relationshijrs between ants (1 lymenoptera:
Eormicidae) and lycaenids (Lepidoptera: Lycaenidae). 1.
Release of food recrtiitment in ants by lycaenid larvae and
pupae. Ethology 80: 71-80.
1 Ieaiii, a. 1997a. Description of a new species of ( )rachrysops\' Ai'i
from the western (ia|)e pror ince of Sotith Africa (Lepidoptera-
Lycaenidae). Metamorphosis 8( 1 ): 26-32.
Hennino, (L a., R. F. Terbianche & J. B. B.m.e (eds.). 2009. South
African Red Data Book - Btitterflies. South African National
Biodiversity Instittite, Pretoria, (in press).
Hennino, S. F. 1983a. Biological groups within the Lycaenidae
(Lepido|ttera) . Jotirnal of the Entomological Society of
Sotithern Africa 46: 65-85.
Hennino, S. E. 1983b. Chemical commtmication between lycaenid
larvae (Lepidoptera: Lycaenidae) and ants (Hymenoptera:
Eormicidae) [Aloeides dentath, Acantholepis capensis, Lepidochry.wps
ignola, C.amponolus niveosetosus]. Journal of the Entomological
Society of Southern Africa 46(2): 341-366.
Hennino, S. F. 1 984. The effect of ant a.ssociation on lycaenid larval
duration (Lycaenidae: Lepidoptera). Entomologist’s Record
and Jotirnal of Variation 96: 99-102.
Hennino., S. E & G. A. Henning. 1989. Sotith Af rican red data book:
butterllies. South African National Scientific Programmes
Report 158. Council for Scientific and Inditstrial Research,
Pretoria.
Hinton, H. E. 1951. Myrmecophilons Lycaenidae and other
Lepidoptera: a summaiy. Proceedings of the South l.ondon
Natural History Society 1949-19,50: 1 11-175.
JAOK.SON, TIL E. 1937. The early stages of some African Lycaenidae
(l.epidoptera), with an accottnt of larval habiLs. Transactions of
the Royal Entomological Society of London 86(12): 201-238.
Lu, S-S. 2003. Biology atid conservation of the threatened Karkloof
blue btitterfly Orcichrysops ariadne (Btitler) (L.epidoptera:
Lycaenidae). University of Natal, Pietermaritzburg. (Thesis
- D. Phil. ) 112 jt.
l.u, S-S. & M. J. Samways. 2001. Life history of the threatened
Karkloof bhie btitterfly, Orachrysops ariadne (Lepidoptera:
L.ycaenidae). African Entomology 9(2): 137-151.
Lu, S-S. & M. J. S.AMWAVS. 2002a. BehaMounil ecology of the Karkloof
blue butterfly, Orachrysops ariadne (l.epidoptera: Lycaenidae)
relevant to its conservation. African Entomology 10(1): 137-
147.
Lu, S-S. & M. J. Samways. 2002b. Conservation management
recommendations for the Ktirkloof blue butterfly, Orachrysops
rtt7rtt/Hc(Lepido|)tera: Lycaenidae). African Entomolog)' 10(1):
149-159.
Pierce, N. E. 1985. Lycaenid butterflies and ants: selection for
nitrogen fixing and other protein rich food plants. The
American Nattiralist 125: 888-895.
Pierce, N.E. 1989. Bntterfly-ant mtuiialisms, pp. 299-324. /«: Grubb
P. J. & Whittaker, J. B. (eds.). Towards a more exact ecolog)’.
The 30th .sym|jositim of the British Ecological .Society. Blackwell
Scientific Publications, I.ondon.
Pierce, N. E., M. F. Braby, A. Hiatii, D. J. 1.ohman,J. M.vnTiEW, D.
B. Rand & M. A. Tr.\v.\ssos. 2002. The ecology' and evohition
of ant association in the Lycaenidae (Lepidoptera). Annual
review of entomology 47: 733-771.
PRiNot.E, E. 1,., G. A. Henninc, & j. B. B.m.e. 1994. Pennington’s
Btttterflies of Sotithern Africa. 2'"' edition. .Struik Winchester,
Cape Town. 800 pp.
Stemi’efer, H. 1967. The genera of the African Lycaenidae
(Lepidoptera: Rhopalocera). Bulletin of the British Miisetim
(Natttral History) Entomology' 10.
S.VMWAYS, M.J. K- .S-S Lu. 2007. Key traits in a threatened butterfly and
its common sibling: implications for conservation. Biological
Conservation 16: 409.5-4107.
Sw.ANE.i’OEE, D. A. 1953. Btitterflies of South Africa. Maskew Miller,
Cape Town. 320 pp.
Terbi.anciie, R. F. & H. Van Hamburg. 2003. The taxonomy,
biogeogra])hy and conservation of the myrmecophilotis
CJirysorilis btttterilies (Le|>ido|ttera: Lycaenidae) in Sotith
Africa. Koedoe 46(2): 65-81.
Terbianche, R. F. & D. /V. Edc.e. 2007. The first record of an
42: 21-33, 2003 (2010)
33
0?w/ir)’io/M I'roni Gauteng. Metamorphosis 18(4): 131-141.
Thomas, J. A., R. T. Ci.arkk, G. W. Ei.mes & M. E. 1 Iocmberu. 1998.
Population dynamics in the genus Marulhira (Lepido]jtera:
lA'caenidae), pp 261-290. In: Dempster, J.P. & McLean, L.F.G.
(eds.). Insect Populations. Kluwer Academic Publishers,
Dordrecht.
Tuom.vs, J. a., G. W. Ei.mes, J. C. W.aruiaw & M. Wowciechowski.
1989. Host specificity among Maculinea butterflies in Myrmka
ant nesLs. Oecologia 79(4): 4.52-457.
Tuom.vs, J. A. & J. C. W.vrdiaw. 1992. The cajjacity of a Myrmira
ant nest to support a predacious species of Maculinea btitterfly.
Oecologia91(l): 101-109.
V.vri, L. 1986. Introduction, pp. vii-x. /w: Vari, L. & Kroon, 1). 1986.
Southern African l,e])idoptera - a series of cross- referenced
indices. The Lepido])terists' Society of Southern Africa & The
Transvaal Museum, Pretoria.
Wii.t.iAMS, M. G. 1990. Gbservations of the biolog)' oi Lepidorhrysops
plehela plebeia (Butler) (Lycaenidae: Polyomattinae) .
Metamorphosis 1(27): 10-1 1.
Wii.i.iAMS, M. G. 1996. Report on research findings concerning the
life history and ecology of the Brenton Blue ( Orarhrysops niohe) .
Metamorphosis 7(1): .3-7.
Wii.i.iAMS, M. C. 1999. Taxonomical changes affecting the
afrotropical butterflies and skippers (Lepidoptera) since
the ptiblication of Garcasson's Butterflies of Africa - Part 1:
Lycaenidae. Metamorjrhosis 10(2): 52-69.
journal oj Ri'searrh on the Lepidoptera
42: 34-49, 2003 (2010)
Life history of the Imperial Moth Fades imperialis (Drury) (Saturniidae:
Ceratocampinae) in New England^ U.S.A.I distribution^ decline, and
nutritional ecology of a relictual islandic population
Paul Z. Goldstein
1 1 1 Gay Head Ave., Vineyard Haven, MA 02568.
drpzgoldslein @gmail. com
Abstract. The decline and current status oi Earles impeiialis (Drury) (Saturniidae: Ceratocampinae)
in New England are re\4ewed, and primary data surrounding the life history and nutritional ecology
presented. Though common throughout much of its historical North American range, this species
declined precipitously in New England during the 20''' century. Suggested explanations for this
region-wide decline include the deployment of pesticides and metal halide street lamps and the
introduction of parasitoid flies. The existence of a remnant population of E. mperialis, thought to have
been extirpated from New England as early as the 195()s, is reported from Martha’s Vineyard Island,
Dukes County, Massachusetts, U.S.A., representing the last relict of a phenotypically, phenologically,
and possibly ecologically infrasubspecific entity. Based on comparisons with museum specimens,
adults from this population appear to be indistinguishable from the few historical specimens known
from nearby mainland Massachusetts, smaller than those from now extirpated populations in
Connecticut, New York, and New Jersey, and slightly larger than members of, the northernmost E.
/m/tcnVf/A populations (£. i. /tinlMichener) found in the Great Lakes region. The Martha’s Vineyard
population is univoltine, peaking in late July and exhibiting a more contracted flight season than
other extant North American populations. Both parentage and food plant significantly affect larval
growth and development, and although laiwae on Martha’s Vineyard feed extensively if not exclusively
on pitch pine (Pinus rigida) in the wild, they grow significantly faster, attain greater pupal weights,
and more efficiently convert ingested and digested tissues of post oak (Qiierrus stellata) to biomass
in the laboratory. Performance as measured by relative growth rate and the efficiency of conversion
of ingested and digested food to biomass (ECI and ECD) are correlated with foliar nitrogen and
water content: post oak foliage during the larval growth season contains more nitrogen and water
than corresponding amounts of pitch pine foliage growing in the same soils. It is suggested that
there exists a non-ntitritional explanation for the association of E. imperialis with pitch pine and for
its pattern of decline and persistence. The taxonomic and possible biogeographic affinities of this
population are discussed from within the context of a growing understanding of New England’s
diverse yet threatened lepidopteran fauna, and the potential for reintroducing E. imperialis to
mainland New England is discussed.
Keywords: Earles imperialis, invertebrate conservation, Martha’s Vineyard, pitch pine.
Introduction
The imperial moth Eacles imperialis (Drury)
(Saturniidae: Ceratocampinae), is one of North
America’s largest and familiar saturniids. Throughout
its extensive range, this species exhibits considerable
regional variation in coloration and size — on the basis
of which three North American subspecific epithets are
currently attributed — as well as variation in phenology
and liost plant utilization (Ferguson, 1971; Coveil,
1984; Tiiskes et ai, 1996) . Considered a common moth
in tlie southern United States, E. imperialis, like many
large bombycoid moths, underwent a precipitous
decline in much of northeastern North America
during the mid-2()''' century (Hessel, 1976; Ferguson,
liereived: 24 July 2006
Accepted: 24 August 2006
1971; Schweitzer, 1988). Ferguson (1971: 25) writes
“[the imperial moth]... like some of the other large
saturniids, is said to have largely disappeared from
heavily populated areas such as those in Connecticut
and the vicinity of New York City, where it was
formerly common.” Various hypotheses for such
declines, ranging from the expanded use of metal
halide bulbs in street lamps (Hessel, 1976) to the
widespread deployment of pesticides aimed at gypsy
moths (Goldstein, 1991) and to the introduction of
parasitoids, specifically the tachiiiid fly Compsilura
concinnata, for the same purpose (Boettner et al,
2000) have been invoked to explain these declines.
Believed extirpated from New England, a relict
population of E. imperialis was verified by the author
in 1982 on Martha’s Vineyard Island (Dukes Co.), off
Cape Cod, Massachusetts, where it quickly became of
interest to conservationists. In this paper, following a
42: 34-49, 2003 (2010)
35
review of the taxonomy and regional variation in this
species complex, I present life histoiy obseiwations and
larval growth and performance data on this population
between 1986 and 1989, discuss this species’ decline
by summarizing historical records and information
on pesticide deployment and parasitoid impacts, and
discuss the nutritional and life history requirements
of this species in light of putative reestablishment on
mainland New England.
Distribution and variation in the Fades imperialis
complex in North America
Extending from (lanada to Ai gentina, the imperial
moth E. imperialis is both the widest-ranging and the
northernmost occurring species in its genus and one
of the most widely distributed saturniids that occurs
in North America (Lemaire, 1988), representing a
complex of ecologically and possibly phylogenetically
distinct intra-nominal entities. Authors have differed
in their treatment of subspecific epithets, variously
recognizing the western E. oslari as a fidl species
versus a subspecies of imperialis and the southern E.i.
nobilis Neumoegen as a subspecies versus a synonym
of nominate imperialis (reviewed in Tuskes el al, 1996) .
Not including these, two recognized subspecies of /f.
imperialis occur in North America (Eemaire, 1988;
Tuskes ei al, 1996): the nominate subspecies and E.
i. pini, which is distributed in the Great Lakes region
and the Adirondacks.
According to Eerguson (1971: 24), E. imperialis
“occupies nearly all of the United States east of the
Great Plains, with the exception of northern New
England and northern portions of Michigan and
Wisconsin.” Eerguson (1971: 25) further reports
records “from southern New Hampshire... through
New York State, the Niagara Peninsula of Ontario,
and southern Michigan, westward to the eastern edge
of the Great Plains, and southward to the Gulf Goast
and southern Florida (but not the Florida Keys). It
has not been taken in Maine.” The New England
states are represented by specimens in collections at
the American Museum of Natural History (AMNH),
the Museum of Gomparative Zoology, (MCZ), the
Peabody Museum of Natural History (PMNH), which
houses the bulk of the F. M. Jones collection from
Martha’s Vineyard, and the collection of the now
defunct Boston Society of Natural History (BSNH),
which curreittly resides at Boston University (Fig. 1).
A single 1900 specimen from Kittery Point (southern
Maine’s York Gounty) is housed at the MGZ, and Patch
(1908; cited in Tuskes et al. [1996: 65]) reported it
from Girmberland Gounty, ME. Beyond these r ecor ds,
Farquhar’s (1934) thesis enumerated various other
Figure 1. Historical distribution of E. imperialis in New
England by county. Arrow indicates presence of lone
extant population on Martha’s Vineyard Island, Dukes
Co., MA.
New England r ecords, also included in Fig. 1.
The species’ crrrrent occurrence iir the
rrortheastern portion of its range sorrth of New
Errgland, iirchtdiirg Long Island, N. Y. and southern
New Jer sey, is associated at least in part with habitats
char acter ized by sandy soils such as pitch piire-scr uh
oak barreirs, where its larval host plant, pitch j)ine
{Pinas rigida), aboutrds. Srrch habitats have been
heavily impacted, in large part due to the ease with
which sandy soils are maniprrlated for building and
constrirction pitrposes. Sandy, well-drained soils
nray be a requirement for Eacles imperialis in that,
like all ceratocarrrpine satrrnriids, Eacles lar vae do
not constrirct cocoons but burrow into and pupate
within the soil, from which the pupae themselves
emer'ge so that the adults may edose above-gr'ound.
The cotrspicrroits dearth of historical recor ds fr om
Gape God, where sandy soils predominate, may
he attributable to a combination of small |)rivate
collections’ having been orphaned.
Each'S imperialis exhihxis apparently clinal variation
in wing maculation and shading as well as in size and
pherrology, with southern popirlations (formerly
attribirted to E. i. nobilis) often exhibiting rrror e intense
bi'owtr postmedial shading than northern poprrlations.
It has also been observed that adrrlt individuals
of northern popirlations attributed to E. i. pini in
36
J. Res.Lepid.
nortliern Michigan , Ontario, Quebec, and New York,
are markedly smaller than their southern and eastern
coimteiparts (Ferguson, 197l;Tuskes etaL, 1996), and
bear more intensive peppering with blackish spots; the
larvae exhibit pronounced dorsolateral scoli relative
to nominate imperialis. The maciilation on specimens
taken from Martha’s Vineyard is consistent both
with museum specimens from the island and with
those taken from mainland New England prior to
the species’ decline there. Based on an examination
of these and other specimens from the northeast,
the mean forewing length for male E. imperialis
from Martha’s Vineyard was 49.64 mm (N = 60, se =
.401), significantly smaller than that of 78 specimens
examined from New York, Connecticut, and New
Jersey (one-way AN OVA, p < .0001, DF = 1, F-ratio
= 88.241; Fig. 2), and at the lower end of the range
of 47.59 mm reported by Tuskes et al. (1996). This
number is higher than the average male wing length
of 47 mm reported for A. i pinihy Michener (1950) in
the original description and out of the 42 mm - 48 mm
range reported for male pini by Tuskes et ai (1996).
Michener (1950) also reported an average wing length
of 54 mm for male nominate imperialisfrom the vicinity
of New York City; specimens I measured from this
area averaged 54.92 mm (N = 36, se = .92), by way
of comparison. Although female wing lengths for
mainland New England specimens were not analyzed
due to their scarcity in collections, Martha’s Vineyard
female specimens averaged 57 mm in wingspan, just
below tlie range of 58-68 mm reported by Tuskes et al,
greater than tlie 51 mm average pini female wingspan
reported by Michener and out of the 47 mm - 54 mm
range reported for pini by Tuskes et al
The familiar green/brown larval polymorphism
of E. imperialis is apparent both among lab-reared
caterpillars and those obseiwed in the wild on Martha’s
Vineyard. Both maternity and food plant affect the
expression of this polymorphism: among the larvae
reared for this study and in situ (P. Goldstein, unpubl.) ,
the lime green color form was less prevalent than the
dark brown, with the majority of reared green larvae
developing on pine versus oak. Ferguson (1971: 26)
writes that “[a] brood from Massachusetts, described
by Eliot and Soule [1902], contained only one green
larva.” Flarris (1890: 404), on the other hand, writes
“[the caterpillars are] for the most part, of a green
color, slightly tinged with red on the back; but many of
them become more or less tanned or swarthy, and are
sometimes found entirely brown.” During the course
of my rearing, I observed seven cases in which larvae
switched from brown to green at one molt only to shift
back at a subsequent molt; a common color morph
of oak-fed larvae. The most common color morpli
Figure 2. Mean forewing length (base to apex, in mm)
of 1 38 male Eacles imperialis from Martha’s Vineyard,
Connecticut, New York, and New Jersey. The mean
forewing length for male E. imperiaiis from Martha’s
Vineyard was 49.64mm (N=60, se=.401), significantly
smaller than that of specimens examined from New York,
Connecticut, and New Jersey (one-way ANOVA, p<.0001 ,
DF=1 , F-ratio=88.241). See text.
* of Individuals
Observed
Figure 3. Flight season of E. imperialis on Martha’s
Vineyard, 1984-1989 inclusive, based on observations of
107 individuals, 86 male and 21 female (see text).
of oak-fed larvae is orange to reddish brown, often
with the spiracles and dorsolateral scoli surrounded
by paler patches.
With respect to life history timing, Harris (1890:
404) writes: “The moth appears here [Massachusetts]
from the 12''' of June to the beginning of July, and
then lays its eggs on the buttonwood [sycamore,
Liquidambar sty rad folia] tree. The caterpillars maybe
found upon this tree, grown to their full size, between
the 2()th of August and the end of September, during
which time tliey descend from the trees to go into the
ground.” Phenologically, based on a sample of 107
individuals (86 male, 21 female) collected or observed
42: 34-49, 2003 (2010)
37
on Martha’s Vineyard between 1982 and 1989, the
population is protandrous, and both males and
females peak at the end of July: 65% (56) of the males
were observed between 21 July and 1 August, and 71%
(15) of the females were observed between 25 July
and 1 August (Fig. 3). This flight season is consistent
with the collection dates of museum specimens from
the nearest known mainland historical records (e.g.
Cohasset, MA; Bristol, RI), has remained predictable
in the years since this study was conducted, and may
represent a more contracted flight season than that
reported in Tuskes et al. (1996) for northern E. i.
imperialis. Most indiMduals appeared at lights after
2200h, and individuals were observed coming to light
until 040()h.
Taken collectively, these observations hint at the
possibility that northern E. imperialis represents at
least one and possibly two biological entities distinct
from southern imperinlis. It is noteworthy that Lemaire
(1988: 31) portrays the range o^ E. i. pmii\s crossing
the Appallachian divide to northern New England.
Although there exists a phenetic similarity of adult
New England specimens to individuals typical of T. i.
piniwith respect to size and macnlation, the diagnostic
characters of adult and larval pini (Tuskes et al, 1996:
67, 68; Pis. 1 , 7, & 8) do not appear in specimens from
New England. Historically, the superficially clinal
nature of variation in this complex has presented
obstacles to a clear understanding of what may be
taxonomically and biologically distinct natural entities.
Notwithstanding the perhaps controversial criteria on
which the retention of saturniid snbspecific epithets
rely (Goldstein, 1997; but see Tuskes et al, 1996 for
an alternative viewpoint), the similarities between
nominate E. impeiialis cmd E. i. pini in wing macnlation,
size, phenology, and especially host plant use are
relevant to the holobiology of this complex. It is
conceivable that the small size of E. i. pini and the New
England T. i. imperialism s related to the combination
of a short growing season and an apparently exclusive
association with pines at northern latitudes. I would
recognize E. pini as a full species and anticipate that
the northeastern, pine-feeding popidations of E.
imperialis and those comprising pini will ultimately
be recognized as separate sister species. Since the
type locality of Earles imperialis is in New York, I would
further anticipate that nohilis be resurrected.
Eacles imperialis on Martha’s Vineyard: past and
present
Jones and Kimball (1943), in their extensive
treatment of the Lepidoptera of Martha’s Vineyard
and Nantucket Islands, described E. imperialis as
Figure 4. Current distribution of E. imperialis on Martha’s
Vineyard as of 28 August, 2009. Courtesy Massachusetts
Natural Heritage & Endangered Species Program.
Westboro, MA.
occurring regularly on Martha’s Vineyard, where it
persists and is widely distributed on both moraine
and ontwash plain soils (Fig. 4). It is not known
from Nantucket, and virtually all mainland New
England specimens deposited in museum collections
I examined were taken during the first half of the
20th century, with only a few taken as late as the early
1950s. By all accounts, this species had essentially
declined dramatically in New England more than a
decade before Ferguson’s (1971) publication, and
indeed was considered extirpated from Massachusetts
during the early drafting stages of the Massaclursetts
Endangered Species Act (MESA; M.G.L. c. 131Aand
regulations 321 GMR 10.00). It is currently listed as
“threatened” in Massachusetts.
The decline of A. imperialism northeastern North
America is not tiniqne, but rather consistent with
a well-known pattern of decline among saturniids
(Hes.sel, 1976; Fergitson, 1971; Frank, 1988; Schweitzer,
1988). In fact, the three most dramatic declines of
saturniids in New England have been ceratocampines:
E. imperialis, the royal walnut moth Citheronia regalis
(Fabricius) , another of North America’s most massive
saturniids, and the pine devil moth C. sepulcralis Grots
& Robinson, another barrens species that feeds on
pine and the type locality of which is Andover, MA.
Martha’s Vineyard appears to have served as a
regional refugium for several species (e.g. Actias
Inna) that remained extremely abundant on the
island while undergoing anecdotal declines — even
temporaiy ones — on the mainland. It is not at j)resent
possible to single out any one of the various possible
causes for these declines; none are mutually exclusive.
Moreover the weak coincidence of the deployment
38
/. Res.Lepid.
of metal halide street lights and pesticides several
decades following the introduction of the tachinid fly
Compsilura concinnata (Diptera: Tachinidae) in 1906
to combat gypsy moths and other pests (Howard &
Fiske, 1911) makes parsing the relative importance of
these factors difficult. In hindsight, it is not surprising
that the sole New England population of E. imperialis
to persist did so on an island that was not as heavily
subjected to as heavy aerial deployment of pesticides
or high-wattage metal halide streetlights, or to the
intentional release of parasitoids, as the mainland.
Available data on the use of DDT and other
pesticides, recorded on a per-county basis between
1948 and 1965, indicate that Dukes Co. (including
Martha’s Vineyard) was one of four counties sprayed
only once during this period, and was subjected to
less intensive treatment (as measured by total spray-
acres) than any other county in the Commonwealth
excepting Middlesex (Bewick, 1979, reproduced in
Table 1). Martha’s Vineyard is approximately 100
square miles, or 64,000 acres; its single documented
pesticide treatment of 17,000 acres in 1956 is less
intensive, for example, than the 31,071 acres sprayed
on Nantucket, whose land mass is roughly half that
of the Vineyard; and far less than the hundreds of
thousands of acres of maritime barrens habitats in
Plymouth and Barnstable comities routinely subjected
to spraying before the use of DDT was discontinued.
Prior to the widespread deployment of DDT, the
parasitoid fly C. concinnatah'Ad become well-established
in New England, shortly after its 1906 introduction
(Culver, 1919) . Introduced to combat the gypsy moth
Table 1. Massachusetts DDT spray history 1948-1965
(Reproduced from Bewick, 1979).
County
Total
spray-acres
# Years
treated
Avg. acres
sprayed per
treatment year
PKniouth
525,962
5
105,193
1 taiii])shire,
1 taiiKlfii, Franklin
505,952
7
72,279
Barnstalrlf
490,130
10
49,013
Worcester, Norfolk
374,905
2
187,453
Berksliire
324,765
7
46,395
Nantucket
31,071
1
NA
Essex
29,685
2
14,823
Bristol
18,496
1
NA
Dukes
17,000
1
NA
Middlesex
16,934
1
NA
Lymantria dispar (L.), the browntail moth Euproctis
chrysorrhoea (L.) and other pests, it quickly became
apparent that this animal attacks a large and diverse
assemblage of macrolepidopteran larvae (Webber &
Schaffner, 1926; Ai nauld, 1978). Recent observations
by Boettner et al. (2000 and unpnbl.) confirm the
extraordinaiy impact of C. concinnata on several native
saturniids on mainland New England and that the flies
will attack E. dw/icria/A caterpillars when presented with
the opportunity. Compsilura concinnata is considered
a stong candidate for playing a role in the demise
of E. imperialis and other large moths on mainland
New England (Boettner et al, 2000); Compsilura
concinnata occurrence on Martha’s Vineyard has not
been verified.
Regional variation and host plant use
Eacles imperialis (and can certainly be reared)
on a wide range of tree hosts (Ferguson, 1971; Stone,
1991; Tuskes et al, 1996), to which it may be locally
specialized, and the moth’s range exceeds that of any
recorded host plant species. Ferguson (1971) lists
an impressive array of recorded hosts: “oak, hickory,
walnut, sycamore, basswood, maple, honey locust,
chokecheriy, sumac, sweet gum, sassafras, elm, beech,
hornbeam, birch, alder, pine, spruce, hemlock, cedar,
cypress, and juniper.” However, the degree to which
a given population of E. imperialis is ever genuinely
polyphagous in nature is not well studied. On Martha’s
Vineyard, E. imperialis appears to feed exclusively on
pitch pine {Pinus ri.gida), a common tree associated
with sandy, well-drained soils and barrens habitats.
Pine-feeding is not nnusnal for Eacles impeiialis
elsewhere, nor is it restricted to the northernmost
tier of the moth’s range: Abbot and Smith (1797)
observed pine-feeding in Georgia over two centuries
ago, and pitch pine is a common host in the New Jersey
pine barrens (D. F. Schweitzer, pers. comm.). All the
recorded hosts of E. i. pini are conifers (Tuskes et al,
1996), including jack pine {Pinus hanksiana), which
replaces P. rigida to the north and west of southern
New England. Erom the perspective of consumption
and digestion, conifer foliage represents a diet high
in fiber, relatively low in water and nitrogen content,
and possessed of allelochemical defenses such as
monoterpenes stored in resin ducts (Raffa, 1991).
The observation of localized conifer specialization
on the part of A. imperialis i?, of interest both from the
perspective of pine-herbivore biology and from that
of the species’ northeastern decline.
Host plant specificity among herbivorous insects
in general and Lepidoptera in particular has been
of broad interest to entomologists at least since the
42: 34-49, 2003 (2010)
39
works of Brues’ (1920, 1924), which were followed by
seminal ecological studies and reviews highlighting-
general patterns in the ecology and evolution of host
use breadth (e.g. Ehrlich & Raven, 1964; Futuyma,
1976; Gilbert, 1979; Cates, 1980; Jenny, 1984). Adult
oviposition cues play a critical role in host plant
specialization (Wiklund, 1975), and variables such
as host plant chemistry and architecture (Cates &
Rhoades, 1977; Scriber & Feeny, 1979; Berenbaum,
1981; Bowers, 1983, 1984; Bernays, 1989), foliar
water, nitrogen and fiber content (Scriber, 1977,
1979b; Mattson, 1980; Mattson & Scriber, 1987),
and maternity (e.g. Mousseati 8c Dingle, 1991) effect
lepidopteraii digestive efficiency. Poptilation genetic
and phylogenetic data have been brought to bear on
the evolution of host specialization and the role of
host shifts in speciation (Berlocher, 1998), and the
co-cladogenesis of insects and plants (Farrell 8c Mitter,
1990, 1998; Futuyma 8c McCafferty, 1990; Funk et ciL,
1995; Becerra, 1997; Farrell, 1998).
Studies of the ecophysiological roles of host plant
growth form and seasonality (e.g. Tilton, 1977;James
8c Smith, 1978; Scriber, 1978) in mediating insect-plant
associations are directly relevant to the evolution of
pine feeding. From a nutritional perspective, folivores
of trees and other woody plants represent a guild
that must often contend with low nitrogen and water
contents relative to graminivores or forb feeders, for
example. Nitrogen is an important growth-limiting
factor for many herbivores which may covary with
water content (Mattson, 1980); low foliar water
content can impede the growth and development of
herbivores (Scriber, 1977) as well as a given herbivore’s
ability to utilize available nitrogen (Scriber, 1979a, b).
These effects can be particularly severe with regard
to the performance of tree feeders (Scriber, 1979b);
since low nitrogen and water contents are typically
associated witli woody plants as opposed to forbs and
grasses, folivores of trees often display low growth and
utilization efficiencies (Scriber & Slansky, 1981).
I pursued a line of investigation tow'ards better
understanding host plant use in the relictual
population of this moth, specifically the question
of whether the apparent confinement to pines is
nutritionally imposed or the result of some unknown
non-nutrionally based or abiotic factor. This endeavor
comprised laboratory-based experiments focusing on
the role of food plant in influencing larval growth
and development. Given the considerable range¬
wide variation in host use among geographically
delimited populations of £. imperialis, the notion that
such local specialization may have been accompanied
by physiological adaptation is of interest from the
perspective of understanding host shifts, regardless
of whether they accompany speciation per se.
Materials and methods
Five treatments from fotir species of host plants
were chosen on the basis of recorded use by E.
imperialis, availability and, in the case of pitch pine,
comparability between material from wild populations
known to be used by £. imperialis arboretum-raised
material. Pitch pine is the only known host of E.
imperialis on Martha’s Vineyard (personal obseiwations
of both larvae and wild oviposition behavior of adult
females) , and was reported as the favored lan al host of
other Massacliusetts E. imperiaUs (Eliot 8c Soule, 1902).
The jack pine P. beraksiana was chosen because it is
associated with E. imperialis pini (Michener, 1950; M.
C. Nielsen, pers. comm.; B. Scholtens, pers. comm.),
comprising the northernmost named subspecies of
E. imperialis and the only other regional populations
associated exclusively with conifers. Jack pine may
be considered an ecological analog of pitch pine, in
that it replaces the latter in habitats to the north and
west characterized by granitic soils that, like maritime
pitch pine-scrub oak barrens, are sandy, well-drained,
and acidic soils (Little, 1979; Schweitzer & Rawinsky,
1988). M. C. Nielsen (pers. comm.) reports that E.
i. pini appears most commonly in association with
jack pine on Grayling soils. With the exception of
tiny remnant stands such as that at West Rock, New
Flaven, CT, the post oak (X stellala is represented in
New England primarily as a di.sjunct population on
Martha’s Vineyard. The nearest large stands of Q.
stellala occur on Long Island, N. Y. and in the New
Jersey pine barrens, which also hosts the largest
northeastern population of E. imperialis. The black
walntU J. nigra was chosen because it is a recorded
host of E. imperialis, yet does not occur regularly on
Martha’s Vineyard. Food plant material was harvested
every five days from the Felix Neck Wildlife Sanctuai'y,
Edgartown, MA (pitch pine and post oak) and the
Arnold Arboretum, Jamaica Plain, MA (pitch pine,
jack pine, and black walnut). LIpon cutting, plant
material was placed in water pics and maintained at
4()°F until used.
Foliage fitted with water pics was placed in rearing
containers, the supply of fresh food maintained, and
the container cleaned of frass every five days. Since
foliar water and nitrogen concentrations have been
demonstrated to decrease with leaf age (Axelsson &
Agren, 1979; Slansky 8c Scriber, 1985) , it was therefore
important to be as consistent as possible when
selecting plant material so that foliage treatments
of wildly disparate ages were not lumped under the
same heading.
40
/. Res.Lepid.
Gravid females from Martha’s Vineyard were
collected in 1988 and 1989 at light and placed in
paper bags for oviposition. Ova were harvested and
segregated according to parent, then maintained in
4” diameter petri dishes tinder constant conditions
of light and temperature (per day, 14 hours light
at 25°G and 10 hours darkness at 20°C). The 1988
livestock came from four females taken between 31
July and 5 August at three different sites oit Martha’s
Vineyard: Gedar Tree Neck, West Tisbnry (4 Atigust,
1 10 ova); Makonikey, West Tisbnry (3 and 5 August,
155 and 78 ova); and Pennywise Path, Edgartown (31
Jtily, 107 ova).
During the hrst (1988) season’s experiments, ova
were selectively cooled at 50°F for up to four days to
synchronize hatching. Larvae from each clutch were
weighed tipon hatching, placed on each of live of
the food plant cohorts, and weighed every five days
(116 hours) through day 15 in all cases and day 20
when ]4ossible. Larvae were reared individually, first
in 4.0” petri dishes for their hrst hve days, and then
in plastic containers 4.5” in diameter and 3.5” in
height. Humidity was maintained iisitig 1” x 2” cut
sections of paper towels secured to the container lid
and moistened twice every live days. All larvae were
maintained under constant conditions of temperature
and lighting as described above. Since leaves that
remain attached to the stem are generally less apt
to lose water than if they are cut (Schroeder, 1984),
food plant freshness was maintained by placing plant
sprigs (or petioles, in the case of/, nigia) in water pics
sititated in larval rearing containers.
Weights of surviving larvae from different clutches
and on different host plants were natural log-
transformed and compared (2-way ANOVA) for each
weighing interval through Day 15. The influence
of food plant treatment was further analyzed (1-way
ANOVA) by lumpittg all suiwiving larvae of a giveti food
plant treatment and age regardless of parentage.
In 1989 these experiments were repeated in part
and with several modihcations, using ova from seven
lemales collected between 26 and 28 Jitly from three
sites on Martha’s Vineyard; Lobsterville, Aquinnah
(26 July, 178 ova); Gedar Tree Neck, West Tisbnry
(three females, all 27 July; 55, 125, and 169 ova);
and Makonikey, M'est Tisbtiry (three females, 26, 27,
and 28 Jtily; 178, 50, and 104 ova). The 1989 work
focused exclusively on two food plants taken from
ctirrent E. habitat (71 rigida, the native host,
and Q. strllala, with all plant material taken from Felix
Neck M'ildlife Sanctuary, Edgartown, MA. Eggs were
not cooled to synchronize hatching, and in order
to minimize handling of yotmg larvae, all hatchling
caterpillars were started not in petri dishes but in the
larger plastic containers. Given observations that
hatchling larvae lost weight to desiccation quickly,
care was taken to ensure that every larva was weighed
and placed on the appropriate food plant immediately
upon hatching. To maintain humidity, I used 1” x
1” X 2” sponges, washed at each weighing instead of
paper towel sections. The sponge holds more water
and for a longer period of time and does not require
additional moistening between weightings. All sponge
blocks were washed repeatedly prior to use to clear
them of chemical additives, and thoroughly cleaned
of larval frass at each weighing to avoid mold. Food
plants were maintained as in 1988 at 40°F, misted with
distilled water and given refreshed water pics every 24
hours. Feedings were made as close to identical as
possible; all the feedings for a given weighing interval
and food plant species consisted of material cut from
a single tree. Sample sizes were increased to fifteen
larvae per female per food plant treatment initially,
for 104 larvae in total on each food plant. Color
morph and instar were noted at each weighing and
larvae were reared to pupation, sexed and weighed
again. Weights were analyzed as described through
day 20 for all larvae and pupae. Since E. imperialis is
a sexually dimorphic species, male and female pupae
were compared separately (1-way ANOVA) for each
food plant cohort. Weights upon hatching were
compared independent of a food plant effect (one-way
ANOVA) to evaluate bias in assigning larvae to food
plants. There was not a large enough sample size per
sex per clutch to retrieve any significant data regarding
a maternal effect on pupal weight. However, all pupal
weights representing each sex were lumped for each
food plant in order to test for a food plant effect via
one-way ANOVA.
The gravimetric assessment of digestive and growth
indices involved forty offspring of a single female on
four of the 1988 food plant treatments: both wild
and arboretnm-grown P. rigida, arboretum-grown P.
hanksiana, and wild Q. stellata. Low survivorship on /.
nigra precluded there being enough data to analyze.
These indices were: relative growth rate (RGR);
relative consumption rate (RGR); approximate
digestibility (AD); efficiency of conversion of ingested
food to biomass (ECI) ; and efficiency of conversion of
digested food to biomass (ECD). The experimental
regime employed here involved monitoring the
food uptake and utilization during the course of a
single instar, from the beginning of the third to the
beginning of the fourth instar. All vegetative material
used in these experiments consisted of pre-weighed
individual leaves or sprigs; unconsumed food and frass
was dried at 95°F and re-weighed. Control samples
of plant material for each feeding were also weighed.
42: 34-49, 2003 (2010)
41
dried, and re-weighed for tlie purpose of calculating
conversion factors. Larvae were weighed at the
beginning and end of the experiment, then frozen,
dried, and re-weighed to determine the dry weight
gained by each larva. Each larva thus provided its
own conversion factor, its final dry weight treated as a
percentage of its final fresh weight and used to estimate
initial dry weight. Based on these weights of plant and
larval material, the hve food plant utilization measures
were determined following Waldbatier (1968). For
each larva used in the calculation of utilization indices,
the dried control food plant material was ground and
analyzed for percent-nitrogen using a Kjeltec nitrogen
analysis system. Mean digestive indices were compared
via one-way AN OVA.
The gravimetric assessment of performance has
been reviewed and critiqued numerotis times since
its introchiction (Scriber & Slansky, 1981; Schroeder,
1984; Agren Sc AxeLsson, 1979; Bowers et al, 1991),
and a substantial body of literature has been devoted
to evaluating the various sources of error associated
with this method. A significant methodological
source of error in the calculation of such nutritional
indices derives from the indirect calculation of the
dry weight of plant material and of the initial dry
weight of the larva (Bowers et «/.,199 1 ) . Since the host
plants used differ in megaphyll morphology, achieving
similarity between treatment and controls is difficult
to standardize. This necessitated frequent feeding
of fresh plant material in order to minimize the
differential effects of desiccation on digestibility. For
each feeding of stellata, a single leaf was bisected,
half used to determine the dry weight conversion
factor. Conversion factors for P. ngidz/ involved the use
of individtial needles excised from sheaths: for each
needle-bearing sheath, a single needle was removed
for immediate drying wliile the others were tised for
feeding. This method has the dual advantages of
providing as accurate a control as possible, since all
needles within a given sheath are the same age and
size, and of minimizing damage to both treatment
and control, since the sheath can be removed from
its enclosed needles without tearing or severing
significant mesophyll ti.sstie.
Preliminary work showed that the short needles
of P. banksiana, which occtir in pairs, were more
vulnerable to desiccation than those of P. rigida. To
offset desiccation, single needles were therefore
retained intact within bisected sheaths, the dry
weight of the inedible sheath later stibtracted from
the estimated dry weight of the initial feeding prior
to calculation of fresh weight/ dry weight conversion
factors.
Results
Food plant and maternal effects on growth
Larval growth varied considerably across the 1988
food plant treatments. The (1988) data indicated
that E. imperkdis larvae grew more slowly at first on
the decidtiotis plants than conifers, with growth most
markedly retarded among the larvae fed /. nigra (Table
2, Fig. 5). Based on weight, larvae responded best to
the diet of arboretum-grown P banksiana, followed by
that of arboretum-grown P. rigida, wild (X stellata and
finally wild P. rigida. However, for a period between
the second and third weightings (days 5 and 10), the
growth of larvae fed Q. stellata stirpassed that of the
other food plant cohorts. Most larvae fed arborettim-
grown jack pine and pitch pine weighed more at
Day 20 than those given other food plants. ANOVA
indicated signiheant food plant as well as maternal
effects on larval growth (Table 3), the latter far less
marked than the former.
Larvae in the 1989 follow-iqD growth ex])eriments,
conducted under modified conditions where foliar
water was more rigorously ensured, consistently gained
biomass and molted earlier when fed post oak than
when fed pitch pine, nnambignotisly demonstrating
enhanced performance of E. iniperialis on wild Q.
stellata relative to wild P rigida based on larval growth
and pupal weight (Fig. 6; Tables 4, 5), again with
significant differences attribtitable both to food plant
and to maternity in eacli of the host plant treatments
(Table 6; Figs. 7, 8).
The variation in larval growth attributable to
maternal effects was, as in 1988 (4able 3), small relative
Figure 5. Fresh weight (mg) of E. imperialison five food plant
treatments taken at 5-day intervals, 1988. Cf. Table 2.
42
/. lies.Lepid.
Table 2. Weights (mg) of larvae reared on five food-plant treatments, 1988. x= mean; se = standard error; N= sample size;
AA = foliage used from Arnold Arboretum, Jamaica Plain, MA; FN = foliage used from Felix Neck Wildlife Sanctuary, Edgartown,
MA. Cf. Fig. 5.
Age
(clay.s)
Pimis rigida (FN)
x(se)
Pinus rigida (AA)
x(se)
Qiiercus stellata (FN)
x(se)
Pinus banksiana (AA)
x(se)
Juglans nigra (AA)
x(se)
0
9.384 (0.083)
Ar=19
8.9 (0.081)
7V=19
9.47 (0.0653)
AA23
7.632 (0.069)
N=19
8.411 (0.083)
N=19
5
43.947 (0.213)
N=19
45.968 (0.21)
fV=19
40.335 (0.179)
W=23
59.058 (0.311)
W=19
34.211 (0.191)
N=19
10
157.789 (.495)
W=19
203.158 (0.45)
Afcl9
246 (0.562)
7V=23
243.342 (0.556)
N=19
68.618 (0.409)
N=17
15
652.829 (1.279)
7V=14
988.174 (0.865)
N=\9
973.099 (1.068)
N=19
1219.421 (1.185)
iV=19
160.769 (0.851)
N=13
20
1964.592 (2.479)
N=14
2471.57 (2.54)
N=\0
1867.557 (3.629)
N=7
3320.9 (1.869)
N=14
296.788 (1.783)
N=8
Table 3. Analysis of variation due to food-plant and maternal effects on larval growth, 1 988. NA not applicable.
Variation due to foodplant
Variation due to maternal effects
Larval age (days)
DF
F-ratio
P-valiie
DF
F-ratio
P-valiie
0
4
NA
NA
3
1.08
0.362
5
4
3.988
0.005
3
6.297
0.001
10
4
22.329
<.001
3
6.259
0.001
15
4
55.356
<.001
3
4.393
0.007
Table 4. Weights (mg) of E. imperialis reared on P. rigida and O. stellata at ages 0 through 20 days, 1989, followed by pupal
weights for males and females. Range refers to mean values for offspring of a given female (not applicable for pupal weights).
Cf. Fig. 6.
Pinus rigida
Quercus stellata
L.arval age (days)
x(se)
Range
x(se)
Range
0
10.221 (0.013)
N=104
8.334-11.727
10.315 (0.014)
N=104
8.531-12.358
5
47.803 (0.035)
N=104
41.508-58.789
59.227 (0.044)
N=100
53.389-66.627
10
315.042 (0.118)
N=102
229.862-468.191
555.959 (0.213)
N=92
383.782-647.46
15
1516.205 (0.268)
N=96
1 161.357-2013.193
2195.288 (0.328)
N=86
1516.931-2711.417
20
3561.943 (0.349)
N=93
3007.108-4226.031
4484.786 (0.387)
N=87
3517.45-5599.417
.Vlale pupal weight (mg)
3719.304 (0.936)
N=26
NA
4751.297 (0.786)
N=29
NA
Female pupal weight (mg)
4473.514 (1.199)
N=22
NA
5705.4 (1.277)
N=22
NA
42; 34-49, 2003 (2010)
43
Table 5. Summary and analysis of development of E. imperialis in therms of instar on R rigida and Q. stellata.
Day 5
Day 10
Day 15
Day 20
Instar 1
2 2
3 3
4 4
5
# Piiic-fcd larvae 24
80 13
89 8
88 28
65
# Oak-fed larvae fi
96 2
90 1
91 12
73
G-value 13
9
6
7
P-value <.001
<.005
<.025
<.025
Table 6. Analysis of food-plant and maternal effects on larval growth, 1989. NA =
: not applicable; NS = insufficient data.
Variation due to foodplant
Variation due to maternal effects
Larval age (day.s) DF
F-ratio
P-\aluc DF
F-ratio
P-value
0 NA
NA
NA 6
I.5..547
<.001
5 1
26.194
<.001 6
3.643
0.002
10 1
55.112
<.001 6
6. 1 76
<.001
15 1
25.382
<.001 6
6.507
<.001
20 1
24.34
<.001 6
5.593
<.001
Male pupa 1
40.049
<.001 NS
NS
NS
Female pupa 1
28.115
<.001 NS
NS
NS
Table 7. Summary and analysis of nutritional indices obtained on four food-plant treatments. AA = foliage used from Arnold
Arboretum, Jamaica Plain, MA; FN = foliage used from Felix Neck Wildlife Sanctuary, Edgartown, MA.
Nutritional Pinus rigida (FN)
index
Pinus hanksiana
Pinus rigida (AA)
Qiiercus stellata
One-way AN OVA
F-ratio P-value
x(se)
x(se)
.v(,se)
x(se)
AD 31.09(0.6)
N=4
31.64 (0.431)
N=7
28.78 (0.2.59)
A''=9
26.5 (0.283)
N=7
0.898
0.457
FXID 32.16(0.714)
N=4
39.38 (0.647)
N=7
41.96 (0.331)
iV=9
46.22 (0.43)
N=7
1 .056
0.387
ECl 15.01 (0..304)
N=4
16..35 (0.197)
N=7
18.08 (0.126)
yV=9
18.48 (0.208)
N=7
4.778
0.01
RGR 0.205 (0.04)
N=4
0.244 (0.021)
N=7
0.251 (0.022)
A’=9
0.264 (0.032)
N=7
2.157
0.121
RGR 0.473 (0.072)
iV=4
0.49 (0.04)
N=7
0.414 (0.02)
N=9
0.425 (0.04)
N=7
2.178
0.1 18
%N 5.83 (0.052)
7V=8
6.79 (0.086)
1V=8
6.84 (0.048)
N=S
8.07 (0.091)
A=8
48.973
<.001
to that attributable to host plant. One trend is tliat of
the consistent relative growth of offspring of several
females; mean larval weights for each of four females
on post oak were more massive than on pitch pine by
Day 5, remaining so at every consecutive weighting
through Day 20. The offspring of each of the four
females grew, relative to one another, in exactly the
same order on oak and pine, with the offspring of
female 5 outdistancing tho.se of females 6, 7, and 2,
respectively (Figs. 7, 8). This trend implies that there
44
/. Res.Lepid.
Mean Individual
l.arval wgt (mg)
Larval Age (Days)
Figure 6. Fresh weight (mg) of E. impehalis on pitch pine
P. rigida and post oak Q. stellata, 1989. Cf. Table 4.
Figure 8. Fresh weight (mg) of pine-fed offspring of four
females of E. imperialis, 1989.
6000
5500
5000
4500
I 4000
t 3500
.? 3000
> 2500
I 2000
j 1500
1000
500
0
0 5 10 15 20 25
1 arval Age (Days)
Figure 7. Fresh weight (mg) of oak-fed offspring from four
female E. imperialis, 1989.
exists little trade-off in relative efficiency from oak to
pine. That is, a larva vvell-eqnipped to utilize pine
relative to another larva may be just as relatively well
equipped to utilize oak. This explanation is consistent
with the fact that no statistically significant interaction
exists between the parental effect and the food plant
effect. Significant differences appeared among mean
weights of larvae from different clutches at each
weighing and among mean weights of hatchling laiwae,
but these relative differences did not persist as such at
snb.sequent weighings. Since there were no significant
differences between mean weights of hatchling larvae
given different food-plant treatments, these results
can not be attributed to bias in the initial separation
of larvae into treatment cohorts.
A comparison of the numbers of larvae that had
achieved a given instar by a given age revealed the
following; significantly more of the oak-fed larvae than
the pine-fed larvae molted to second instar by Day 5
(DF=1, G=12.996), third instar by Day 10 (G=8.5()2),
fourth instar by Day 15 (G=:6.162), and fifth instar
by Day 20 (G=6.688). Additionally, mean male and
female pupal weights were significantly higher for oak-
fed larvae (4751.297 mg and 5705.4 mg, respectively)
than for pine-fed larvae (3119.304 mg and 4473.514
mg, respectively).
In both years the number of larvae exhibiting
the green color morph was higher for the pine-fed
cohort than tiie oak-fed cohort. Exactly 50% (52 of
104) of all the 1989 larvae reared on pine exhibited
green coloration; most of these turned green at the
.second molt (beginning of the third instar), and seven
reverted to brown at subsequent molts, five at the third
and two at the fourth. Of the 52 green larvae from
both 1989 food plant treatments, only four had been
reared on oak. As many as 13 of 15 and as few as 5
of 15 offspring of a given female fed pitch pine were
green. Almost all larvae reared on oak exhibited a
lighter brown or reddish body color.
Nutritional indices
Nutritional indices, calculated exclusively during
the third instar, corroborated enhanced growth rate
and efficiency on oak relative to pine, as did the higher
pupal weights among oak-fed versus pine-fed larvae
(Table 7). The efficiency of conversion of ingested
food (ECD), the efficiency of conversion of digested
food (EGI), and the relative growth rate (RGR)
were positively correlated with foliar nitrogen and
42: 34-49, 2003 (2010)
45
water content across food plants; the approximate
digestibility (AD) and the relative consnmption rate
(RCR) were not. The only significant differences,
however, were among the ECI and percent nitrogen
values. The foliage of wild grown post oak and
arboretnm grown pitch pine contained significantly
more nitrogen and water than corres]>onding amounts
of wild pitch pine and arboretum-grown jack pine,
and these numbers were paralleled by larval ECIs.
(Table 7).
Discussion
The life history constraints of host specialization
have been an important focus within the study of
herbivore evolution. It has been hypothesized that
the limits imposed by a contraction in the spectrum
of potential host species are offset by an enhanced
efficiency with which an herbivore utilizes that
narrower host range (Brties, 1924; House, 1962;
Emlen, 1973; Gilbert, 1979). The validity of this
“feeding specialization hypotliesis” is central to our
understanding of evolved herbivoi'y (Slansky & Scriber,
1985). Not only have consistent patterns of higher
utilization efficiencies among monophagous versus
polyphagotis or oligophagous herbivores failed to be
demonstrated, but Scriber and Feeny (1979) have
contended that host plant chemistry is responsible
for most of the variation seen in larval performance.
That is to say the “costs” of specialization have not
been well-dehned or demonstrated in a broad sense
because the axes along which organisms specialize
may or may not intersect. It has become increasingly
clear that in order to effect proper experimental and
analytical procedures to test the feeding specialization
hypothesis as a general paradigm, one must recognize
a range of organism-specific variables, from elements
in plant foliage that affect herbivore development to
life history manifestations of constraints imposed by
the host plant. These variables defy simple patterns,
being too numerous and interdependent for their
roles to be parsed except very broadly (Gaston 8c
Reavey, 1989). Scriber (1983) suggested that one
reason for our relative lack of understanding derives
from the paucity of studies narrowly focused on groups
of taxonomically and ecologically similar organisms.
To these I would add studies of ecologically similar but
phylogenetically independent and phylogenetically
well understood groups.
Notwithstanding the predictable effects of nutrient
rich foliage among arboretum-grown plants relative
to wild foliage, the growth rates and efficiencies of
consumption and digestion of oak versus the wild pine
host suggest that, ntitritionally. New England imperial
moth caterpillars do not require pitch pine alone in
order to survive. At the same time, E. imperialis may
be adapted or pre-adapted physiologically to conifers.
Conifer feeding on the part of herbivorous insects
represents a nutritional dynamic different from
deciduous leaf feeding. Pitch pine, in particidar,
is a complicated fire-adapted plant, and perhaps a
more relevant comparison than that between larval
performance on arboretum-grown, well-fertilized
plants and performance on native hosts of disjtinct
moth populations might be undertaken between
geographically disparate populations on the wild
northern conifer hosts and among different age
cohorts of pitch pine foliage growth in viable habitats
of E. imperialis. That said, differential patterns in
nutritional content between evergreen and deciduous
trees have been demonstrated (Miller & Stoner, 1979),
with evergreen foliage having generally lower nutrient
contents. Pines and other conifers typically contain
less foliar nitrogen than deciduous angiosperms
under similar conditions of growth and development
(Bidwell & Dnrzon, 1975; Slansky & Scriber, 1985), and
wild pitch pine from barrens and typically nutrient-
poor (Forman, 1979; Schweitzer & Rawinski, 1988).
Eolivores of nutrient-poor, woody plants tend to show
greater breadth of dietary tolerance (i.e. be more
polyphagotis) than those on highly nutritions foliage
(Matt-son & Scriber, 1987). Mattson and Scriber (1987)
cite Holloway and Hebert (1979) who found that
conifer-feeding Lepidoptera “are less specific in host
plant choice than species feeding on angiosperms.”
The data presented in this study are consistent with
this claim in that the larvae of E. imperialis ure capable
of sustained development on different hosts. Both
the published host records of E. imperialis and the
restilts of this study support the contention that this
species, including populations functionally restricted
to pine, can metabolize a broad range of potential if
not realized host plants.
Large body size is also considered an advantage
when feeding on low-nutrient diets (Wasserman &
Mitter, 1978; Peters, 1983; Mattson & Scriber, 1987),
such as pines or late-season tree foliage. In fact, tree¬
feeding lepidopteran species active late in the growing
season tend to be large (Mattson, 1980; Niemela et
ai, 1981), as would be expected especially for those
in which the adults do not feed (Slansky & Scriber,
1985) such as E. impenalis. There may also exist such
a trend for folivores of evergreen versus deciduous
plants. Opler (1978) noted that leafminers feeding
on evergreen oak species tended to be larger than
those on deciduous species. Although phylogenetic
data were not yet available to evaluate the evolution
of size in a cladistic framework, ntimerous authors
/. Res.Lepid.
4(')
have observed phylogenetically biased patterns in
lepidopteran size associated with host plant use and
life histoiy (Mattson, 1977; Wasserman & Mitter, 1978;
Nieinela et at., 1981; Hayes, 1983; Gaston & Reavey,
1989), and although adaptive speculation is frivolous,
it is woi'th noting that E. imperialis, the most massive
saturniid extant in New England, is also the latest
feeding saturniid in the region, active as larvae as
late as October. By this time many of the host plants
utilized further south, where the flight season of E.
imperialis is more protracted, are senescent or nearly
so northward, potentially accounting in part for the
more strict association with conifers northward.
In contrast to pitch pine, wild grown post oak
contained significantly higher amounts of nitrogen
than even arboretum grown j)itch pine, even tbough
ECl’s were not significantly different for larvae fed the
two food plants. This implies either more efficient
nitrogen utilization of pitch pine versus post oak on
the part of Earles or simply that oak contains more
nitrogen than EV/cfes larvae can effectively metabolize.
Despite the fact that the only two plant cohorts for
which nitrogen content was not significantly different
were the two arboretum-grown pines, the ntean EGI
was significantly higher for larvae on arboretum-
grown pitch pine than for those on Jack pine; both
were significantly higher than for wild pitch pine.
The mean EGI for arboretum-grown pitch pine was
comparable to (i.e. not significantly different from)
that of Martha’s Vineyard post oak, on which larvae had
the liighest ECIs, and which supported a significantly
higher nitrogen content (in fact the highest of all food
plants measured). Taken collectively, these results
suggest a potential physiological adaptation to pine¬
feeding in general, and pitch feeding specifically on
the part of northern E. imperialis.
The results presented here go to show that simply
because a particular food plant species meets an
berbivorous organism’s nutritional requirements and
the organism is ]ihysiologically capable of growth and
development on that food is not an indication that
it is an actual, realized host in nature. There might
be any of a number of possible explanations for the
fact that Massachusetts E. imperialis larvae appear to
grow faster and more efficiently on a non-utilized
host (Q. stellala) than on the native host {P. rigida).
Ghemical oviposition cues such as terpenes specific
to conifers, selective predation of larvae on one host
versus another, abiotic habitat requirements of soil
pupation, and even simple availability may all play
a role in the restriction of northern E. imperialis to
conifers. Eor example, I observed late instars of wild-
reared larvae placed on (7. stellala undergo heavy
predation by vespid wasps {Vespa vulgaris-, pers. obs.)
relative to those reared in situ on P. rigida. The frass
of oak-feeding larvae is less dry and more prone to
mold than that of pine-feeding larvae, and may serve
to attract predators.
The restriction of Earles imperialis to the common
pitch pine on Martha’s Vineyard is of interest
from the standpoint of conservation as well as
evolutionary ecology. Earles imperirdis is one of 24
regionally threatened moth species occurring on
Martha’s Vineyard protected under the Massachusetts
Endangered Species Act (MESA; M.G.L. c. ISlAand
regulations 32 1 GMR 1 0.00) , not including at least one
additional species, Dntana rontrarta (Notodontidae)
that appears to have been impacted severely on
mainland southern New England and may be locally
extirpated. As thorough an understanding as possible
of why species such as these have declined — and
what they require to persist — is a mission-critical
prerequisite to any reintroduction and restoration
effort. As conservationists consider potential sites
at which to reintroduce and restore this species,
we must weigh a variety of considerations, among
them suitability of habitat, availability of host plant,
probability of success, verifiability of historical
occurrence, and legal logistics.
Biologically, the most obvious candidate sites, those
showing the greatest promise for success, are barrens
habitats on Cape God and in Plymouth County and
on Nantucket Island. Ironically, historical records
of E. imperirdis from Cape Cod are lacking, and the
conspicuous absence of this moth and its near relatives
from Nantucket has long been noted: Jones and
Kimball (1943) made the observation that although
four species of ceratocampine saturniids occur on
Martha’s Vineyard, none were known at the time
of that writing from Nantucket. Jones and Kimball
speculated that such heavy bodied moths found it
difficult to distribute across water barriers. As was
the case during Jones and Kimball’s time, four species
of Ceratocampinae {E. imperialis, Anisota senatoria,
A. stigma, and A. virginiensis) persist in numbers on
Martha’s Vineyard. Anisota stigtua, at one point listed
under the Massachusetts Endangered Species Act,
occurs less ubiquitously on mainland New England than
on Martha’s Vineyard (Mello et rd., 1999). However,
this species has apparently colonized Nantucket (K.
Coombs-Beattie, pers. comm.; Goldstein, 1997),
where it now occurs commonly, possibly obviating
the argument that all ceratocampines have difficulty
crossing water barriers.
Although Jones and Kimball did not discuss the
historical ecology or land use history per se of either
island, the possible role of habitat destruction and
fragmentation of barrens habitats must be considered.
42: 34-49, 2003 (2010)
47
There can be little debate that viable habitat persists
at mainland barrens sites, including the extensive
maritime barrens in Plymouth County at Myles
Standish State Forest (approx. 16, ()()() acres) and
at the Massachusetts Military Reservation (roughly
15,000 acres), as well the 2,000 acre inland barrens at
Montague Plain, Franklin Co., MA and on Nantucket
Island. Jones and KimbalFs (1943) observation that
ceratocampines were absent from Nantucket during
the20th century of course begs the question of
whether they were ever there. The land use history
of Nantucket, like that of Martha’s Vineyard, involved
significant alteration and conversion of forested and
shrubland habitats for the purposes of agriculture
(Dunwiddie, 1992). Although both Martha’s Vineyard
and Nantucket were part of an extensive coastal
plain as recently as 10, GOO years ago, Nantucket was
almost completely denuded of forest during the
Revolutionaiy War, which no doubt had an impact
on the lepidopteran fauna. It may be observed that,
in addition to the ceratocampines, other groups of
forest tree Lepidoptera are depauperate on that island
relative to Martha’s Vineyard. There is a marked
contrast, for example, between the islandic faunas
of Limacodidae: whereas nine species of limacodids
{Euclea delphinii, Isa textiila, Phobetron pitchecium,
Prolhnacodes hadia. Apod a bigut tat a, Lithacodes fasciola,
Packardia elegans, P geminata, Torticidia flexuosa) occur
regularly oil Martha’s Vineyard, only two {E. delphinii
and L. fasciola) were recorded on Nantucket byjones
and Kimball (1943: 123-125) . Jones and Kimball’s data
also suggest a comparative dearth of leaf litter feeding
deltoid noctuids on Nantucket relative to Martha’s
Vineyard, which would be expected following systemic
deforestation.
Pitch pine, however, is now an extremely common
plant on Nantucket and, ironically, it is conceivable that
the introduced tachinid C. concinnata, to be verified
from the island of Martha’s Vineyard or Nantucket,
may prevent the re-establishment of E. imperialis on
mainland New England. It has yet to be determined
whether or not the introduced parasitoid C. concinnata
poses a barrier to recolouizing the mainland, whether
or not the fly’s absence on Martha’s Vineyard is, if
not an artifact of under-sampling, a reason for Eacles'
persistence there.
Acknowledgements
Much of this \vt)rk was conducted as an undergraduate tltesis
under the mentorship of M. Deane Bowers and James M. Carpenter.
All errors, omissions and otlicr such gaffes remain the author’s sole
responsibility. Many then at the .Vluseum of Comparative Zoolog}'
and the Biological Laboratories at Harvard University are to be
thanked for their help, guidance, and friendship: Eric Fajer, Ed
Armstrong, Charlie Vogt, Scott Shaw, David Furth, Mark Skinner,
Katht' Brown-Wing, and Peter Frumlioff. E(|nally iinjtortant were
my fellow naturalists in southeastern Massachusetts who kindly
contributed field work and observations and, through the various
conservation organizations for which they worked, granted
|3ermission to conduct that work on a variety of protected areas. Of
particular help were Tim Simmons (Sheriff’s Meadow Foundation),
Gus Ben David (Massachusetts Audubon Society), anti 'Fttm Chase
(The Trustees of Reservations). Mary Lesniak kindly enabled
acce.ss to the collection of the Boston Society of Natural History,
currently housed at Boston University. Jeff Boettner (University of
Massachusetts) and Tim Simmons (Massachusetts Natural Heritage
& Findangered Species Program) |)rovided tnany valuable insights
and clarifications. I thank Mo Nielsen (Michigan State University),
Paul Opler (Colorado State University), Rav Pupedis (Peabody
Museum of Natural History, Yale Lhiivesity), and Brian Scholtens
(College of Charleston) for relevant observations and collection
records from their respective institutions. Rodger Gwiazdowski
(University of Ma.ssachusetts, .Amherst) provided real-time checking
of EV/efevdata labels at UMass. I thank Sean Bober for assisting with
the assemblage of figures and Mike Nelson (Massachusetts Natural
Heritage & Endangered Species Program) for invaluable eleventh
hour help with maps.
Literature cited
Abbot, J. & J. E. Smu h. 1797. The natural history of the rarer
lepido]5terous insects of Georgia. 2 vols. London: printed hv
T. Bensley lot J. Edwards.
ARNAtut), P. H.,Jr. 1978. A host-parasite catalog of North American
Tachinidae (Diptera). USD.A. Science and Education
Administration, Washington. D. C. publication 1319.
Acren & Axei.sson. 1979. Energ-y budgets do balance. Oecologia
42: 375-370.
Be(:err.\, J. X. 1997. Insects on plants: macroevolutionaiy chemical
trends in host use. Science 270: 253-256.
Berenbaum, M. 1981. Patterns of furanocoumarin distribution
and insect herbivory in the Umbelliferae: plant chetnistry and
commnnity structure. Ecology 62: 125T1266.
Bereociier, S. 11. 1998. Can sympatric speciation be proven from
biogeographic and phylogenetic evidence? I’p. 3-15. hv. 1). J.
1 loward and S. H, Bet locher (eds). Endless forms: species and
s|)eciation. New York. NY: Oxford University Press.
Bernavs, E. a. 1989. Host range in jthvtophagous insects: the
potential role of generalist itredators. Evolutionary Ecolog)'
3:299-311.
Bewick, J. A. 1979. Gypsy moth control |5rojcct report. Ma.ssachusetts
Executive Office of Environmental Affairs. Boston, AIA.
BinwEi E, R. G. S. & D. J. Dur/.on. 1975. Some recent aspects
of nitrogen metabolism. Pp. 152-155. hv. P. [. Davies (ed.).
Historical and current aspects of jtlant phy.siolog}': a svmposium
honoring F. G. Stewart. State College of Agricultural and Life
Sciences, New York.
Boeitn'er, C. J.. J. S. Ei.kinton, & C. G. Boeitner. 2009. Effects of
a biological control introduction on three nontarget native
species of saturniid moths. Conservation Biology 14(6): 1798-
1806.
Bowers, M. D. 1983. Iridoid glycosides and larval hostplant
specificity in checkerspot butterflies (Euphydrya.s, Nymphalidae).
J. Chem. Ecol. 9: 47.5-493.
Bowers, M. D. 1984. Iridoid glycosides and hostplant specificity in
larvae of the buckeye butterfly, yitttothrt coenia (Nymphalidae).
J. Chem. Ficol. 10: 1567-1577.
Bowers, M. D., N. E. Stamp, & E. D. Fa|er. 1991. Factors affecting
calculation of nutritional indices for foliage feeding insects:
an experimental approach. Entomologia Exjterimentiilis &
48
/. Rf.'t.Lepid.
A])plicacla 61: 101-116.
Brues, C. T. 1920. The selection of food-plants by insects, with
special reference to lepidopterons larvae. Ain. Nat. 54: 313-
332.
Brues, C. T. 1924. The s]>ecificity of foodplants in the evolntion of
irhytophagons insects. Am. Nat. 58: 127-144.
C.vnts, R. G. 1980. Feeding patterns of nionophagous,oligophagous,
and polyphagous insect herbivores: the effect of resource
abundance and plant chemistiy. Oecologia (Berl.) 46: 22-31.
(Ivies, R. G. & D. F. Rhoades. 1977. Patterns in the production
of anti-herbivore chemical defenses in plant communities.
Biochem. Syst. Ecol. 5: 185-193.
GovEi.i,, G. V. 1984. A field guide to the moths of Eastern North
America. Boston: Houghton Mifflin, Go.
Gui,ver, J. J. 1919. A study of Comfmlura concinnala, an imported
tachinid parasite of the gipsy moth and the brown-tail moth.
United States Department of Agriculture, Bulletin 766.
DuNwinniE, P. W. 1992. Changing landscapes: a pictorial field guide
to a century of change on Nantucket. Privately published.
Eiirlk:!!, P. R. & P. H. Rwen. 1964. Butterflies and plants: a study
in coevolution. Evolution 18: 586-608.
Ei.io'it I. M. & C. G. SoiiEE. 1902. Caterpillars and their moths.
New York: The Centuiy Co.
Emi.en, J. M. 1973. Feeding ecology. Pp. 157-185. /n: Ecology: an
evolutionary approach. Reading, MA: Addison-Wesley.
F.vrrei.l. B. D. 1998. “Inordinate fondness” explained: why are
there so many beetles? Science 281: 555-559.
Farrell, B. D. & C. Mrm'.R. 1990. Phylogenetics of insect/plant
interactions: have Phyllohrolka leaf beetles (Chrysomelidae)
and the Lamiales diversified in parallel? Evolution 44: 1389-
1403.
F..\rrell, B. D. & C. MirruR. 1998. The timing of insect/plant
diversification: might Tetmopes (Coleoptera: Cerambycidae)
and Asdepias (Asclepiadaceae) have co-evolved? Biol. J. Linn.
Soc. 63: 553-577.
F.vrquh.vr, D. W. 1934. The Lepidoptera of New England. PhD
dissertation. Harvard University.
Fergii.son, D. C. 1971 . The moths of North America, Fascicle 20. 2A
Bombycoidea: Saturniidae (Part). London: Curwen Press.
Forman, R.T.T (ed.). 1979. Pine barrens: eco.system and landscape.
New York: Academic Press.
Fr..\nk, K. D. 1988. Impact of outdoor lighting on moths: an
asessment. Journal of the Lepidopterists’ Society 42: 63-93.
Funk, , D. j., D. J. Fu'euvma, G. Or'i i, & A. Meyi-:r. 1995. A histoiy
of host associations and evolutionary diversification for
Oplimdla (Coleo|)tera: Chrysomelidae): new evidence from
mitochondrial DNA. Evolution 49: 1008-1017.
Futuyma, D. J. 1976. Foodplant specialization and environmental
predictability in Lepidoptera. Am. Nat. 1 10: 285-292.
Futuyma, D. J. Sc S. S. MoC.-vekeriy. 1990. Phylogeny and the
evolution of host plant associations in the leaf beetle genus
Ophmella (Coleoptera: Chrysomelidae). Evolution 44: 1885-
1913.
Ga.si()n, K. j. & D. Re,\vi-:y. 1989. Patterns in the life histories and
feeding strategies of British macrolepidoptera. Biol. J. Linn.
Soc. 37: 367-381.
Gilbert, L. E. 1979. Development of theory in the analysis of iiisect-
jjlant interactions, pp. 1 17-154. Im D. J. Horn, G. S. Stairs, and
R. 1). Mitchell (eds.). Analysis of Ecological Systems. Columbus:
(Dhio State University Press.
Goldstein, P. Z. 1991. Investigation of the natural history
and nutritional ecology' of a remnant jropiilation of Eades
imperia/is Druiy on Martha’s Vineyard Island, MassachusetLs.
Lhidergraduate thesis. Harvard University, Cambridge, MA.
Goi.iwtein, P. Z. 1997. Review of: Tuskes, Tuttle, and Collins.
The wild silk moths of North America. J. New York Ent. Soc.
105(1-2): 121-125.
Harris, T. W. (C. L. Flint, ed.) 1890. Treatise on some of the insects
injurious to vegetation. New York: Orange Judd Co. 640 pp.
[2'“' edition of: Harris, T. W. 1841. A report on the insects
of Massachusetts, injurious to vegetation. Cambridge, MA:
Folsom, Wells and Tluirston.]
H.4YES,J. L. 1983. Acomparison of the life history and moiphological
character patterns in temperate butterflies. J. Kans. Ent. Soc.
56: 547-551.
Hessel, S. A. 1976. A preliminaiy scan of rare and endangered
Nearctic moths. Atala 4: 19-21.
Hollow.ay.J. D. & P. D. N. Herbert. 1979. Ecological and taxonomic
trends in macrolepidopteran host plant selection. Biol.J. Linn.
Soc. 11: 229-251.
House, H. L. 1962. Insect nutrition. Ann. Rev. Biochem. 31:
653-672.
Howard, L. O. & W. F. Fiske. 1911. The importation into the United
States of the parasites of the gipsy-moth and the browntail moth.
USDA Bur. Entomol. Bull. 1911, 1.
J.AME.s, T. D. 'W. 8c D. W. Smith. 1978. Seasonal changes in the
major ash constituents of leaves and some woody components
of trembling aspect and red osier dogwood. Can. J. BoL 56:
1798-1803. "
Jermy, T. 1984. Evolution of insect/host plant relationships. Am.
Nat. 124: 609-6.30.
JoNE.s, F. M. & C. P. Kimball. 1943. The Lepidoptera of Nantucket
and Martha’s Vineyard Islands, Massachusetts. The Nantucket
Maria Mitchell Association. Vol. IV. Nantucket, MA.
Lem.vire, C. 1988. The Saturniidae of America. Ceratocampinae.
Museo Nacional de Costa Rica, San Jose.
Little. S. 1979. Fire and plant succession in the New Jersey Pine
Barrens. Pp. 297-.314. /«: Forman, R. T. T. (ed.). Pine Barrens:
ecosistem and landscape. Orlando, FL: Academic Press.
M.\tt.son, W. j. 1977. Size and abundance of forest Lepidoptera in
relation to host plant resources. Colloques Inteniatioiiaux du
C. N.R.S. 265: 429-441.
M.-vit.son, W. j. 1980. Herbivory in relation to plant nitrogen
content. Ann. Rev. Ecol. Syst. 11: 119-161.
M/Vrr.soN, W. J. & J. M. Scriber. 1987. Nutritional ecology' of insect
folivores of woody plants: nitrogen, water, fiber, and mineral
considerations. Pp. 114-139. /w: F. Slansky and J. G. Rodriguez
(eds.) , Nutritional ecology of insects, mites, spiders, and related
invertebrates. John Wiley and Sons, New York.
Meli.o, M., M. Ai.iberti, S. Galllsi-la, K. Gerber, F. Hohn, A. Lawrence,
D. Luers, R.J. Nagel, T. Ruehi.i & B. Stephen.son. 1999. Lloyd
Center for Environmental Studies. Inventory of state-listed
Lepidoptera and other insects at Massachusetts Military
Reservation 1996-1998. Report to Massachusetts Natural
Heritage & Endangered Species Program.
Michener, C. D. 1950. A northern subspecies of Backs imperialis
(Lepidoptera: Saturniidae). Jour. Kaiis. Ent. Soc. 23: 17-21.
Miller, P, C. & W. A. Stoner. 1979. Canopy structure and
environmental interactions. Pp. 428-458. Im O. T. Solbrig,
S. fain, G. B. Johnson and P. H. Raven (eds.), Topics in plant
population biology. New York: Columbia University Press.
Moli.s.seau, T. A. & H. Dingle. 1991. Maternal effects on insect life
histories. Ann. Rev. Entomol. 36: 511-534.
Niemeia, P., S. Hanhimaki, & R. M.anniia. 1981. The relationship
of adult size in noctuid moths (Lepidoptera: Noctuidae)
to breadth of diet and growth form of host plants. Annales
Entomologici Fennici 47: 17-20.
Opi.er, P. a. 1978. Interaction of plant life histoiy components as
related to arboreal herbivoiy. Pp. 23-32. Im G. G. Montgomeiy
(ed.). Ecology of Arboreal Folivores. Washington, D.C.:
Smithsonian Institute.
Patch, E. M. 1908. Insect notes for 1908. Maine Agric. Exp. Stn.
Bull. 162: 351-.387.
PF.TER.S, R. H. 1983. The ecological implications of body size.
42; 34-49, 2003 (2010)
49
(Cambridge: (lambt idge University Press.
R\iia, K. F. 1991. Induced del'ensive reactions in conifer-bark
beetle .systems. Pp. 245-276. In: D. W. Tallainyand M.J. Raupp
(eds.) Phytochemical induction by berbivores. New York:
Academic Press.
ScHWF.n zKR, D. F. 1983. Rare Lepidojitera of the Kiitama Plain on
Martha’s Vineyard, Massachtisetts. Report to Massachusetts
Natural Heritage and Engaiigered Species Program, Boston.
Sc.HWEirzKR, D. F. 1988. Stattis of Satnrniidae in the northeastern
USA: a quick review. News of the Lepido|>terists’ Society
[1988] 1:2-3.
Sc.HWEiT/.FR, D. F. &T. j. Rawin.ski. 1988. TNU Element stewardship
abstract: northeastern itch jDine/scrtib oak barrens. The Nature
Conservancy, Eastern Heritage Task Force, Boston, MA.
SciiROEDER, L. A. 1984. Comparison of gravimetry and planimetry
in determining dry matter budgets for three species of
phytophagous lepidopteran larvae. Entomol. Appl. 35: 25.5-
261.
St.RiBER, ). M. 1977. L.imiting effect of low-leaf-water content on
the nitrogen utilization, energy budget, anrl larval growth of
Hyaloplwm cecropia (Lepidoptera: Satnrniidae). Oecologia 28:
269-287.
ScRiBER, J. IVl. 1978. Fhe effects of larval feeding specialization
and plant growth form on the consumption and utilization of
plant biomass and nitrogen: an ecological consideration. Ent.
Exp. App. 24: 694-710. '
ScRiBER, |. M. 1 979a. The effects of sequentially switching foodplants
upon biomass and nitrogen utilization by polyphagous and
stenophagous larvae. Fait. Exp. Appl. 25: 203-215.
ScRiBER, J. M. 1979b. Fdfects of leafwaler .su]i]>lementation u|ion
postingestive nutritional indices of foil), slmib, vine, and
treefeeding l.e|)idoptera. Ent. Exj). Appl. 25: 240-252.
ScRiBER, J. .M. 1983. fhe evohuion of feeding s|)ecialization.
physiological efficiency, and host races in selected Papilionidae
and Satnrniidae. Pp. 373-412. In: Denno, R. F’. and M. S.
McClure (eds.). Variable plants and herbivores in natural and
managed .systems. NewYoi k: Academic Press.
ScRiBER, J. M. & P. Feeny. 1979. Growth ol herbivorous cateipillars
in relation to feeding s|)ecialization and to the growth form of
their food |)lant.s. FTology 60; 829-850.
ScRiBER, J. M. & F. Seansky. 1981. The nutritional ecology of
immature insects. Ann. Rev. Entomol. 26: 183-21 I.
Si.ANSRY, F. & J. M. ScRiBER. 1985. Food consumption and
utilization. Pp. 87-163. In: G. A. Kerkut and T. 1. Gilbert
(eds.). Comprehensive Insect Physiology, Biochemistry, and
Pharmacolog)' Vol. 4. Pergamon Press.
Sro.NE, S. E. 1991. Foodplants of world Sattirniidae. Tepid. Soc.
Memoir 4. L.epidopterists’ Society, Lawrence, Kans.
Tii.ton, D. L. 1977. Seasonal growth and foliar nutrients oi Lai ix
laricina in three wetland ecosystems. Can. j. Bot. 55: 1291-
1 298.
Tuskes, P. M., j. P. Tuiti e, & .VI. M. Cott.iNs. 1996. The wild silk
moths of North America. A natural history of the saturuiidae
of the United Stales and Canada. Ithaca; Cornell University
Press.
W.M DBAUER, G. P. 1968. The consumption and utilization of food
bv insects. Advances in Insect Physiology' 5: 229-288.
W.\s,SERMAN, S. S. & C. Miri'ER. 1978. The relationship of body size to
breadth of diet in some Le|)idopiera. Flcol. Fait. 3: 15.5-161).
Webber, R. T, & j. Sch.aeener Jr. 1926. 1 lost relations of Cowpsilnm
concinnutn Meigen, an important tachinid parasite of the gipsy
moth and the lirown-tail moth. Washingoii 1). C., USDA
bulletin 1363.
WiKi.L'Ni), C. 1975. The evolutionary relationships between adult
oviposition preference and larval host plant range in VnpiUo
machaonl,. Oecologia 18: 185-197.
journal oj Rrsearrh on the Lepuloptera
42: 50-55. 2003 (2010)
Association of three species of Strymon Hiibner (Lycaenidae: Theclinae;
Eumaeini) with bromeliads in southern Brazil
Simone Schmid*'--, Volki:r S. Schmid'-^, Rafael Kamke'^, Josefina Steiner^ and Anne Zillikens'-'^
'Mecl.-Naturwissenschaftliches Forschiingszentrum, Universitat Tubingen, 72074 Tubingen, Germany
-De])artnieiit of Cell Biology, Embiyology and Genetics (BEG), CCB, Federal Lbiiversity of Santa Catarina, Campus Universitario Trin-
dade, 88.040-900 Florianopolis, SC, Brazil
simigrohme@holmaiLcom
Abstract. As part of a project studying the species richness of bromeliad flower visitors and the
diversity and nature of their animal-plant interactions, three species of the lycaenid butterfly genus
Strymon were recorded as pests of bromeliad inflorescences. Strymon ziba fed on the fruits of Aechmea
n udicaulis, S. oreaki on those of Ae. lindenii and Ae. caudata and S. serapio on the dry capsules of Vriesea
friburgensis. The caterpillars of 5. zAfland S. oreala, pests t)f cultivated pineapple, were facultatively
associated with ants. One S. ziba pupa was parasitized by a chalcidid wasp. One S. oreala pupa was
parasitized by an ichneumonid wasp. BehaGoiir and life history data of the caterpillars are described
and aspects of the host specificity of the lycaenids and potential pest control by parasitoid wasps
are discussed.
Key words: Aechmea, animal-plant interactions, Atlantic rain forest, Bromeliaceae, Chalcididae,
herbivory, Ichneiimonidae, parasitism, restinga, Vriesea.
Introduction
Bromeliaceae, a neotropical plant family, can be
considered keystone species by providing microcosms
for the richness of tropical rain forests due to the
high diversity of animal taxa, especially arthropods,
associated -with them (Frank & Lounibos, 2008).
Among the latter, Lepidoptera are major lierbivores
with many caterpillars feeding upon bromeliad foliage:
Napaea eiicharilla Bates (Riodinidae) on Werauhia
sanguinolenta (Cogniaux & Marchal) R. Grant (syn.
Vriesea sanguinolenta, Schmidt & Zotz 2000), Aechmea
bracteata Grisebach, Ae. nudicaulis (L.) Grisebach
(Beiitelspacher, 1972) And Ananas comosus {V.) Merrill
(Schmidt & Zotz, 2000), Cana domitianus moFabridiis
(1793) (Riodinidae) on TUlandsia caput-medusae E.
Morren (Beuteispacher, 1972; Frank & Lounibos,
2008), Dynastor darius darius Stichel and D. niacrosiris
Westwood (Nymphalidae, Urich & Emmel, 1991a,
b) on Ae. nudicaulis and Castnia boisdiivalii Walker
(Castniidae, Biezaiiko, 1961; Frank & Lounibos, 2008)
on T. aeranthos (Loiseleur) L. B. Smith. Beuteispacher
( 1972) also mentioned Theda te|;m7«ButIer & Druce
1872 (Lycaenidae), which is a mistaken record of
Ziegleria hesperilis, feeding on TUlandsia caput-medusae,
but voucher specimens of “Theda hesperitis" in UNAM
*Correspon d i ng a ulhor
ReceixH'd: 25 Sepletnber 2009
Accepted: 15 October 2009
(Universidad Nacional Autonoma de Mexico)
examined by Robert K. Robbins are in fact S. serapio
Godman & Salvin (1887) (R. K. Robbins, pers.
comm.). Not only the plants’ vegetative parts, but
also their inflorescences contribute significantly to the
local fauna! biodiversity by providing resources for a
great variety of flower visitors that act as pollinators
or pollen and nectar robbers (Sazima & Sazima, 1999;
Machado & Semir, 2006; Caneia & Sazima, 2003;
Schmid et al, b, submitted). In addition to causing
leaf damage, some herbivorous arthropods associated
with bromeliad inflorescences directly interfere
with plant reproduction by feeding on reproductive
tissues of flowers and fruits, like beetles, butterflies
and moths, grasshoppers and even crabs (Fischer et
al., 1997; Caneia & Sazima, 2003; Frank & Lounibos,
2008). An example of inconspicuous herbivory
affecting plant reproductive success was observed in
the bromeliads Vriesea friburgensis Mez and Werauhia
gladioliflora (H. Wendland) J. R. Grant whose buds
are parasitized by Eurytoma wasps (Hymenoptera,
Eurytomidae) so no fruits are formed (Gates &
Cascaiite-Marm, 2004; Grohme et at, 2007). Beyond
that, cases of seed predation by C/jo/ms and Metamasius
weevils (Coleoptera, Ciircolioiiidae) (Frank 1999) and
Epimoritis testaceellusVAigonoi 1887 (Pyralidae) larvae
that develop in flower pods of TUlandsia fasciculata
Swartz (1788) (Biigbee, 1975; Heppiier, 1992) have
been I'eported. New World hairstreaks (genus Strymon,
Lycaenidae: Theclinae: Eumaeini) use ornamental
bromeliads (genera Aechmea, TUlandsia) and the
commercial pineapple {Ananas comosus) as host plants
42; 50-55, 2003 (2010)
51
(Robbins & Nicolay, 2002). Strymon megarus Godart
1824 (syn. Theda basilides, also misspelled as T. basalides)
larvae feed on Ananas and odier bromeliads like Ae.
bracteata (Bentelspacher, 1972; Frank & Lonnibos,
2008) and can be considered pest species. Strymon
ziba, S. serapio (Robbins & Nicolay, 2002) and .S', oreala
(Zikan, 1956) , the species examined in our study, were
reported to eat bromeliads, S. ziba Hewitson 1868 and
S. oreala Hewitson 1868 are known pests of A. comosus
(Harris, 1927; Zikan, 1956). Since caterpillars and
other immature stages of the Eumaeini are small and
ci'yptically coloured, food plants have been recorded
for only 25% of the species (Duarte et al., 2005).
Studying the species richness of bromeliad
flower visitors and the diversity and nature of their
animal-plant interactions in tlie Atlantic rain forest
of southern Brazil, we found lycaenid caterpillars
attacking developing fruits. In order to assess
the specificity of these associations we examined
inflorescences of four common sympatric bromeliad
species, Aechmea nudicauUs, Ae. Undenii (E. Morren)
Baker, caudato Lindman 1891 (Bromelioideae) and
Vriesea friburgensis (Tillandsioideae), for the presence
of larvae and reared them for identification. also
recorded basic data on development, behaviour and
natural enemies of the caterpillars.
Materials and methods
Bromeliads with inflorescences were searched for
eggs and larvae between November 2006 and June
2008 at four study sites (frost-free subtropical habitats) :
Santo Antonio de Lisboa and the Environmental
Conservation Unit Desterro UGAD (both secondary
forest; 27°.80’26” S, 48°30’28” ’V\^; 27°.3r 50” S, 48°30’50”
W) (Zillikens et al, 2001; Zillikens & Steiner, 2004) as
well as Joaquina Beach and Campeche Beach (dune
vegetation, Sampaio et al, 2002; 27°40’.38” S, 48°28’48”
W; 27°37’37” S, 48°26’59” W), on Santa Catarina
Island, southern Brazil. All bromeliads examined were
growing terrestrially although Aechmea nudicaidis Aho
occurs on trees. In total, 20 infested bromeliads of
four species {Aechmea nudicauUs, n = 11; Ae. lindenii,
n = 2; Ae. caudata, n = 5; and Vriesea friburgensis, n =
2), growing terrestrially on rocks, in sand or shallow
soil, were taken to the laboratory. Presence, size and
colour of eggs and caterpillars on the inflorescences
were observed regularly eveiy 1-2 days. Ants a.s.sociated
with lycaenid larvae were also collected. When larvae
had finished feeding and retreated for pupation, tlie
bromeliad plants were enclosed with fine gauze to
capture the emerging adult butterflies.
Voucher specimens of the recorded butterfly,
ant and parasitoid species were deposited in the
entomological collection of J. Steiner at the Native
Bee Laboratory (LANUESC), BEG, Federal University
of Santa Catarina, Florianopolis, Santa Catarina,
Brazil.
Results
Three lycaenid species of the genus Strymon were
reared from the caterpillars found on four bromeliad
species. All constitute new records of parasite/
host association. Up to four caterpillars were found
simultaneously on one inflorescence.
Strymon ziba (Hewitson 1868)
We found 24 laiwae of S. ziba on 1 1 inflorescences of
the bromeliad Aechmea nudicauUs, yielding an average
of 2.2 caterpillars per inflorescence (range 1-4) from
November 2006 to January 2007. Seventeen adults
emerged in the laboratory, overall sex ratio was 0.7
(M/F) . On all inflorescences we detected small white
spherical bodies, the eggs from which the larvae had
hatched (Fig. lA, B).
The colour of the larvae was cryptic and changed
during their growth from wliitish-yellow to reddisli-
pink (Fig. 1C, D). The former matched well to
the fruits whereas the latter matched well to the
inflorescence stem. The larvae appeared shortly after
the end of the flowering period and stayed close to the
ripening fruits. Larval feeding behaviour consisted of
gnawing a hole into the fruit base large enough for the
smaller larval stages to enter the fruit completely and
for the larger stages to insert the head anrl anterior
part into the cavity. Through this hole they fed on the
soft nutritive tissues of the ovaiy and ovules, leaving
the rigid cortical outer wall of the developing fruit
mostly intact (Fig. lA, B). On an inflorescence of
Ae. nudicauUs with two larvae feeding, 30 fruits were
damaged, resulting in a mean of 15 fruits damaged
per larva. Mean fruit loss per inflorescence was 84.5%
(n = 2). Occasionally, the larvae drew back from the
fruits to hide under the bracts for about lialf a day,
probably for moulting.
Development in the egg took five days (n = 2).
The larval phase lasted 1.3-15 days (ii = 1 ). The fully
grown larvae (-12-15 mm length) moved into the
bromeliad rosette where they pupated on the upper
side of the leaves half way between tip and base;
one male pupated on a bract of the inflorescence.
Pupation took 8-11 days (n = 3). Imagines (Fig. IE)
emerged between mid November until end of January,
synchronized to the flowering/fruiting period of Ae.
nudicauUs.
In the laboratory, caterpillars were occasionally
52
/. Res.Lepid.
Figure 1. Strymon larvae on bromeliads on Santa Catarina Island, Southern Brazil.
A-P; Strymon larvae and imagines and associated ants
A-B: Infested fruits of Aechmea nudicauiis, Santa Catarina Island, Brazil. A: Fruit with feeding hole and larval faeces of
Strymon caterpillar and a hatched egg of Strymon ziba at the base of the fruit. B: Fruit with feeding hole and a closed egg.
C-D: Colour change in Strymon ziba larvae. C: Small, whitish-yellow. D: Larger larva after colour change to reddish-pink. E:
Strymon ziba female, collected on Aechmea nudicauiis, Santa Catarina Island, Brazil. Right-hand side ventral view, left-hand
side dorsal view. F-l: Ants associated with Strymon ziba caterpillars. F; Crematogaster limata. G: Linepithema iniquum. H:
Monomorium sp. (floricola). I: Paratrechina sp. J: Strymon oreala, female, right-hand side ventral view, left-hand side dorsal
view. K; Strymon oreala larva feeding on fruits of Aechmea caudata. L: Larva of S. oreala feeding on withered flower petals.
M: Tapinoma melanocephalum ant on the back of a S. oreala larva (v/hite arrow). N: Strymon serapio, female, right-hand side
ventral view, left-hand side dorsal view. O: Larva of S. serapio on dry fruit of Vriesea friburgensis with feeding hole. P: Dry fruit
of Vriesea friburgensis with exuvia of S. serapio inside. Length of exuvia: = 1 2 mm.
Q-W: Strymon larvae at A. lindenii and parasitoids.
Q-R: Strymon larvae. Q: Strymon larva on A. lindenii feeding on fruit. R: Strymon pupa on infructescence.
S-T: Anisobas, a parasitoid of Strymon sp. S: Lateral view of the Anisobas imago that hatched from the Strymon exuvia. T;
Opened Strymon exuvia besides hatched Anisobas imago. U-W: Conura, a parasitoid of Strymon sp. U: Opened pupal case
of Strymon sp. V: Imago of Conura sp., dorsal view. W: Lateral view.
42: 50-55, 2003 (2010)
53
tended by ants of four species: Crematogaster limatn^mith
1858, Linepithema iniquum Mayr 1870, Monomorium
//onro/fl Jerdon 1851 and Paratrechina (Fig. lF-1).
Tending worker ants walked over the bodies of the
caterpillars and took up small droplets secreted
posterodorsally (Fig. IF).
Additionally, we observed S. z//;a imagines sucking
extrafloral and floral nectar from inflorescences of
Ae. nudicaulis and one female laying one single egg
on each of two recently withered flowers, respectively.
The female flew around the inflorescence and sucked
nectar of several flowers before ovipositing. The
initially greenish eggs turned white after a few minutes.
Thereafter, the female left the inflorescence.
Strymon oreala (Hewitson 1868)
We discovered seven larvae of ,S’. oreala (Fig. IJ) on
five inflorescences of the bromeliad Ae. caudata (April
2008) and two larvae on two inflorescences of Ae.
lindenii (August - September 2007) . As described foi¬
ls'. ziha on Ae. nudicaulis larvae fed on the developing
fruits of A^'. lindenii And Ae. caudata (Fig. IK-M) and
retreated into the rosette for pupation. Additionally,
a larva was seen feeding on withered flower leaves,
probably eating old reproductive structures inside the
petals (Fig. IL). On an inflorescence of Ac. caudata
with one larva feeding, 15 fruits were damaged. The
pupal stage took 15-16 days (n = 4). The larvae were
reddish-pink like the inflorescence stem (Fig. 1 K-M).
Occasionally, single ants of the species Tapinoma
melanocephalum Fabricius 1793 were observed on .S',
orm/rt larvae (Fig. IM).
Strymon serapio (Godman 8c Salvin 1887)
We detected four browuish-yellow larvae of
S. serapio (Fig. IN) on two inflorescences of the
bromeliad Vriesea friburgensis in secondary forest in
December 2007. The larvae chewed a hole into the
hard capsule of the developing fruit (Fig. lO) and
fed on the seeds within. Pupation took place inside
the empty fruit capsule (Fig. IP), the imago emerged
after 1 1 days (n = 1).
Parasitoids
On two occasions we found Strymon brood infested
with a parasitoid. The first case (14 November 2005,
Oampeche Beach) was a larva on an inflorescence
of Ac. lindenii (Fig. IQ). Since the only identified
Strymon infestation of this bromeliad was by .S’, orecda
(see above) we assume that the parasitized larva
belonged to the same species. The larva pupated
on the infriictescence on 18’'’ November 2005 (Fig.
IR). This might, however, not be the usual location
for pupating because Aurum® insect glue had been
applied to the infriictescence stem, thus preventing
the caterpillar from moving down to the rosette. After
18 days an ichneumonid wasp of the genus Anisohas
(subfamily Ichneumoninae) emerged from the pupa
(Fig. IS, T).
In the second case, discovered 6 January 2007 at
Santo Antonio, a pupa (Fig. lU) was located at the
upper margin of a leaf of Ac. nudicaulis (plant with
infriictescence). So far, we found this bromeliad
species only to be infested with .S', ziba (see above);
hence we assume that the pupa belonged to this
species. On 23 January 2007, a chalcidid wasp of the
genus Conura (subfamily Chalcidinae), “most probably
of the //aw; group” (Gerard Delvare, pers. comm.),
emerged from the pupa (Fig. IV, W).
Discussion
Larval behaviour and host plants
Our findings constitute new host records for the
associated Strymon species. The only lycaeuids so far
recorded on Ac. lindenii Are larvae of an uuidentified
species of Theda on Santa Catarina Island (Lenzi
et al. 2006) with a similar feeding behaviour and
life history data as described here for .S', oreala. It
is therefore possible that they did in fact observe
larvae of a species of Strymon. Our observations also
confirm some life history traits rejiorted by Duarte et
al. (2005) such as the cryptic coloration of the larvae
w4uch is well adapted to parts of the plants on which
they move or feed. Besides the evident association
of Strymon larvae with infructescences, they were
even more selective in the sense that they fed only
on the internal parts of the developing fruits, i.e.
the ovaries, but not on leaves, sepals or other plant
tissues. By hollowing out the fruits they create their
own shelter for feeding or even pupal chambers (in
case of .S', serapio) .
We further report here the first data ou the
life cycle of the three species, all of which develop
within about one month and without diapause. It is
therefore likely that the Strymon species studied by
us are multivoltine having several generations per
year. This is in agreement with the pattern reported
for other Strymon species in the tropics (Opler et al.
2009). The choice of hosts by ovipositing females
depends on seasonal availability of fruiting plants.
The bromeliads studied by us all have relatively short
and seasonal fruiting periods, so that only one or two
generations can develop on a given ])lant population.
54
J. Res.Lep 'td.
Adults emerging at the end of a flowering period have
to seek for alternative hosts for egg laying. In our
study, Strymon orealawAS the only species recorded on
two hosts both in the genus Aechmea. Interestingly,
the inflorescences and flowers of Ac. lindenii and Ae.
caudata are very similar in floral morphology and
coloration (Kiimke, pers. obs.), but Aechmea lindenii
flowers from August to November (Dorneles et at,
ms) whereas Ae. caudata flowers from March to June
without overlap, though single plants of both Aechmea
species can be found flowering outside the main
flowering period, for example Ae. lindenii on more
open areas in restinga sites throughout the year (Lenzi
et al. 2006) and Ae. caudata in secondary forest in
September (Ktimke, pers. obs.). Nevertheless, there is
a gap of several months for which we do not yet know
the host plants. We know, however, that S. oreala does
not attack the infructescences of Ae. nudicaulis or V.
frihurgensis, which flower between. Therefore, a switch
to another host, whether bromeliad or not, must occur
in .S’, orecdn, S. serapio and S. ziba.
As .S', ziba and S. oreala are pests of cultivated
pineapple it would be interesting to further identify
alternative host plant species in order to better
understand under which circumstances the larvae
reach pest status and to assess their damage to the
crop. In this context it is also worth emphasizing
our record of a possible natural enemy of S. ziba, a
parasitoid wasp of the family Chalcididae. Its potential
as natural biological control agent should be assessed
by elucidating its life history, abundance and host
specihcity.
Association with ants
As has been reported from other lycaenid
caterpillars, the larvae of .S', ziba possess a dorsal
secretory organ, the Newcomer’s gland (Malicky
1970), that might exude honey-like droplets to
appease ants. Of the species recorded, Monomorium
Jloricola dnd Tapinoma melanocephalumme invasive ants
(Delabie et al. 1995; Campos-Farinha 2005) and only
occurred in the laboratory. We consider the same
to be true for Pciratrechina sp. for this species was
only observed in the laboratory. Cremcitognster limata
and Linepithema inicjuum, however, were frequently
found nesting in the bromeliads or visiting their
inflorescences (Rostimek et al. 2008, Schmid et al a,
ms) and were thus brought to the laboratory together
with the plants taken in the field. These two, at
least, may be considered associated with the Strymon
cater|)illars under natural conditions, albeit only
facidtatively since larvae observed in the held were
mostly not tended by ants.
Diversity of the Strymon - bromeliad association
Our hnding that four species of bromeliads were
parasitized in very similar ways by Strymoyi larvae
is remarkable in yet another aspect. It conhrms a
relatively high diversity and abundance of sympatric,
even syntopic, Strymon species in bromeliad-rich
Atlantic forest and restinga habitats of southern Brazil.
Thus, the fact that three co-occurring species were
recorded in studies on only four bromeliad species
sitggests that a thorough examination of further
bromeliad inflorescences might result in the hnding of
more Strymon species and underlines the importance
of these plants for sustaining a high diversity of the
lepidopteran fauna in the Mata Atlantica.
Acknowledgements
We tliank Robert K. Robbins for lycaenid identibcation and
valuable help with Strymon taxonomy and literature, as well as David
Wahl and Gerard Delvare for parasitoid identification. This study
is part of the Project “Internal dynamics of rain forest: specificity
of animal-plant interaction” within the Brazilian-German program
“Mata Atlantica”, and we acknowledge the financial sup]>ort by
BMBF (01LB02()5A1) and CNPq (59004()/2()0(>5).
Literature cited
Bi:uiEt..st>ACHKR, C. R. 1972. Some observations on the Lepidoptera
of bromeliads. Jonrtial of the Lepidopterists’ Society 26: 133-
137.
Bikz.vnko, C. M. 1961. Castniidae, Zygaenidae, Dalceridae,
Encleidae, Megalopygidae, Cossidae et Hepialidae da Zona
Missioneira do Rio Grande do Sul. Arqiiivos de Entomologia
Serie B, Escola de Agronomia “Eliseu Maciel” 14 : 1-12.
Buoisee, R. E. 1975. A new species of the getius Eurytoma
(Hymenoptera: Emytomidae) from a |tyralid occurring in the
flower pods of Titlnndsia famrulata. Journal of the Georgia
Entomological Society 10: 91-93.
Gami’os-Farinha, A. E. 2005. Urban pest ant.s of Brazil (Hymenoptera:
Formicidae). In: Proceedings of the Fifth International
Conference on Urbati Pests. Chow-Yang Lee and William II.
Robinsoti (editors), 81-84.
C.ANEt.A, M. B. F. & M. .SAZtMA. 2003. Florivoiy by the crab Arntnsn
angustipes influetices hntmningbird visits to Aechmea pectinata
(Bromeliaceae). Biotropica 35: 289-294.
Delabie, |. H. C., I. C. Do Nascimenio, P. Pacheco & A. B.
Casimiro. 1995. Community structure of house-infesting ants
(Hymenoptera: Formicidae) in southern Bahia, Brazil. Florida
Entomologist 78: 264-270.
Dorneles, L. L., A. Zillikens, B. Harier-Marques & J. Steiner.
Submitted. Mixed pollination by hummingbirds and bees
in Aechmea lindenii (Bromeliaceae) in Atlantic Rain Forest
at Santa Catarina Island, southern Brazil. Sid>mitted to
Entomologia Generalis.
Duarte, M., R. K. Robbins &• O. H. H. Miei.ke. 2005. Immature
stages of Cnlycopis rantonia (Hewitson, 1877) (Lepidoptera,
Lycaenidae, Theclinae, E.umaeini), with notes on rearing
detritivorous hairstreaks on artificial diet. Zootaxa 1063:
1-31.
Fischer, E. A., L. F. I.. Du.vri e & A. C. Ar-VUIo. 1997. Consumption of
42: 50-55, 2003 (2010)
Bromeliad flowers by the crab Melasesarma ndmpes in a Brazilian
coastal forest. Crustaceana 70: 118-123.
Fr..\nk, ]. H. 1999. Bronieliad-eating weevils. Selbyana 20: 40-48.
Fr.-\nk, J. H. & L. P. Lolinibos. 2008. Insects and allies associated
with bronieliads: a review. Terrestrial Arthropod Reviews 1:
125-153.
G. vtes, M. W. & A. Cascan’I'e-M.-vrIn. 2004. A new phytophagotis
species of Euryloma (Hymenoptera: Eurytoniidae) attacking
Wmiuhia gladioUflora (Bronieliales: Bronieliaceae). Zootaxa
512: 1-10.
Grohme, S., J. Steiner & A. Zii.i.ikens. 2007. Destruction of floral
buds in the bi'oineliad Vriesea friburgensis by the phytophagous
lan'ae of the wasp Ewjlomasp in southern Brazil (Hymenoptera:
Eun'tomidae). Entomologia Generalis 30: 167-172.
H. arris, W. V. 1927. On a lycaenid butterfly attacking pineapples in
Trinidad, B.W.l. Bull. Entomological Research 18: 183-188.
Heppner, J. 1992. Bromeliad pod borer, Epimorms leslaceellus
(Lcpidoptera: Pyralidae: Gallerinae). Florida Department of
Agriculture and Consumer Services, Division of Plant Industiy,
Entomology Circular 351: 1-2.
Lenzi, M., }. Z. De M.\tos & A. 1. Ortu. 2006. Variacao morfologica
e reprodutiva de Aechmea Undenii (E. Morren) Baker var. lindenii
(Bronieliaceae). Acta Botanica Brasilica 20: 487-500.
M.ACH.41X), C. G. &J. Semir. 2006. Fenologia da lloracao e hiologia
floral de bromeliaceas ornitofilas de uma area da Mata Atlantica
do Sndeste brasileiro. ReMsta Brasileira de Botanica 29: 163-
174.
M.ai.k'.ky, H. 1927. New asjiecLs on the association between Ivcaenid
larvae (Lycaenidae) and ants (Formicidae, Hymenoptera).
Journal of the Lepidopterists’ Society 24: 190-202.
Opi.er, P. a., K. Lorrs & T. N.vberh.aus. 2009. Butterflies and moths
of North America. Bozeman, MT: Big Sky Institute. Available
from: http:/ /www.butterfliesandmoths.org/ (Accessed
23/09/2009).
Robbins, R. K. & S. S. Nic:oi..av. 2002. An overview of Stnmoti
Hiibner (Lycaenidae, Theclinae, Eumaeini). Journal of the
Lepidopterists’ Society 55: 85-100.
Rosumek, F. B., M. a. Ui.yssea, B. C. Lopes, J. Sieiner & A. Zii.i.ikens.
2008. Formigas de solo e de bromelias em uma area de .Vlata
Atlantica, llha de Santa Catarina, sul do Brasil: Levantamento
de especies e novos registros. Biotemas 21: 81-89.
S.\.\ipaio, .M. C., L. E. Perisse, G. A. De Oliveira & R. 1. Rios. 2002.
The contrasting clonal architecture of two bronieliads from
sandy coastal plains in Brazil. Flora 197: 44.3-451.
S.azima, M. & I. S.AZiMA. 1999. The perching bird Com’ba flaxml a
as a co-pollinator of bromeliad flowers in southeastern Brazil.
Canadian Journal of Zoology 77: 47-51.
ScHMin, V. S., S. Schmid, J. Steiner & A. Zii.i.ikens. a. Accepted.
High diversity of ants foraging on extrafloral nectar of
bronieliads in the Atlantic rainforest of southern Brazil.
Accepted for publication in Studies on Neotropical Fauna and
Environment.
Schmid, S., V. S. Sch.mid, B. Harier-Marques, J. Sieiner & A.
Zii.i.ikens. b. Submu'Ied. Biniodal pollination system of the
bromeliad Aechmea nudicaulis involving hummingbirds and
bees. Submitted to Plant Biology.
Schmidt, G. & G. Zotz. 2000. Herbivoiy in the epiphyte, Vriesea
sanguinolen/a Cogn. & Marchal (Bronieliaceae). Journal of
Tropical Ecology 16: 829-839.
Urich, F. C. & T. C. Emmel. 1991a. Life history of neotropical
butterflies from Trinidad 4. Dynastor macrosiris (Lepidoptera:
Nymjihalidae: Bra.ssolinae). Tropical Lepidoptera 2: 141-144.
Urich, F. C. & T. C. Emmet. 1991b. Life history of neotropical
butterflies from Trinidad 5. Dynastor darius darius (Lepidoptera:
Nymphalidae: Brassolinae). Tropical Lepidoptera 2: 14.5-149.
ZiK.\N, J. F. 1956. Beitrag zur Biologie von 12 Theclinen-Arten.
Dusenia 7: 139-148.
Zii.LiKENS, A., J. .Steiner & Z. Mihalko. 2001. Nests of A ugochlora
(A.) raoxin bronieliads, a previously unknown site for sweat bees
(1 Ivmenoptera: Halictidae). Studies on Netitropical Fauna and
Environment 36: 137-142.
Zii.i.ikens, A. & J. Steiner. 2004. Nest architecture, life cycle and
cleptoparasite of the neotropical leaf-cutting bee Megachile
{(ihrysosanis) pseudanthidioides .Moure ( Hymenojitera:
Megachilidae). Journal of the Kansas Entomological Society
77: 19.3-202.
journal of lirsearch on the I .epidoptera
42; 56-63, 2003 (2010)
Temporal and spatial segregation of Battus devilliers and B. polydamm cubemis
(Papilionidae) in La Habana, Cuba
Ormaily Madrliga Rios* and Alejandro Barro Canamero
Departamento de Biologia Aiiinial y Humana, Faciiltad de Biologi'a, Universidad de La Habana, calle 25 # 455 e/ I yj, Vedado, CP: 10
400, Ciudad de La Habana, Cuba.
al)airo@fhio. uh. ru
Abstract. The spatial and temporal distribution of two syntopic species of the genus Battus
(Papilionidae) that inhabit two areas in the north coast of La Habana, Cuba, is analyzed. The study
was carried out from April 2006 to March 2007. Samples were taken using transects 100 m long,
separated from each other by 80 m gaps. Populations of E. polydamas rubensis and B. devillim of
(he evergreen forest at Boca de Canasi, the most natural habitat, had similar abundance, while in
the secondary scrub at Boca dejaruco, an extremely degraded area, B. polydamas cubmsis wd.s much
more abundant than B. devilliers. Analysis of structural subniche usage by season showed significant
differences in daily actirity (from 9:00 am to 12:00 m and from 12:{)() m to 3:00 pm) and habifcit
type for each species. Flight stratum had lesser influence than sunlight intensity on both butterflies.
Populations of the latter seemed to be influenced by seasonality, while those of if. polydamas cubensis
seemed more infhienced by habitat.
Keywords: Battus, Cuba, Papilionidae, .segregation, syntopic species.
Introduction
Ecological roles of butterflies are important for
ecosystems functioning, with their study needed to
better understand their ecological interactions and
functions. In Cuba, only Fontenla (1989) and Genaro
et al. (1994) have conducted studies focusing on
butterflies communities and their resource partitioning
in a particular habitat. Due to their rapid reproduction
and close association with specific physical factors
and plant resources butterflies are highly sensitive to
environmental changes, so they are good indicators
of ecosystem health (Brown, 1991; Kremen, 1992;
New et al, 1995; New, 1997; Brown & Freitas, 2000).
Battus presents a Neotropical distribution (Sims &
Shapiro, 1983) with 12 or 14 species (Tyler et at,
1994; Racheli & Pariset, 1992, respectively). The
coevolutionary association of Battus with their host
plant, Arist(}lochias\i\). (Aristolochiaceae), as well as the
mimetic interactions among members of this butterfly
genus may be the subject of many studies on butterfly
community structure (Young, 1972, 1973).
Battus devilliers (Godart, 1823) and B. polydamas
^Current addres.r. Vicedirecdoii Curatofial, Miuseo Nacioiial de
Histoi'ia Natural de Guba. Obispo 61, esq. Oficios, Habana Vieja,
CP: 10 100, Ciudad de La Habaua.
ormaily@ninhtic.inf.cii
Received: 21 May 2009
Accepted: 30 July 2009
cubensis (Dufraiie, 1946) are the only members of
the genus that inhabit Cuba. The former occurs in
Bahamas (Knowles & Smith, 1995) and the latter was
reported at Cayman Islands in 1938 (Carpenter &
Lewis, 1943), but there has been no recent mention
of further records for these islands (Askew, 1980,
1988; Schwartz et al, 1987). On several occasions
(Alayoii & Solana, 1989; Racheli & Pariset, 1992;
Nunez & Barro, 2003) both species were recorded in
Cuba as syntopic {sensu Rivas, 1964) . The interaction
becomes more interesting considering the different
habitat requirements of B. polydamas and B. devilliers
mentioned by Tyler et al (1994), who established
that Battus polydamas is very common in disturbed
forest, while B. devilliers prefer more natural seasonal
forest. Since resource use for both species in Cuba
is completely unknown, we undertook a study of
temporal and spatial patterns of two populations on
the northwestern coast of Cuba.
Materials and methods
Study areas
The study was conducted at two localities of tlie north
coast of La Habana. Both areas are dose to human
populations and show different levels of degradation.
Boca de Jariico is 45 km east of La Habana city, at
23° 1 r N, 82°0r W. The site is typified by secondaiy
vegetation with many herbs and bushes and is the most
impacted area, which is why the habitat is categorized
42; r>(>63, 2003 (2010)
57
Figure 1 . Study Sites. A: Secondary scrub of Boca de Jaruco. B: Sea grape forest of Boca de Canasi. C: Evergreen forest
of Boca de Canasi. D: Summit of the hill where the evergreen forest canopy of Boca de Canasi becomes open.
as secondaiy scrub (Fig. la). The unique eniei'gent
large trees are isolated Ficus sp. (Moraceae). There
are many invasive plants, the most abundant being
Acacia famesiana (L.) Willd., (Mimosaceae), Comocladia
dentaia ]-AC(\. (Anacardiaceac) and members of the
family Poaceae. Common species also includes Lantaua
Camara L. (Verbenaceae) and Viguiera dcntata (Cav.)
Spreng., (Asteraceae), and vines as Merrcmia dissecta
(|acq.) Hallierf., (Convolvulaceae), Cucumis dipsacnis
Ehrenb., (Curcubitaceae) and Aristolochia hilahiata L..
During the dry season there are natural burns.
Boca de Canasi is 20 km east from Boca de jaruco,
at 23°09’ N and 81°47’ W. Two different habitat were
analyzed there: a sea grape [Coccoloba uvifera (L.) L.
(Polygonaceae)] forest (Fig. lb), and an evergreen
forest (Fig. Ic, d). The latter is crossed by several
paths, but is less frequented by persons than the
former. It also has higher relative humidity due to
the cover of arboreal species such as Burscra simaruha
(L.) Sarg. (Burseraceae) and Coccoloba divcrsifolia
Jacq. that reduce incident sunlight. Endemic plants
like Coccolriuax borhidiaua O. Mnhiz (Arecaceae),
Lcptocercus lurightii Leon (Cactaceae) and Eugenia
molUfoUaXJrh. (Myrtaceae) are also common (Borhidi,
1996). On the summit of the hill (ca. 100 m above
sea level) the evergreen forest canopy opens and
bushes like Acacia faruesiana and Croton lucidus L.
(Euphorbiaceae) are abundant.
Ecological counts
Boca de Jaruco was sampled from April 2006 to
March 2007. At Boca de Canasi sampling started July
2006 in the evergreen forest, while in the sea grape
habitat counts began on April 2006, ending on March
2007 and January 2007, respectively. The transect
58
/. Res.Lepid.
iiietliod was followed. Individuals were counted only
when seen from the sides or the front of observer,
never from behind, within a range of approximately 5
m. At least once a month, eight transects were sampled
each hour, from 9:00 a.m. to 3:00 p.m., at each
studied site. Transect length was 100 m, the transects
se|)arated from each other by 80 m. At the end of the
study a total of 992 transects in the secondary scrub
of Boca dejarnco were covered, 352 in the sea grape
and 336 in the evergreen forest.
Simlight intensity and flight stratum were recorded
for each specimen. These dimensions of structural
snbniche were used to analyze part of the spatial
segregation. Border values of each category in a
particidar dimension were determined following
previous Cid^an ecological studies on butterflies
(Fontenlak, 1989; Genaro et al, 1994).
For sunlight intensity three categories were dehned:
sunny (when individual flies directly in sunlight,
without any vegetation cover), filtered sun (when
individual flies under some vegetation cover, but still
in sunlight) and shading (when individual flies where
vegetation cover is so dense that it is difficult for
sunlight to enter). Three categories of flight stratum
from ground to above 3 m were defined: first level from
the ground (0 - 1.5 m), second 1.5 - 3.0 m, and third >
3.0 m. Wdien the same individual moved from one level
to another only the first stratum seen was recorded.
Due to variation of climate throughout the day, the
ttvo variables were analyzed separately over a two hours
range, 9:00 am -12:00 m, and 12:00 m -3:00 pm.
Relative abundance was correlated with mean
precipitation of the previous month. This correlation
was due to both the influence of rain on vegetation and
the time it taikes for plant growth (rains increase flower
abundance, for example). We used a correlation
between these variables based on published residts
showing that nectar source availability is an important
condition for a well developed butterfly community
(('Jansen et al, 2001). 'Values of mean precipitation
per month were supplied by the Instituto Nacional de
Recursos Hidraulicos.
Statistical analysis
(iraphPad InStat, version 3.01 (1998) software
was used for data analysis. The Kohnogorov-Smirnov
test was the first step in every case to evaluate data
normality (p < 0.10). Median and 25 and 75 percentils
were calculated. A Mann- Whitney U-test was used to
compare the values of the same variable due to the
nonparametric natitre of data. Comparison of three
or more values was performed with a Kruskal-Wallis
test. W'hen the later was significant (p < 0.05), a
Dunn’s Multiple Comparisons Post-Test was applied.
Correlation between two variables was analyzed with
a Nonparametric Correlation (Spearman r).
Results and discussion
Spatial segregation
Habitat use. The greatest difference between
populations of both species relates to their abundance
in each habitat type. In the three habitats B. polydamas
cubensis is common while B. dexnlliers is rare (Fig. 2).
Human disturbance of both studied areas may be
one of the factors affecting rarity, considering the
habitat requirements mentioned by Tyler et al. (1994) .
Boca de Jarnco is the most disturbed site and has
the highest proportional abundance of B. polydamas
cubensis across all the sites sampled. On the other
hand, the evergreen forest of Boca de Canasf is the
best preserved habitat of the triad and possesses the
highest proportion of B. devilliers individuals, even
during the dry season (Fig. 3). Concerning habitat
requirements, Alayon and Solatia (1989) reported that
both species coexist in Cuchillas del Toa, specifically
in the ecotone between forest and cleared areas.
No statistical significance was found correlating
precipitation mean of the previous month and species
relative abundance, except in the sea grape forest
(Table 1). This may be due this site being mostly a
feeding area, since no host plants were found. Thus
the presence of butterflies is strongly related with
flower availability. Additionally, the presence, in this
habitat, of non native plants probably might increase
tlie flower availability annually (Nunez & Barro, 2003) ,
and could be the reason why the rain acts like the
primary factor influencing flowering. Although the
secondary scrub presents almost the same non native
plants as the sea grape forest, there is no correlation
of butterfly abtmdance with rain. It is likely that, in
this habitat, flower availability is not the primaiy factor
Table 1. Values of the Nonparametric Correlation
(Spearman r) between relative abundance of the
populations (measured as the mean of the major number
of individuals in a single count) and precipitation mean of
the previous month.
Specie.s/I labitat
Secondary
scrub
Evergreen
forest
Sea grape
forest
Battus pots'damns
0.3082
0.3531
0.6786
cubensis
Battus dndttiers
0..3935
-0.09258
No
42; 56-63, 2003 (2010)
59
2006 2007
I I Battus polydamas cubensis ■■■ Battus devilliers — Precipitations
B
45
240
200
160
120
80
40
0
2006
2007
c
2006 2007
I I Battus polydamas cubensis
I Battus devilliers
—h— Precipitations
I I Battus polydamas cubensis Battus devilliers — Precipitations
Figure 2. Population densities of Battus devilliers and B. polydamas cubensis, from April, 2006 to March, 2007. A: Secondary
scrub of Boca de Jaruco. B: Evergreen forest of Boca de Canasi. C: Sea grape forest of Boca de Canasi. Gray line represents
precipitations per month. Black squares represents relative abundance of Battus devilliers and the white ones those of B.
polydamas cubensis. The blank spaces were not sampled. Relative abundance was the highest number of individuals observed
in one hour.
B
100%
80%
60%
40%
20%
0%
■o
o
S
62,
100%
80%
60%
40%
20%
0%
Rain Season
Dry Season
Rain Season
Dry Season
Figure 3. Proportional abundance of Battus devilliers and B. polydamas cubensis in the habitats in which they coexist. A:
Secondary scrub of Boca de Jaruco. B: Evergreen forest of Boca de Canasi. The black colour represents Battus devilliers
and white shows B. polydamas cubensis.
influencing the abundance of the.se butterflies. It may
be host plant availability, for example.
At Boca de Canasi both species coexist only in the
evergreen forest (Fig. 2), thus, no statistical analysis
was made for the sea grape liabitat. However, nearness
of the two sites and the floristic diversity at the latter
(Nunez & Barro, 2003) seem to support the idea of
delimited feeding and breeding areas for a single
population of B. polydamm cubensis. In this manner,
the sea grape forest may be the foraging area and the
evergreen forest the reproductive site (liost plants
observed only in the latter). This behavior was
previously described for a Costa Rican population
of this species by Young (1972). It may also explain
/. Res.Lepid.
(■)()
the differential abtindance of /j. polydamas cubensis Al
each habitat, secondary scrub and evergreen forest.
Another consec|nence of the behavior may be the
similarity between relative abtindance of both species
in the evergreen forest dtiring the rainy season (U =
3.5, p = 0.2469) due to an underestimation in counts of
the actual ntimber of individttals in the population of
B. polydai/ias cuhensis (Fig. 4). Data for the dry season
were instifficient for analysis.
By contrast, populations of both species in Boca
de Jarnco differed significantly (U = 1.5, p = 0.01 04)
during the rainy season and more so dtiring the dry
period (U = 0, p = 0.0022). Battus dnrilliers was always
rare compared with B. polydamas cuhensis (Fig. 4).
However, OMR saw both species in equal proportion
during the study period at another site approximately
1 km west of transects and nearest to Jarnco River,
where native vegetation was best preserved.
Another reason concerning life cycle and
reprochictive strategy may contribtite to the success
of B. polydamas cuhensis. Gregarionsness of eggs and
larval stages may be the most important becatise of
the benefits described for the behavior as stated by
Stamp (1980), Matsttmoto (1989) and Reader and
Hochtili (2003). Gregariotis early stages are absent
in B. dmilliers.
Structural subniche
Sunlight intensity. Large sunny patches are common
in Boca de [ariico due to the presence of abundant
herbs and bushes and only few isolated large trees.
Accordingly, sunny patches were the category most
tised in that habitat. The Kruskall-Wallis Test shows
differences among the different levels for both
s})ecies. The Dunn’s Mtiltiple (ionijjarisons post test
demonstrates that in the morning those differences
occur between sunny patches and the other levels
(p < 0.001 for both species). During the afternoon
differences in the tise of three levels were also present.
The results of post test were p < 0.001 comparing
stmny patches w'ith the other two, although sun filtered
and shading patches usage by B. polydamas cuhensis
increases (Fig. 5a, b).
At Boca de (ianasf, vegetation cover is more highly
developed, .so snn filtered and shading patches are
more freqtient than at Boca de Jarnco. Neverthele.ss,
vahies of Krnskall-Wallis Test show differences among
the mentioned levels. Only B. devilliers increased
significantly the using of sun filtered sites in the same
|)roportion as stmny patches. Statistical differences
were between stmny and shading levels (p < 0.05)
and between filtered and shading ones (p < 0.01) in
the first hours of day, while dtiring the afternoon the
same relation occurs, btit without individuals flying
in shading patches (Fig. 5c, d). On the other hand,
B. polydamas cuhensis always preferred sunny patches.
Differences in the morning were between first level
(stmny) and the filtered and shading patches (p < 0.001
in both cases). During the afternoon no individuals
were observed flying in shading patches (Fig. 5c, cl).
Our results show that the tise of this structural
dimension depends not only c:m habitat, but on
the ecological requirements of species. At Boca de
Jarnco, sunny sites ccwer most of the sttidy area and
coirsequently both species made major use of them.
Nevertheless, in Boca de Canasf, even when vegetation
cover increased in the forest, t^nly B. devilliers used
filtered patches as well as sunny ones. This tendency
matches witli the primary habitat of each species,
mentioned by Tyler et al. (1994) , that explains why B.
polydamas \s a widespread and flexible species, whereas
B. devilliers is sensitive and vtilnerable, dependent on
forested areas.
Flight stratum
In the morning, at Boca de Jarnco both species
mostly fly in the two lower strata (Fig. 6a, b). Battus
dn)illi(ms c\id nc:)t change this strategy during the entire
all day, while B. polydamas cuhensis started to use any
strattim indiscriminately after midday. Krtiskall-Wallis
valties were significant in the morning for both species.
The post hoc test demonstrated differences between
the highest strattim and the lowest one for both species
(p < 0.001), and between the intermediate and the
highest stratum with p < 0.01 for B. devilliers and p
< 0.001 for B. polydamas cuhensis. After midday, KW
vahies did not show any difference among strata used
by either species, although graphically we observed
that B. devilliers keeps similar proportions to those of
the morning (Fig. 6a, b).
At Boca de Canasf, there was no difference in flight
stratum use during the day. Bcdtus devilliers mostly flies
in the lowest strattim, with patches of filtered sun.
On the other hand, B. polydamas cuhensis iWes in all of
the three strata. For B. devilliers the post test display
differences between the lowest and the intermediate
strata with p < 0.01 at both time intervals. Between
the lowest and the highest strata we found the same p
value for the morning, and p < 0.001 for the afternoon.
By contrast, there was no statistical difference in the
tise of flight stratum by B. polydamas cuhensis in this
habitat (Fig. 6c, d).
Flight strata were more indiscriminately used
by both species in the two habitats. The restdts
demonstrate almost no selection for this structtiral
dimension, perhaps because strata are not limiting
42: 5r)-63, 2003 (2010)
61
A
45 T
40-
35-
30-
25-
20-
15-
10-
JC.
Rain Season
Dry Season
B
Figure 4. Relative abundance (individuals/hour) of Battus devilliers (gray) and B. polydamas cubensis (black) In the two seasons
defined in Cuba as Rain (May-October) and Dry (November-April). A: Secondary scrub of Boca de Jaruco. B: Evergreen forest
of Boca de Canasi. The graphic represents the median and the 25% and 75% percentils.
A
B
■ shading
□ filtered sun
□sunny
B. devilliers B. polydamas cubensis
B. devilliers B. polydamas cubensis
c
D
100%
75%
50%
25% ■
0%
■ shading
□ filtered sun
□sunny
B. devilliers B. polydamas cubensis
B. devilliers B. polydamas cubensis
Figure 5. Spacial segregation of Battus devilliers and B. polydamas cubensis in the structural subniche, specifically in the light
intensity used by each one. A and B: Secondary scrub of Boca de Jaruco (morning and afternoon, respectively). C and D:
Evergreen forest of Boca de Canasi (morning and afternoon, respectively). Analysis only for the rainy season. Morning 9;00
am -11 :00 am and afternoon 12:00 pm - 2:00 pm.
resources like flowers and host plant availability or
because of' low ecological relevance for both species.
Similar results were obtained by Fontenla (1989) in a
larger butterfly community.
Temporal segregation
Seasonality. Another relevant divergence in population
ecology is the seasonal pattern of B. devilliers (U = 3.5,
p = 0.0425) by contrast to the continuous dynamics
of the other species (U = 10.5, p = 0.2620) (Fig. 2a, b;
Fig. 4). This strategy and its presence in all sampled
habitats show the greater ecological plasticity of B.
polydamas cubensis. It is relevant that absence of B.
devilliers in the sea grape habitat is recent, as five years
ago it was observed by Nunez and Barro (2003) and
again in lower frequency than B. polydamas cubensis.
Annual fluctuations of popnlations, like those
/. Res.Lepid.
(i2
A
100%
■ 3,0m
75%
□ l,5-3,0m
50%
□ 0-1, 5m
25%
0%
B. devilliers B. polydamas cubensis
B. devilliers B. polydamas cubensis
B. devilliers B. polydamas cubensis
Figure 6. Spacial segregation of Battus devilliers and B. polydamas cubensis in the structural subniche, specifically in the
flight height or stratum used by each. A and B: Secondary scrub of Boca de Jaruco (morning and afternoon, respectively). C:
Evergreen forest of Boca de Canasi (there were not found significant differences in both day-hours). It was analized only rain
season. Morning 9;00 am - 11:00 am and afternoon 12:00 pm -2:00 pm.
Battus polydamas cubensis
Battus devilliers
Figure 7. Daily activity of Battus devilliers (gray line) and B. polydamas cubensis (black line) for the rain season in the two
studied habitats. A: Evergreen forest of Boca de Canasi. B: Secondary scrub of Boca de Jaruco.
obsen'ed in pa.st years in Boca clejarnco by the second
author or changes in habitat structure may influence
population dynamics.
Daily activity. We analyzed the daily activity for each
species and habitat during the rainy season (Fig. 7).
Although no statistical analyses were made with these
data, two different trends were observed in each
population. While the abundance of B. polydamas
cubensis decreases during the day, with a peak of
activity at 10:00 am, abundance of B. devilliers tends
to increase until midday with the maximum number
of individuals at noon. Thus at 12:00 the means of
both pojtulations were similar in the evergreen forest.
At the same time, in the secondary scrub of Boca
de Jaruco, although the mean values of abundance
were so different, the standard tleviations were too
overlapped. This behavior is not surprising since B.
polydamas cubensis flies in sunny patches more than
42: 5f>63, 2003 (2010)
03
B. devilliers that prefers sliade and is less influenced
by high temperature of noon. This mechanism may
affect thermoregulation permitting the species a
longer diurnal flight period.
Battus deiulliers and B. polydamas cubensis present
more selectivity for the dimension sunlight intensity
of tlie structural subniche than for the flight stratum
since the late was more indiscriminate used. Temporal
segregation seems to occur between these species, B.
dniilUersx^ influenced by seasonality wliile B. polydamas
cubensis is present all tlie year.
Acknowledgements
We thank especially the persons who helped with the field
work: Rayner Nunez, Alejandro Garcia, Joel Lastra, Elier Fonseca
and Rene Marzuk. We also are gratel'ul to Ariam jinienez. who was
ol great help w’ith the statistical analysis. Our gratitude to Gilberto
Silva, Rayner Nunez and Oraily Madrtiga tor their helpful conunents
about the manuscript and also our thanks tor the botanical
assistance to Iralis Ventosa and Antonio l.opez. Three anonymous
reviewers contributed to clarifying the submitted manuscri|5t.
Literature cited
Ai.ayon, G. & E. Sor.vNA. 1989. Lista de mariposas diurnas
(Lepidoptera: Rhopalocera) colectadas en la Reserva de la
IMostera Guchillas del Toa (Holgtiin- Guantanamo), Cuba.
Garciana 7: 2-4.
Askkw. R. R. 1980. The butterfly (Lejtidoptera, Rhopalocera) fauna
otthe Cayman Islands. Atoll Research Bulletin 241: 121-138.
Askf.w, R. R. 1988. Butterflies ot Grand Cayman, a dynamic island
fauna. Journal ot Natural Histoiy 22: 87,'i-888.
Borhidi, a. 1996. Phytogeogra]thy and vegetation ecology' of Cuba.
Akademiai Kiado. Budajtest. 923 jtp.
Brow'n, K. S. Jr. 1991. Conservation of Neotrojtical environments:
insects as indicators, |rp. 349-404. In: N. .\1. Collins and J.
A. Thomas (eds.), The conservation of insects and their
habitats. London, Royal Entomological Society Symposium
XV; Academic Press.
Brown, K. S. Jr. & A. V. L. Frkit.as. 2000. Atlantic forest butterflies:
indicators for landscape conservation. Biotropica 32 (4b):
934-956.
Carpenter, G. D. H. & Lewis, C. B. 1943. A collection of Lepidoptera
(Rhopalocera) from the Cayman Islands. Annals of the
Carnegie Museum 9: 371-396.
Ci.ausen, 11. D., H. B. Hoi.beck & J. Rei)der.sen. 2001. Factors
influencing abundance of butterflies and moths in the
uncultivated habitats of an organic farm in Denmark. Biological
Conservation 98: 167-178.
Ft)NTENLA, J. L. 1989. Particion de recursos en una comunidad de
mariposas (Lepidoptera: Rhopalocera). Poeyana 385: 1-26.
Genaro, J. A., A. C. Sanchez. & V. Berovides. 1994. Solapamiento
del nicho ecologico de dos especies del genero Anarlia
(Le|>idoptera: Nymphalidae). Revista Biologi'a 8: 141-144.
Gr.ai’IiPad InStat. 1998. InStat Prism, version 3.01 from GraphPad
Prism (http://w'ww.graphpad.com). (Active in June, 2007)
Knowles, D. O. & D, S. Smi ih. 1995. First records oi Parachomnthus
magdalia (l lesperiidae) from the Bahamas, and extension of
the baliamian range oi Battus dnnlliers (Papilionidae). Journal
of the Lepido|jterist.s Society 49 ( 1 ): 91-94.
Kremen, C. 1992. Assessing the indicator properties of species
assemblages for natural areas monitoring. Ecological
Applications 2: 203-217.
Matsumoto, K. 1989. Effects of aggregation on the survival and
development on different host plants in a papilionid butterdy,
Luehdorfia japonica Leech. Japan Journal of Entomology 57
(4): 853-860.
New, r. R. 1997. Are Lepidoptera an effective “umbrella group”
for biodiversity conservation? Journal of Insect Conservation
I: .5-12.
New, T. R., R. .VI. Pvi.e.J. A. Thom.as, C. D. Thomas, & P. G. Ha.mmond.
1995. Butterfly conservation and management. Annual Review
of Ecology and Systematics 40: 56-83.
Nunez, R. & A. Barro. 2003. Composicion y estructura de dos
comunidadesdemariposiLs (Lepidoptera: Papilionoidea) en Boca
de Canasi, La Ilabana, Cuba. Retista Biologia 17 (1): 8-17.
Racheli, T. & L. P.ARisET. 1992. II genere Battus. Tassonomia e
Storia Naturale. Fragmenta Entomologica 23 (Su|rlemento).
163 pp.
Reader, T. & D. F. Hochuli. 2003. Understanding gregariousness
in a larval Lejridopterau: the role of host |rlant. jrredation and
microclimate. Ecological Entomology' 28: 729-737.
Rivas, L. R. 1964. A reinterpretation ol the concepts “simpalric”
and “allo|jatric”yvith propo,sal of the additional terms “syntopic”
and “allotopic.” Systematic Zoology 13 (1): 42-43.
Sims, S. R. & A. .M. Shapiro. 1983. Pupal dia|5ause in Battus phiknor
(Lejtidoptera: Pa|)ilionidae). Annals of the fintomological
Society' of America 76 (3): 407-412.
Sciiyv.yRTZ, A., F. L. Gonzalez, & R. M. Hender.son. 1987. New
records of butterflies from the West Indies. )ournal of the
Le]3ido|3terist.s' Society 41 (3): 14.5-450.
Stamp, N. E. 1980. Egg deposition patterns in butterflies: yvhy do
some species cluster their eggs rather than de|)osit them singly?
American Naturalist 115 (3): 367-380.
Tvt.ER, H. A., K. S. Brown Jr. & K. H. Wtt.soN. 1994. Syvallowtail
butterflies of the Americas. A study iti biological dynamics,
ecological diversity, biosystematics and consen'ation. Scientific
Publishers. 376 pp.
Youno, a. M. 1972. Mimetic associations in populations of tropical
butterflies. II .Vlimetic interactions of Battus polydamas atid
Battus b(dlus. Biotropica 4(1): 1 7-27.
Youno, A. M. 1973. Notes on the life cycle atid natural history of
Parides areas mylotes (Papilionidae) in a Gosta Rican premontane
wet forest. P.syche 80: 1-21.
/oitrnal of Research on the Lepidoptera
42: 64-73, 2()()3 (2010)
A tale of two species: detritivory, parapatry, and sexual dimorphism in
Lamprospilus collucia and L, orcidia (Lycaenidae: Theclinae: Eumaeini)
Roberi K. Robbins', Annexe Aiello-, Julie Feinstein'\ Amy Berkov'\ Astrid Caldas*, Robert C. Busby"’
AND MaROELO DliARTE"
'DejDartmciit of Entomolog)'. I’O Box 37012, NllB SU)p 105, Smithsonian Institution, Washington, DC 20013-7012, USA
robhinsr@si.edu
-Smithsonian 'IVo]>ical Research Institute, Smithsonian Institution, A|3artado 0843-03092 Balboa, Ancon, Panama
aieUoa@si.edu
■’Department of Biology, City College of New York, City University of New York, Convent Avenue at 138th Street, New York, NY, 10031, USA
jfstein@aninh.org, herhov@.sri. rrny.euny.edu
'De|5ariment of Entomology, PO Box 37012, NHB Stop 105, Smithsonian Institution, Washington, DC 20013-7012 USA
ast rid ra ! das @yah oo.ro m
■’’7 Countryside Way, Andover, MA 01810-6041 USA
rr. busby@romrast. net
'’Coleyao de Lepidoptera, Museu de Zoologia, Lhiiversidade de Silo Paulo, Av. Nazare 481, 04263-000 Sao Paulo, SP Brasil
mduartes@usp.br
Abstract. Lamprosj)ilus rolluria (I lewitson) and L. orridia (Hewitson) are facultatively detritivorous
hairstreaks. Eeinales in nature lay eggs on dead twigs and leaves that are on or near the ground. In
the lab, females oviposit readily on dead leaves. Caterpillars of both species eat dead plant material
in nature and can be reared in the lab to the adult stage on artificial diet to which no plant material
has been added. Lamprospilus rolluria and L. orridia have parapatric distributions; the former species
is endemic to the Transandean Region and the latter to the Amazonian and Atlantic Regions. Both
species have similar male behavior, which is consistent with the hypothesis that their parapatric
distributions are maintained by mating interference. The sexes of L. rolluria and L. orridia have
been incorrectly associated in compendia of Neotropical butterllies and are associated in this paper
by geographic distribution, wing pattern similarity, and rearing data. Although L. rolluria and L.
orridia have been considered to be conspecific, an analysis of geogra|rhical variation supports the
hypothesis that they are distinct biological species.
Key words: Amazonian Region, biogeography, hairstreak systematics, Lecythidaceae, Transandean
Region.
Introduction
Lantpw.spilits collucia (Hewitson) and L. orcidia
(Hewitson) are common and widespread lowland
Neotropical lycaenids (Theclinae: Eumaeini) that
are biologically significant for a ntimber of reasons.
First, L. collucia and T. orcidia are ecologically
tmusual. LaiYal detritivory occurs rarely in the
“Macrolepidoptera” (Powell e! al., 1998; Holm &
W’agner, 2002), but has been reported in Lamprospilus
Geyer (Duarte & Robbins, in press), specifically in
L. collucia and L. orcidia. Second, L. collucia and L.
orcidia are biogeographically significant because they
have been cited as a representative parapatric species
|)air with a Gentral/South American distribution
(Robbins, 2004a). This biogeographic pattern, while
well-known in forest-dwelling aposematic butterfly
laxa (Brown, 1982), has not been doctimented
Rerewed: 15 September 2009
Accepted: 12 October 2009
previously in the Eumaeini. Third, L. collucia and
L. orcidia are of taxonomic interest because they are
widely misidentihed in publications on Neotropical
btitterflies (e.g., Godman & Salvin, 1887; Weeks
1911; Draudt, 1919-1920; Kitye, 1921; Barcant, 1970;
Robbins & Small, 1981; D’Abrera, 1995). Both species
are sexually dimorphic. The males have similar wing
patterns (Figs. 1-4, 13-16, 21-22), forwhich rea.son they
have been considered to be conspecihe (Godman &
Salvin, 1887-1901; Kitye, 1921). Alternately, the female
wing patterns (Figs. 5-12, 17-20, 23) are different
from each other and from those of the males, with
which they have rarely been associated (e.g., Dratidt,
1919-1920).
The purpose of this paper is to address the
ecology, biogeography, and taxonomy of L. collucia
and L. orcidia by answering basic questions abotit
them. Where do females oviposit? What do their
caterpillars eat? When and where do males set tip
mating territories? What are the distributions of L.
collucia and L. orcidia? In which habitats do they occur?
How are T. collucia and L. orcidia distinguished? How
42: 64-73, 2003 (2010)
65
do they vary seasonally and geographically? On what
basis are the sexes associated? What is the available
evidence that they are different biological species?
We add brief notes on nomenclature to confirm that
we are using the correct names. The placement of/..
coUuciam\d L. orcidiam /.rtw/;ros/>//«5Geyer is dealt with
elsewhere (Duarte & Robbins, in press).
Materials and methods
Eggs were obtained in the lab following the
methods detailed in Duarte et al. (2005) . Larvae from
these eggs were reared on artificial diet to which no
vascular plant material was added other than wheat
germ and linseed oil (Duarte et al., 2005). Rearing
methods for immatures collected in nature generally
follow Feinstein et al. (2007). Depositories for
vouchers are noted.
Biogeographic and taxonomic results for L.
collucia are based on 96 males (6 genitalic dissections
from Mexico, Panama, western Ecuador, and eastern
Colombia) and 70 females (6 genitalic dissections
from Mexico, Costa Rica, Panama, and Trinidad).
Analogous results for L. orridia are based on 50 males
(6 genitalic dissections from Ecuador, Peru, and 3 states
in Brazil) and 57 females (6 genitalic dissections from
Peru and Brazil). We map the distributions of each
species by sex because these distributions are evidence
for associating the sexes. Although mitochondrial
“barcodes” are reported for L. collucia and L. orridia
(BOLD website, http://w\\'w.barcodinglife.org/\’iews/
login. php, accessed 26 Aug 2009), the barcodes are
not publically available and the “barcoded specimen”
of L. orcidia is misidentified.
Genitalic terms follow Klots (1970), as modified for
theEumaeini (Robbins, 1991). Wing venation follows
Comstock (1918), and other morphological terms
follow Snodgrass (1935). Geographic distributions
are mapped by gender. Months are abbreviated by
their first three letters in English.
Vouchers for the distribution maps and other
results are deposited in the following collections:
(AA) Annette Aiello Collection, Ancon, Panama;
(BMNH) Natural History Museum, London, UK;
(DZUP) Universidade Federal do Parana, Curitiba,
Parana, Brazil; (MCZ) Museum of Comparative
Zoology, Harvard University, Cambridge MA, USA;
(MECN) Museo Ecuatoriano de Ciencias Naturales,
Quito, Ecuador; (MUSM) Museo de Historia Natural,
Universidad Nacional Mayor de San Marcos, Lima,
Peru; (MZUSP) Museu de Zoologia, Universidade
de Sao Paulo, Brazil; (RCB) Robert C. Busby
Collection, Andover, MA, USA; (USNM) National
Museum of Natural History, Smithsonian Institution,
Washington, DC, USA.
Results
Ecology and biogeography
Oviposition and food “plants.” As part of a study of
plant fungal diseases (Davidson et al., 2000), a “mostly
dead” seedling of Anacardium excelsurn (wild cashew,
Anacardiaceae) was collected by Davidson about 9
Jun 1996 near the Rio Frijoles, Pipeline Road, Canal
Area, Panama (see Ridgely, 1976 for information on
the Pipeline Road locality). A dark reddish brown
larva of L. collucia was found three days later eating
the cotyledon of the dead seedling. Aiello fed the
caterpillar the peduncle of Anacardium occidentale
to complete its development. On 18 Jun 1996, a
dark brown pupa with erect setae on the sides of the
abdomen was formed. The pupa turned black on 1
Jul 1996, and a male of L. collucia emerged later that
day. The reared adult male is deposited in AA (Aiello
lot: 1996-10).
A female of L. collucia was collected by Robbins
and Caldas on 30 Mar 2000 in Ancon, Canal Area,
Panama. She laid 22 eggs over 6 days in the lab on
dead leaves and on the side of a \'ial. Aiello reared
the hatched larvae on artificial diet without any added
plant material. A female emerged on 13 May 2000.
The reared female and her mother are de[)osited in
USNM.
Robbins and Caldas observed a female of L. collucia
ovipositing on a twig on the ground in Ancon on 31
Mar 2000. After caj)ture, the female butterfly laid
another 44 eggs over the next 5 days on dead leaves
in the lab. Aiello reared the resulting caterpillars on
artificial diet without any added plant material, and
three males and one female emerged 14-16 May 2000
(Figs. 1,5). The mother and her reared offspring are
deposited in USNM.
Robbins and Caldas observed a female of L. collucia
ovipositing on a green leaf about 10 cm from the
ground on 2 Apr 2000 (Fig. 9) . She was not captured
and the egg was not collected.
A male of L. orcidia was reared from the fallen
androecia of Esclnoeilera coriacea (Lecythidaceae, plant
vouchers deposited in New York Botanical Garden)
from lowland moist forest 7 km north of Saiil, French
Guiana (3°37’ N, 53° 12’ W). The androecia were
collected by Berkov 21 Oct 1995 in the diy season,
and the adult male of L. orcidia emerged 8 Nov 1995
(voucher deposited in USNM, Fig. 1 6) . Another eight
Lycaenidae that belong to another genus were also
reared from these androecia (Feinstein, Robbins, &
Berkov, in prep.).
/. Res.Lepid.
(i6
Figures 1-12. Lamprospilus coilucia adults. 1. c? ventral, Panama, reared, male sibling of 5. 2. ventral, Panama, form
typically seen in the wet season. 3. (J ventral, Panama, form typically seen in the dry season. 4. dorsal of 1 . 5. $ ventral,
Panama, reared, female sibling of 1 . 6. $ ventral, Panama, form typically seen in the wet season. 7. $ ventral, Nicaragua,
form typically seen in the dry season. 8. $ ventral, no locality, reproduction of figure from the original description. 9. $ ventral,
Panama, female walking on a twig near the ground before laying an egg. 10. $ dorsal, Venezuela. 11. 5 dorsal, Venezuela.
12. $ dorsal, no locality, reproduction of figure from the original description.
A male and two females (Fig. 20) of L. orcidia
(identified as Lycaenidae #2 in Feinstein el at 2007)
were reared from larvae found in fallen androecia of
L('cylhis corrugata (I.ecythidaceae) during the first three
months of 2003 in the wet season at Les Noiiragues
Re.search Station in French Guiana (4°05’ N, 52°4rW;
IK) km south of Gayenne). Although 17 other
Lycaenidae were reared, none belong to Lamprospilus.
Reared adult vouchers are deposited in USNM.
Male behavior. Lamprospilus males display
“territorial” behavior that is similar to that reported in
other eiimaeines (e.g., Alcock & O’Neill, 1986; 1987);
males wait for receptive females to fly through the
territory and “defend” these areas by flying at other
males that enter tlie territory. Males of L. colluda and
L. orcidia set up mating territories in the morning on
hilltops (vouchers below are deposited in USNM,
observations are by Robbins; times are standard time
42: 64-73, 2003 (2010)
67
1 cm
Figures 13-23. Lamprospilus orcidia aduWs. 13. c? ventral, Brazil (Para), presumed holotype. 14. ventral, Peru. 15. (S
ventral, Peru. 16. c? ventral, French Guiana, reared from fallen androecia of Lecythidaceae. 17. $ ventral, Peru, arrow points
to brown scales basal of the postmedian line. 18. $ ventral, Peru. 19. $ ventral, Peru. 20. $ ventral, French Guiana, reared
from fallen androecia of Lecythidaceae. 21. (5* dorsal, Brazil (Para), presumed holotype. 22. (5' dorsal, Peru. 23. $ dorsal,
Peru.
at that locality).
Lamprospihis collucia in Panama, 0730-1045 hours
4 S observed (2 vouchers), 5 Oct 1978, 0730-0745
hours, Canal Area, Paraiso, Cerro Paraiso.
5 S (5 vouchers), 1 Jan 1979, 1000-1030 hours.
Canal Area, Paraiso, Cerro Paraiso.
1(5' (1 voucher), 5 Mar 1979, 1045 hours. Canal
Area, Paraiso, Cerro Paraiso.
>25(5' observed (2 vouchers), 17 May 1979, 0830-
1030 hours, Canal Area, Cerro Calera.
\S (1 voucher), 28 Jiil 1979, 1000 hours, Canal
Ai ea, Paraiso, Cerro Paraiso.
Lamprospihis orcidia in Brazil, 0904-0920 hours
68
/. Res.Lepid.
1(5' (1 v(3ucher), 18 Mar 1991, 0904 hours, Sao
Paulo, 17 km west of Teodoro Sampaio.
1(5 (1 voucher), 24 May 1998, 0920 hours, Rio de
Janeiro, Iguaba Grande.
Habitat. Lmnprospilus collucia and L. orcidia occur
in wet and dry lowland forest, ranging from “relatively
virgin” forest (e.g., Parque Manu, Peru) to mature
secondary forest (e.g., Gamboa, Canal Ai'ea, Panama)
to patchy disturbed forest in urban areas (e.g.. Ancon,
Canal Area, Panama) . We have seen no specimens of
L. coZ/Mcm collected above 1,000 m elevation in Central
America, but in western Ecuador they have been
found in wet forest at 1,500 m and on a ridge with dry
forest at 2,100 m where there is often a strong westerly
wind. Most individuals of L. orcidia m'e recorded from
lowland forest, but some have been recorded from
1,000 m elevation in southern Brazil. Adults of L.
collucia and L. orcidia are most abundant at the end
of the dry season and beginning of the wet season in
Panama and southeastern Peru, a pattern typical of the
I Mniprospilus ^eciion (Duarte & Robbins, in press).
Distribution. Males of L. collucia are recorded from
northeastern Mexico to Ecuador west of the Andes
and to Trinidad, northern Venezuela, and central
Colombia east of the Andes (circles in Fig. 24) while
males of L. orcidia are known east of the Andes from
central Venezuela to southern Brazil and Bolivia
(squares in Fig. 24). Males of L. colliiciamd L. orcidia
are not sympatric.
Females of L. collucia'dre recorded from northeastern
Mexico to the northwestern tip of Peru west of the
Andes and to Trinidad, and central Venezuela east of
the Andes (circles in Fig. 25) while females of L. orcidia
are known from east of the Andes from the Guianas
and southern Venezuela and southern Colombia to
southern Brazil (squares in Fig. 25). Females of L.
collucia 'And L. orcidia Ate not sympatric.
There is one ntale of L. orcidia and one female of
L. collucia from the Rio Suapure, Venezuela (MCZ),
a tributary of the Rio Orinoco in central Venezuela
(Bolivar state) that flows through llanos (savannah)
and Amazonian forest habitats (arrows in Figs. 24-25) .
These specimens lack collection date or more specific
locality data. Weeks (1911) noted only that they were
collected in “the neighborhood of the Suapure River
in Venezuela.” It is unknown if both were collected at
the same locality along the Rio Suapure, but if so, it is
the only locality where both species have been found.
The female from Rio Suapure was listed and illustrated
as Theda madie Weeks, but the male was apparently
misidentilied as Theda xenata (a misspelling of Theda
xeneta Hewitson, see taxonomy section below) (Weeks,
1911). There are no males of Calycopis xeneta from the
Rio Suapure in the Weeks Collection (MCZ).
Taxonomy
Distinguishing male characters. Location of the
charcoal-black patch on the ventral forewing is the
most consistent and easy way to distinguish males
of L. collucia and L. orcidia (Figs. 1-3, 13-16). In L.
collucia, this patch is distal of the postmedian line
whereas in L. orcidia, it is distal and basal with the basal
part darker in some individuals. We have not seen a
male with an intermediate wing pattern. Godman
and Salvin (1887-1901) and Kaye (1921) apparently
considered this difference to be intraspecific variation,
but Comstock and Huntington (1962) noted that the
two wing patterns were distinct.
The ventral wing patterns of these males are similar
to those of other species with charcoal-black patches.
Males of some other Lamprospilus species, such as L.
coelicolor (Butler & Druce) and L. aunus (Cramer),
are easily distinguished by the better defined and
more triangular shape of the dark brown patch on
the ventral forewing (Fig. 42 in Duarte 8c Robbins,
in press). Males of Calycopis xeneta (Hewitson) have a
brown spot in ventral hindwing cell Cip-2Ajust distal
of the postmedian line (Fig. 58 in Duarte & Robbins,
in press) that is lacking in Lamprospilus.
Variation of male wing pattern. Wing pattern
variation in male L. collucia is most evident on the
ventral wings (Figs. 1-3). The width and exact shape
of the postmedian line on both wings is perhaps the
most variable element. The darkness and extent of
the charcoal-black patches is also variable. Those
individuals with a ventral wing pattern which is a bit
lighter than average (Fig. 3) are more prevalent in the
dry season, but we find no evidence for geographical
variation.
Wing pattern variation in male L. orcidia is also
most evident on the ventral wings (Figs. 13-16). Again,
the shape of the postmediaii line and the extent
and darkness of the charcoal-black patches on both
wings are the most variable elements. We do not have
sufficient data to assess seasonal wing pattern variation,
but find no evidence of geographical variation.
Distinguishing female characters. Shape and color
of the ventral forewing postmedian line is the most
consistent way to distinguish females of L. collucia and
L. orcidia. This line is relatively thick and reddisli to
dark maroon in L. collucia (Figs. 5-9) and is a relatively
thin black and white line with diffuse liglit brown
scaling basally in L. orcidia (Figs. 17-20, arrow points
to brown scaling).
The ventral wing pattern of female L. collucia could
be confused with that of female L. lanckena (Schaus),
42: 64-73, 2()()3 (2010)
69
Figures 24-25. Distribution of L. coHucia (circles) and L. orcidia (squares). Arrows point to possible sympatry on the Rio Suapure
(Venezuela). The shaded area is an extremely close approximation to the Transandean Region of Brown (1982: 456); this area
of endemism was proposed without exact borders. 24. Males. 25. Females.
but the later has the ventral forevving postmedian
line of L. collucia in cell Car,-2A and more rounded
hinchvings. The black and white forewing postmedian
line with brown basal scaling is the best way to
distinguish L. orcidia from other hairstreak species,
hut this character is sometimes inconspicuous (Fig.
19). Even with genitalic dissection, some females of
L. orcidia may he difficult to identify definitively.
Variation of female wing pattern. Wing pattern
in female L. collucia is quite variable. Dorsal ground
color has variable amounts of blue scaling (Figs. 10-
11), which varies in hue from shining blue to chalky
gray. The ventral brownish-black patch of scales distal
of the postmeclian line varies from absent (Fig. 7)
to conspicuous (Figs. 5-6). The color of the ventral
postmedian line varies from reddish to dark maroon,
but the thick forewing line from the costa to vein Cu,,
is a constant feature. As in the male, intlividuals with
a lighter ventral wing pattern (Fig. 7) tend to be most
frequent in the dry season.
Wing pattern variation in female L. orcidia is
similarly variable. Dorsal ground color varies from
blue to chalky gray. The ventral wing pattern is rather
“non-descript”, but the black and white postmedian
line with basal brownish scaling appears to be constant,
even if its expression is variable (Figs. 17-20).
Male genitalia and their variation. The male
genitalia of L. collucia and L. orcidia are typical of
Lamprospilus (Duarte & Robbins, in press) with a single
medium sized tooth on each gnathos arm (arrow
in Fig. 26). The only evident genitalic difference
between the two species is that the penis of L. orcidia
consistently has a small second cornutus (arrow in Fig.
27) while that of L. collucia may or may not (Fig. 26)
have the second cornutus. Otherwise, the illustrated
differences in the saccus, penis, and valvae (Figs. 26-
27) fall within the range of intraspecific variation.
Female genitalia and their variation. The female
genitalia of/., collucia me typical of Lamprospilus Wnh
“fan-shaped” signa (Figs. 28-29) and an inwardly
curved sclerotized ridge on the distal end of the 8th
abdominal tergum (illustrated in Duarte & Robbins,
in press). The shape of the ductus bursae, especially
the posterior end, varies intras(}ecifically, but does not
distinguish the species. The signa of the two species
differ in the sample (Figs. 28-29), but are structurally
quite variable, for which reason we suspect that this
difference might not be confirmed by a larger sample
size.
Nomenclature. Theda collucia Hewitson was
70
/. lies.Lepid.
Figures 26-27. Male genitalia, ventral aspect (left), lateral aspect (right), penis in lateral aspect (bottom). 26. L collucia,
Panama (Canal Area), arrow points to single “tooth” on the gnathos. 27. L. orcidia, Brazil (Minas Gerais), arrow points to small
second terminal cornutus. Scale 1 mm.
described from at least one pair in the Hewitson
Collection (now in BMNH), but only the female was
illustrated (Figs. 8, 12). No type locality was given.
Johnson (1993: 22) designated a female lectotype
(B.M. Type Rh 1010) from Esp. Santo (presumably
Espirito Santo, Brazil) that fits the original illustration
very well even though it is missing most of its forewings.
However, there was no type locality in the original
description, and a photograph of the lectotype and
its labels from the 1970s shows that this specimen
lacked a locality label at that time. Johnson (1993:
22) did not list Brazil as part of the South American
distribution of collucia, so his “Esp. Santo” citation is
difficult to interpret. Primary types of Theda collucia's
Junior synonyms have been examined: madie Weeks
($, MCZ), am/Wradc Schaus ($, USNM, the original
description erroneously listed the BMNH), iodiniis
Kaye {S, BMNH), Dyar ($, USNM), and shueyi
Johnson ((5',AMNH).
lliecla orcidia Hewitson was described from at least
one male in the H. W. Bates collection (now in BMNH)
from the Amazon. There is one male in the BMNH
that fits this description (Figs. 13, 21, B.M. Type Rh
872) and is presumed to be a liolotype. Illustrations
of the holotypes (by original designation) of junior
.synonyms to/i'cm'w Johnson (AMNH), Johnson
& Kroenlein (BMNH), .vi/uw Austin & K. Johnson
(I)ZUP), ron doni a Xmiin & K. Johnson (DZUP),
ofaarra Austin & K. Johnson (DZUP), j&cr/ifexa Austin Sc
K. Johnson (DZUP) , and purpura Kiisiin Sc K. Johnson
(DZUP) can be found in the original descriptions
(Johnson, 1993; Johnson & Ki'oenleiii, 1993; Austin
& Johnson, 1997).
The wing pattern of female L. orcidia is non¬
descript, as noted. Perhaps for that reason, a female
of L. orcidia was included in the type series of the
unrelated Theda ceromiaHeMntson. However, Johnson
and Kroenlein (1993:4) designated another specimen
as the lectotype, which is the reason that Theda ceromia
is now placed in Ziegleria (Robbins, 2004b; Duarte Sc
Robbins, in press).
Discussion
Detritivory, Females of L. collucia have been
recorded in nature ovipositing on dead twigs on the
ground and on a leaf near the ground. In the lab,
females oviposit readily on dead leaves. Caterpillars
of L. collucia and L. orcidia in nature have been found
eating a “nearly” dead seedling and the androecia
of Lecythidaceae flowers on the ground. In the
lab, larvae complete development on live and dead
organic matter. Although many butterflies, including
Lycaenidae, can be reared on an artificial diet to
which dried, ground leaves of the food plant are
added (Morton, 1981; Mark, 1993; 1995), larvae of
42: 64-73, 2003 (2010)
71
Figures 28"29. Female genitalia, dorsal (left) and lateral aspects. 28. L. collucia, Panama (Canal Area). 29. L. orcidia, Peru
(Madre de Dios). Scale 1 mm.
L. collucia and L. orcicUa readily ate and completed
development on an agar-ba.sed artificial diet without
the addition of'leaves. These results are very similar to
those reported for Calycopis (S. Johnson, 1985; Rohhins
et al., 199(i; Duarte et ah, 2005), and are consistent
with the hypothesis that L. collucia and L. orcidia are
facultative detritivores.
Different kinds of detritus provide different kinds
of nutrition for a caterpillar. A preliminaiy analysis
of some Lecythidaceae androecia showed that they
have higher sugar and phosphorus content than “leaf
litter” (nitrogen levels were variable), but a lower
content of other minerals and fiber (A. Wliigham pers.
comm.). Detritivores may also eat micro-organisms
living on detritus (Findlay & Tenore, 1982; Hohn 8c
Wagner, 2002) , but to date, the ntitrition that lycaenid
detritivorous caterpillars derive from different food
objects is an unexplored subject.
Maximal adult abundance of L. collucia and L.
orcidia at the end of the dry season and beginning of
the wet season suggests that larvae find more suitable
food or suffer lower mortality during the dry season.
Many trees are deciduous during the dry season, hut
whether fungi and other caterpillar pathogens and
predators are less abundant at that time is an open
question.
Parapatry. Brown (1982) partitioned the
distribution of Neotropical forest butterflies into
four slightly overlajjping “fuzzy-edged” biogeographic
regions of endemism, three of which (Transandcan,
Amazonian, and Atlantic) consist primarily of
areas under 1,500 m elevation. The biogeographic
distribution of L. collucia is a “textbook” example of
Brown’s Transandean Region; this species occupies
virtually the entire Transandean Region (shaded
part of Figs. 24-25). The distribution of L. orcidia is
a combination of Brown’s Amazonian and Atlantic
Regions. So far as we are aware, this is the first time
that a clear-cut Transandean/Amazonian parapatric
distribution has been documented in the Eumaeini.
In most other potential cases, such as Lamasina drauclti
(Lathy) and L. ganimedes (Cramer) (Robbins & Lamas,
72
J. Res.Lepid.
2008), species are not sufficiently well-represented
in ninsenin collections to determine whether
distiibntions are allopatric or parapatric.
The parapatric distributions of L. collucia and L.
orcidia (Figs. 24-25) are unlikely to be maintained by
competition for larval food; it is difficult to visualize
the dead organic matter that the caterpillars eat as
a limiting resource. However, males of both species
set up mating territories in the morning on hilltops
and occur in similar habitats. These findings suggest
the testable hypothesis that mating interference is
responsible for maintaining parapatry between the
two species.
Associating males and females. The evidence that
males and females of L. coZ/wr/a are correctly associated
is that the distribution of each sex is almost identical
(Figs. 24-25), both sexes have a dark brown patch on
the ventral forewing distal of the postniedian line
(Figs. 1-3, 5-9) , and both sexes have been reared from
eggs laid by the same mother (Figs. 1,5). The evidence
that the male and female of L. orcidia are the same
species is that the distribution of males and females is
almost identical (Figs. 24-25), both sexes have darker
scales (albeit, much reduced in the female) basal of
the ventral forewing postniedian line (Figs. 13-20),
and both have been reared from fallen flowers of
Lecythidaceae (Figs. 16, 20; no other Lamprospilus
species were reared from these flowers). Finally, no
other “unassociated” Lamprospilus male or female has
the same distribution as either species.
Biological species. With the possible exception
of the old Rio Siiapure specimens mentioned above
from Weeks ( 1 9 1 1 ) , the distributions of L. collucia and
L. orcidia 'Ave parapatric (Fig. 24-25). Distinguishing
characters are consistent throughout the range of
each species and do not vary in the areas where the
distributions meet. This evidence is consistent with
the hypothesis that the two taxa do not interbreed.
Lamprospilus collucia and L. orcidia are likely to
be phylogenetic sisters. In a phylogenetic analysis
intended to determine relations among the genera
of the '‘'Lamprospilus Section” (Duarte & Robbins,
in press), the morphological character coding for
L. collucia and L. orcidia was identical. However, the
coding was also very similar to that for L. coelicolor And L.
aivnus. For this reason, an analysis of phylogenetically
informative characters among Lamprospilus species is
needed to test whether L. collucia and L. orcidia are
indeed sister species.
Acknowledgements
We are grateful to Karie Darrow for preparing the plates of
adults, to Vichai Malikul for preparing the genitalic illustrations,
to Brian Harris for help with technical aspects of this project, to
Gerardo Lamas for providing data on L. collucia in Peru, and to
Amie Wliigham for allowing us to cite lier preliminary iinpublislied
information. For supporting travel by both Duarte and Robbins and
for substantial funds, we thank Fundagao de Amparo a Pe.squisa do
Estado de Sao Paulo/FAPESP (as part of the project “Systematics,
Bionomy, and Evolution of Neotropical Lepidoptera”; process
numbers 02/ 1 3898-0 and 03/ 1 3985-3) and Pro-Reitoria de Pesqitisa
da Universidade de Sao Paulo/USP/Projeto 1. For excellent
suggestions on the manuscript, we thank Paul Goldstein, Andre
Freitas, and Rudi Mattoni.
Literature cited
AlcockJ. & K. M. O’Neu.l. 1986. Density-dependent mating
tactics in the gray hairstreak, Strymon melinus (Lepidoptera,
Lycaenidae). Journal of Zoology 209: 105-113.
Aixock, J. & K. M. O’Neill. 1987. Territory preferences and
intensity of competition in the grey hairstreak Strymon melinus
(Lepidoptera: Lycaenidae) and the tarantula hawk wasp
Hemipepsis usiulata (Hymenoptera: Pompilidae). American
Midland Naturalist 11: 120-138.
Au.stin, G. T. & K.Jt)HN,soN. 1997. Theclinae of Rondonia, Brazil:
Gigantorubra and Anguloph, with descriptions of new species
(Lepidoptera: Lycaenidae). Insecta Mundi 1 1(3/4): 255-272.
Barcant, M. 1970. Butterflies of Trinidad and Tobago. London,
Collins. 314 pp., 28 pis.
Brown, K. S. 1982. Historical and ecological factors in the
biogeography of aposematic neotropical butterflies. American
Zoologist 22(2): 453-471.
Comstoc:k, J. H. 1918. The wings of insects. The Comstock
Publishing Company, Ithaca. 430 pp.
CoM.STOCK, W. P. & E. 1. Huntinciton. 1962. An annotated list of
the Lycaenidae (Lepidoptera: Rhopalocera) of the Western
Hemisphere. Journal of the New York Entomological Society
70: 39 46.
D’Abrer,\, B. L. 1995. Butterflies of the Neotropical region. Part
VII. Lycaenidae. Black Rock, Hill House, i-xi + 1098-1270
pp.
D.AVID.SON, J. M., S. A. Rf.hner, M. Santana & E. Lasso. 2000. First
report of Phytnphthora heveae and Pythiuni spp. on tropical tree
seedlings in Panama. Plant Disease 84(6): 706.
Divuidt, M. 1919-1920. Thedini F., pp. 744-812, In: A. Seitz (Ed.).
Die Gross-Schmetterlinge der Erde, vol. 5. Die amerikanischen
Tagfalter. Stuttgart, Alfred Kernen.
Duarte, M. & R. K. Robbins. In press. Description and phylogenetic
analysis of the Calycopidina (Lycaenidae, Theclinae, Eiimaeini):
a subtribe of detritivores. Revista Brasileira de Entomologia.
Duarte, M., R. K. Robbins, & O. H. H. Mielke. 2005. Immature
stages of Calycopis caulonia (Hewitson, 1877) (Lepidoptera,
Lycaenidae, Theclinae, Eumaeini), with notes on rearing
detritivorous liairstreaks on artificial diet. Zootaxa 1063:
1-31.
Eliot, J. N. 1973. The higher classification of the Lycaenidae
(Lepidoptera): a tentative arrangement. Bulletin of the British
Museum (Natural History) Entomology 28(6): 371-505.
Feinstein, J., S. Mori, & A. Berkov. 2007. Saproflorivory: a diverse
insect community in fallen flowers of Lecythidaceae in French
Guiana. Biotropica 39(4): 549-554.
Findiay, S. & K. Tenoril 1982. Nitrogen source for a detritivore:
detritus substrate versus associated microbes. Science 218:
371-37.3.
Goi)m.-\n, F. D. & O. Salvin. 1887-1901. Biologia Centrali-Americana.
Insecta. Lepidoptera-Rhopalocera. Fam. Lycaenidae. 2:
1-112.
Hohn, F. M. & D. L. Waoner. 2002. Larval substrates of herminiine
42: 64-73, 2003 (2010)
73
noctuids (Lepidoptcra): niacrodecoiiiposers of teni|)erate leal
litter. Eiivironnieiital Eiitoniolog)' 29: 207-212.
Johnson, K. 1993. Neotropical hairstreak butterflies: new sister
genera of the “Elerlroslrymon/ Angulopis" grade of Enniaeini
(Lepidoptera, Lycaenidae, Theclinae) . Reports of'the Museum
of Natural History. University of Wisconsin (Stevens Point)
32: 1-76.
Johnson, K. 8c K. R. Krof.ni.kin. 1993. Revision of Angiilopis
(l.epidoptera, Lycaenidae, Theclinae). Reports of the Museum
of Natural History. University of Wisconsin (Stevens Point)
33: 1-38.
JoHN.soN, S. A. 1985. Uultnringadetritivore, Calycopis isobeon (Butler
& Druce). News of the Lepido|>terists’ Society 3: 41-42.
Kaye, W. J. 1921. A catalogue of the Trinidad Lepido]3tcra
Rhopalocera. Memoirs of the Department of Agriculture of
Trinidad and Tobago 2: i-xii, 13-163.
Kiors, A. B. 1970. l.epidoptera, pp. 1 15-130, In: S.L. Tuxen (Ed.),
Taxonomist’s glossary of genitalia in insects. Munksgaard,
(Copenhagen.
Lamas, G., R. K. Roisisins & D. J. Harvey. 1997. Mariposas del
alto Rio Napo, Loreto, Peru (Lepido|Ytera: Pajtilionoidea y
Hesperioidea). Revista Peruana de Entomologfa 39: 63-74.
Mark, H. -G. 1993. Erste .Vlitteilung fiber Tagfalter- und
Zyganenzuchten mit semisynthetischem Kunstfutter.
Nachrichten des Entomologischen Vereins Ajtollo, N.F., 14:
27.5-280.
Mark, H. -G. 1995. Tagfalter- und Zygaenenzuchten mit
semisynthetischem Kunstfutter, zweite Mitteilung: Lepidojttera,
Lycaenidae. Nachrichten des Entomologischen Vereins Apollo,
N.F., 16: 263-274.
Morion, R. S. 1981. Rearing butterflies on artificial diet. Journal
of Research on the Lepidoptera 18: 221-227.
Powiti.i , J., G. Muter & B. D. Farrei i.. 1998. Evolution of larval
food preference in Lepidojttera, pp. 403-422, In: N. P.
Kristensen (Ed.). Band/ Volume IV Aithropoda: Insecta.
Lepidoptera, Moths and Butterflies: Evolution, .Systematics, and
Biogeography. In: M. Fischer (Ed.). Handhuch der Zoologie.
Handbook of Zoology. Berlin, Walter de Gruyter.
Rinor.i.v, R. S. 1976. A guide to the birds of Panama. I’rinceton
Univ. Press, Princeton, NJ. 394 i5|t.
RoBiiiNS, R. K. 1991. Evolution, comparative morphology, and
identification of the eumaeine butterflv genus Rckoa Kaye
(Lycaenidae: Theclinae). Smithsonian Gontribution to Zoology
498, 64 pp.
RoiiiiiNS, R. K. 2004a. Introduction to the checklist of Eumaeini
(Lycaenidae), pp. xxiv-xxx, in: Lamas, G. (Ed.), Ghecklist: Part
4A. Hesperioidea - Papilionoidea. In: Heppner, J. B. (Ed.),
Atlas of Neotropical Lepidoptera. Volume .5A. (ktinesville.
Association fbrTro|)ical Lepido|)tera; Scientific Publishers.
Robbins, R. K. 20()4b. Lycaenidae. Theclinae. Tribe Eumaeini, jtp.
1 18-137, In: Lamas, (k (Ed.), Ghecklist: Part 4A. Hesperioidea
-Papilionoidea. In: Heppner, J. B. (Ed.), Atlas of Neotropical
l.epidoptera. Volume .5A. Gaine.sville, A.ssociation lor Tropical
LepidojYtera; Scientific Publishers.
Robbins, R. K. & Ck Lymas. 2008. Nomenclature, variation, and the
biological species concept in Lnmasina (Lycaenidae: Theclinae:
Eumaeini). Revista Brasileira de Zoologia 25(1): 1 16-127.
Robbins, R. K., G. L.ymas, O. H. H. Miei.ke, D. J. Harvey & M.
G.\.s.\gr.\ni)E. 1996. Taxonomic composition and ecological
structtire of the species-rich butterflv community at Pakitza.
Parque National del Mann, Peru, |)|). 217-252, In: Mann:
fhe biodiversity of Southeastern Peru (D. E. W'ilson and A.
Sandoval, (Eds.). Smithsonian Institution Press, Washington
DG. 679 ]tp.
Robbins, R. K. & G. B. Smai.i,. 1981. Wind dispersal of Panamanian
hairstreak butterllies (Lejtidoptera: Lycaenidae) and its
evolutionary significance. Biotropica: 13(4): 308-315.
SNonoR.\.ss, R. E. 1935. Principles of insect inoiphologY’. McGraw-
Hill Book Go., New York, 667 jtp.
Weeks, A. G. 1911. Illustrations of diurnal l.epidoptera. With
flescri]3tions. Boston, The L niversity Press. 2: xvi + 37 p.
Journal oj Research on the Lepidoptera
42: 74-78, 2003 (2010)
Ag-gregated oviposition in Actinote pellmea pellenea Hubner (Lepidoptera?
Nymphalidae)
Ronaldo Bastos Francini' and Andre Victor Lucci Freitas-*
'Universidade Catolica de Santos, Campus D. Idiliojose Soares, Av. Conselheiro Nebias, 300, 11015-200, Santos, Sao Paulo, Brazil.
fra ncini@unisan las. br
“Departamento de Bioiogia Animal and Museu de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109,
13083-970, Campinas, Sao Paulo, Brazil.
bak u@ii nka mp. br
Abstract. The oviposition pattern of Actinote pellenea pellenea on Austroeiipatorium inulaefolium was
investigated in two coastal sites in SE Brazil to test if there is any pattern of preference for host plant
traits. At both sites, host plants were marked and measured for height, distance of the nearest plant,
number of leaves with A. p. pellenea immatiires (eggs and first instar larvae), number of groups of
immatures, and total number of eggs per plant. An apparency index was calculated relating plant size
to distance from its three nearest conspecific neighbours. Total leaf area, orientation and inclination
were recorded for each leaf with a group of immatures. There was no significant correlation between
the number of ovipositions on each plant and habitat and plant characteristics as plant height
and apparency index. The number and density of eggs by oviposition was not correlated with leaf
characters as area, orientation or inclination. At botli sites clusters of immatures showed a grouped
distribution, with some plants having more immatures than predicted by chance. In the only case
of a double oviposition on the same leaf, the later cluster was significantly smaller. The results show
that distribution of eggs - reflecting female choice - was not related w'ith the above measured plant
and leaf traits. However, the results do suggest that females probably choose plants where immatures
are already present, resulting in the observed grouping pattern.
Keywords: Actinote, Austroeupatorium, host plant selection, oviposition.
Introduction
For most holometabolous insects in general, and
with herbivores in particular, adults are more mobile
than immatures, with the decisions of ovipositing
females often critical for the fitness of the offspring
(Doak et at, 2006). For most herbivorous insects,
host plant acceptability and quality vary strongly
among plant species, populations and individuals
and even among different plant parts (Strong et al,
1984; Price, 1997; Kerpel et at, 2006). The ability
of females to choose among different liosts or host
parts has important consequences on their offspring’s
performance, with the females usually using plant
cues to identify the most suitable food resource.
Many different cues are used by females during
the oviposition process. These include secondary
compounds, visual signals (plant and leaf shape),
presence of natural enemies or mutualists, presence of
conspecific immatures, microclimate (Raiisher, 1978;
Williams & Gilbert, 1981; Freitas & Oliveira, 1996)
H’.orrespon den ce a u thor
Received: 22 June 2009
Accepted: 25 June 2009
and plant vigour (Price, 1991, 1997). Furthermore,
ovipositing females can also respond to indirect cues
such as leaf age and size, internode length (Price et al,
1987; Freitas et al, 1999), plant apparency, grouping
and position of host plants across the landscape
(Feeiiy, 1976; Courtney & Courtney, 1982; Mackay &
Singer, 1982).
The Neotropical genus Actinote Hiibner, [1819]
(Nymphalidae: Helicoiiiinae: Acraeiiii) has 31
described species distributed through Central and
South America, reaching maximum diversity in the
montane regions in the Andes and Southern Brazil
(Francini et al, 2004; Lamas, 2004; Paluch, 2006;
Paluch et al, 2006; Silva-Brandao et al, 2008). Al
known species feed on Asteraceae and are gregarious
during all stages (Francini, 1989, 1992; Paluch et al,
2005; Freitas et al, 2009).
The widespread Actinote pellenea Hiibner, [1821]
has 17 recognized subspecies distributed across all
South Aiierica from Colombia to Northern Argentina
found over a wide variety of secondary and open
habitats (Francini, 1989, 1992; Paluch, 2006). In
coastal Southern Brazil, A. pellenea pellenea Hubner,
[1821] is very common with four or five generations
per year. Here larvae of A. p. pellenea feed on three
species of Asteraceae: the vines Mikania micrantha
and Mikania cordifolia, and the shrub Austroeupatorium
42: 74-78, 2003 (2010)
75
inulaefolium (Francini, 1989, 1992) (Fig. 1).
The following study describes the pattern of
oviposition distribution of A. p. pellenea on patches
of A. inulaefolium, and discusses the factors that may
explain the observed patterns.
Methods
Study sites
The study was carried out at two coastal sites of Sao
Paulo State, Southern Brazil: 1) Xixova-Japui State
Park (JAPUI), Sao Vicente, Sao Paulo (23°59’ S, 46°23’
W), in July and 2"‘‘ , 1991, and 2) the valley of the
Cubatao river, (VRCUB), Cubatao, Sao Paulo (23°53’
S, 46°27’ W) during November 12, 1992. Both sites
are covered by lowland subtropical forest (Ururahy el
ai, 1984). Annual rainfall reaches 2500 mm and the
average annual temperature is 21°C (Setzer, 1949;
Nimer, 1989). Field work was conducted along open
trail edges and in early succession stages secondary
vegetation.
Sampling procedures
At each site all individuals of A. inulaefolium j^resent
along a previously defined linear transect of 200
m were sampled, including all plants to a 5 meters
distance on both sides of the transect, including all
nearby plants in the area. Immatures of A. p. pellenea
of each host plant were recorded and all ovipositions
were collected for laboratory work. Each individual
plant was tagged and recorded for height (five
classes of 100 cm), distance of the nearest plant (in
meters), orientation in relation to the nearest plant
(in degrees), number of leaves with immatures, total
number of immature groups and total number of
immatures. For each leaf with immatures, the area,
inclination (to the horizontal), orientation (in degrees
to the central axis of the plant), amount of herbivory
and number of immatures per group were recorded.
An “apparency index” (AI, follow'ing Feeny, 1976) was
calculated for each individual plant, as: AI = [(Ho -
Ha + DA) + (Ho - Hb + DB) + (Ho - He + DC)] / 3;
where Ho = plant height, Ha, Hb, He = height of the
nearest three plants of the species, and DA, DB, DC
= distance of the nearest three plants of the same
species present along the linear transect. This index
is lowest (including negative values) when the distance
between a pair of plants is less than the lower plant of
the pair. The index increases with increasing distance
between the two plants. To determine the distribution
of the plants, the study area was included in a 108
m- rectangle, and this was subdivided in 27 squared
sectors of 2x2 m (three rows and nine columns). The
distribution pattern of plants was determined using
the index of dispersion (Ludwig & Reynolds, 1988)
with values < I indicating a uniform distribution, = 1 a
random distribution and > 1 a grouped distribution.
Inclination and orientation of each leaf was
estimated with compass and protractor with a
precision of 1°. Each oviposition was assigned to one
of three developmental stages based on predominant
egg colour following Erancini (1989), where Y =
yellow (0-1 day after oviposition), O = orange (1-3
days after oviposition), R = red (more than 3 days
after oviposition), B = black (1 or two days before
eclosion). First instars were also considered in the
present study, since larvae usually remain, together
with their empty egg shells, on the same leaf for the
first days following eclosion.
All measured leaves were scored into four
categories of herbivore damage: (0) 0%; (1) up to
10%; (2) 11% to 25%; (3) 26%\o 50%; (4) more than
51%. Since the leaves of A. inulaefolium are nearly
rhombus-shaped, leaf area (in cm-) was estimated
using the formula (L*W)/2, where L = length and
W = width.
Egg density for each oviposition was estimated from
the average of hve independent counts of eggs over
different sections of each oviposition event, giving
the number of eggs per cm'*^. The number of eggs in
each oviposition was estimated as the product of the
average density by the area of the oviposition.
Results
Host plant density. At JAPUI 23 |)lants of A.
inulaefolium \were inspected showing a density of 0.21
plants/m‘‘^ with a non-random distribution (Poi.s.son
test, x- = 4.2031, DF = 2, p < 0.05). The dispersion index
was 1.331, indicating that the plants are grouped. At
VRCUB 1 1 plants were inspected with a density of 0. 10
plants/m- with a random distribution (Poisson test;
y- = 0.7365, DF = 1, p > 0.70) and dispersion index of
0.8042, which indicated a homogenous distribution.
Host plant height. AtJAPUl A. inulaefolium height
ranged from 100 to 500 cm ( J - 213.0 cm, SD = 109.98,
n = 13), significantly lower than from VRCUB, that
ranged from 300 to 700 cm ( x = 472.7 cm, SD = 1 10.37,
n = 1 1 ) (t test = -6.4339, DF = 32, p < 0.001 ) . At JAPUl
the AI (apparency index) ranged from -100 to 1760
while at VRCUB the range was greater, from 800 to
3040, indicating that plants with high apparency co¬
occur with plants with low apparency. There was no
correlation between the AI and plant height at either
site (Spearman, r = 0.0689 in JAPUI, t = 0.3163, DF =
21, p > 0.75, and r = 0.1908 in VRCUB, t = 0.5831, DF
76
J. Res.Lepid.
= 9, P>().57).
Distribution of immatures. AtJAPUI 43 groups of
ininiatures (eggs or first iiistar larvae) were recorded
on 42 leaves of all plants with the number of groups
per plant ranging from 0 to 9 {X= 1.9 ovipositioiis/
plant, SD = 2.40, n = 23) and a dispersion index
of 3.078. At VRCUB 41 groups of immatures were
recorded on 41 leaves of all plants, with a range from
0 and to 1 1 (X = 3.7 ovipositioiis/ plant, SD = 12.82,
n = 23) and a dispersion index of 3.439. The values
of the dispersion indexes indicate that distribution of
immatures on the plants of both sites was grouped.
Ovipositions were recorded on leaves ranging from 15
to 450 cm above ground atJAPUI and from 130 to 500
cm at VRCUB. When grouped into intervals of 100
cm, the data showed a concentration of 27 ovipositions
within the interval 101 - 200 cm in JAPUI, and of 16
ovipositions in the interval 201 - 300 cm in VRCUB.
A double oviposition on the same leaf was observed
once during the study.
Oviposited leaves. The average surface area of
leaves that showed oviposition atJAPUI ( X = 2553.21
mm2, SD =1929.36, n = 58) was significantly lower than
at VRCUB (x = 4549.3 mm2, SD = 2653.82, n = 25)
(t test = -3.8755, p < 0.0002, DF = 81). There was no
preferential orientation of oviposited leaves at either
site (JAPUI X-' = 2.00, p = 0.57, DF = 3; VRCUB X’ =
3.37, p = 0.34, DF = 3) . With respect to leaf inclination,
most oviposited leaves were between 10° and 20°
from the horizon at both sites. Considering only
leaves showing oviposition, most were leaves with low
herbivoiy damage (0 to 10% herbivoiy) at both JAPUI
(67.6%) and VRCUB (92.6%). However, because
the patterns of leaf orientation and inclination, and
herbivory, were not evaluated for all plants, these data
are not useful in sliowing tendencies or preferences
by ovipositing females.
Eggs X plants. AtJAPUI the number of eggs per
plant ranged from 0 to 3850, with a total of 20,100
eggs from 14 of 23 plants (X = 873.9 eggs/plant, SD
= 1154.42) and with a dispersion index of 1525, a
significant grouped pattern. No significant correlation
was determined among the following parameters:
number of eggs and plant height (Spearman, r =
0.1179, t = O.sW, DF = 21, p > 0.59), number of
ovipositions and plant height (Spearman, r = 0.0982,
t = 0.4521, DF = 21, p > 0.66), the AI and number of
eggs per plant (Spearman, r = -0.1485, t = -0.6879, DF
= 21, p > 0.49), or the AI and number of ovipositions
per plant (Spearman, r = -0.3571; t= -1.7521, DF = 21,
p < 0.09). At VRCUB the number of eggs per plant
ranged from 338 to 4236 (all plants with at least one
oviposition) giving a total of 15,880 eggs on 1 1 plants
(X= 1443.6 eggs/plant, SD = 1399.91) and with a
Figure 1 . A female Actinote pellenea pellenea ovipositing
in Austroeupatorium inulaefolium.
dispersion index equal to 1357.55. These data also
revealed a significant grouped pattern. Again, as at
JAPUI, no significant correlation was demonstrated
between the following parameters: number of eggs
and plant height (Spearman, r = 0.1908, t = 0.5830,
DF = 9, p > 0.57), number of ovipositions and plant
height (Spearman, r = 0.2435, t = 0.5392, DF = 9, p >
0.6) , the AI and number of eggs per plant (Spearman,
r = 0.3184, t = 0.31, DF = 9, p > 0.76), or the AI and
the number of ovipositions per plant (Spearman, r =
0.3184, t = 1.0078, DF = 9, p > 0.33).
Eggs X leaves. AtJAPUI the average density of eggs
ranged from 1 1 1 to 470 eggs/ cm- ( x = 259.5 eggs/
cm-, SD = 68.32, n = 57) with the number of eggs
per oviposition ranging from 86 to 1266 (x = 479.2
eggs, SD = 228.93, n = 56). There was no significant
correlation among the following parameters: mimber
of eggs and leaf area (Spearman, r = 0.1054, t = 0.7934,
DF = 56, p < 0.43) , number of eggs and leaf orientation
(Spearman, r = -0.01 14, t = -0.0856, DF = 56, p > 0.93),
or number of eggs and leaf inclination (Spearman, r
= 0.0144, t = 0.1078, DF = 56, p > 0.91). At VRCUB
the average density of eggs was from 95 to 374 eggs/
cm'*^ ( X = 238.5 eggs/cm^; SD = 66.81, ii = 27) with the
number of eggs per oviposition ranging from 100 to
883 ( X = 422.31 eggs, SD = 199.01 eggs; ii = 26). And
again there was no significant correlation among the
parameters: number of eggs and leaf area (Spearman,
r = -0.2736, t = -1.3644, DF = 23, p > 0.18), number
of eggs and leaf orientation (Spearman, r = -0.0415, t
= -0.1991, DF = 23, p > 0.84), or number of eggs and
leaf inclination (Spearman, r = 0.0327, t= 1.1571, DF
= 23, p < 0.87). Correlations between leaf area and
42: 74-78, 200,8 (2010)
egg density were also not significant at either JAPUI
(Spearman, r = -0.718, t = -0.339, DF = 55, p > 0.9) and
in VRCUB (Spearman, r = -0.1327, t = -0.0419, DF =
23, p> 0.52).
Discussion
Oiir study was not conclusive in revealing any
consistent pattern of oviposition in A. p. pellenea,
except for clearly indicating that ovipositions tend
to be grouped. The morphological plant traits
investigated by our study were apparently not used by
the females when selecting oviposition sites. There
are of course several additional factors that would
be important in selection by oviposition sites by A. p.
pellenea females that were not evaluated in our study,
such as: 1) other plant features, such as secondary
compounds, nutritional c|uality and/or vigor (Kerpel
et ai, 2006), 2) presence of alternative host plants
in the same area (the common scandent vines M.
micranlha And M. cordifolia) that might influence the
patterns we found, and 3) a strong preference for
plants previously oviposited by females (Ulmer et
ai, 2003). Despite of which factors are influencing
female choice, it is worth noting that the grouped
pattern of immatures was revealed at both sites. As
a result, many plants were not used for oviposition
females at all, by contrast to a few that received up
to nine ovipositions (> 3000 eggs). The advantages
of grouped eggs are well known for many species of
Lepidoptera, including protection against desiccation
and predation (Stamp, 1980; (dark & Faeth, 1998).
Gregarious larvae from egg clusters also benefit
from increased develojiment rates and survival as
well as reduced predation and parasitism (Lawrence,
1990; Clark & Faeth, 1998; Denno & Benrey, 1997).
On the other hand, as pointed out above, super-
oviposition results in high mortality of small larvae
which will not get enough food as we frequently
observed in the field. The reasons for this grouped
pattern of immatures in A. p. pellenea require further
investigation to reveal if the advantages in many larvae
feeding in the same plant are higher than the risk of
death by starvation. Additionally comparisons with
other species of Actinote are also needed to reveal if
the pattern of group immatures can be generalized
in this genus.
Acknowledgements
We would like to thank Renato Rogner Ramos tor help in field
work, and Carla Penz, Daniela Rodrigues and Rudi Mattoni for
valuable suggestions in the manuscript. This study was funded by
FAPESP (grants 84/04.82-.8, 86/0618-5, 88/;t069-8 and 93/0097-9 to
RBF, and grants 00/01484-1 and 04/05269-9 for AVl.F) and is jtart
of the project “Lepidoptera of Siio Paulo State” (BIOd'A-FAPFSP
program - grant 98/05101-8). Andre V. L. Freitas thanks also
the Brazilian CNPq (fellowship 300282/2008-7) and the National
Science Fotmdation (DEB-0527441).
Literature cited
CiARK, B. R. & S. H. Faeth. 1998. The consequences of larval
aggregation in the hutterflv Chlosync taciiua. Ecological
Eiuomology 22: 408-415.
Courtney, S. P. & S. Coiirtney. 1982. The ‘edge-effect’ in butterfly
oviposition: casuality in Anthocharis rardamines and related
species. Ecological Entomology 7: 131-137.
Denno, R. F. & B. Benrey. 1997. Aggregation facilitates larval
grouth in the neotro|5ical nymphalid hutterflv Cldos\ne junais.
Ecological Entomolog)’ 22: 13.3-141.
Do,\k, P., P. Kvreiva & |. Kinc'.soi.n'er. 2006. Fitness consequences
of choosy oviposition for a time-limited btitterfly. Ecology 87:
395-408.
Ft;ENY. P. 1976. Plant apparency and chemical defense. Recent
advances in Phytochemistry 10: 1-40.
Fr.\n(;ini, R. B. 1989. Biologia e ecologia das horholetas Actinote
(Le])ido|ttera: Nymjrhalidae, Acraeinae) na transi(;ao
subtropical no stideste do Brasil. Ms Thesis. Universidade
Estadual de Campinas, Campinas, Sao Paulo, Brazil.
Francini, R. B. 1992. Ecologia das taxocenoses de Actinote
(Lepidoptera: Nym|)halidae) em Asteraceae (Angiosperma,
Magnoliatae) no sudeste do Brasil: stihsKlios para conservat^iio.
PhD Thesis. Universidade F/stadtial de Campinas, Cam|>inas,
Sao I’atilo, Brazil.
Fr.\n(;im, R. B., a. \'. L. Frei evs & C. Penz. 2004. Two new' species
of Actinote (Lejtidoptera, Nymphalidae) from Southeastern
Brazil. Zootaxa7l9: 1-10.
Freitas, A. \'. 1,. & P. S. Oi,i\tir-\. 1996. Ants ;ls selecti\e agents on
herbivore hiolog)': effects on the behaviour of a non-mymiecojrhilous
hutteifly. Jotirnal of Animal Ecology 65: 20.5-210.
Freitas, A. V'. L., I. R. I,e.\t & S. O. Ferreir,\. 1991. Selection of
oviposition sites by a lejridopteran community of a tropical
forest in southeastern Brazil. Biotropica 31: 372-375.
Freitas, A. V. L., L. A. Kaminski, R. C. M.vros & K. L. Sitva-Brand.ao.
2009. Immature stages of the Andean butterfly Actinote rn/ina
(Nymphalidae: lleliconiinae: Acraeini). Tropical l.ejtidoptera
Research 19: 18-21.
Keri’ET, S. M., E. S<)I>r.\no &• G. R. P. Moreir.\. 2006. Effect of nitrogen
on Passijlora stiherosa L (Passifloraceae) and consequences
for larval performance and oviposition in Heliconius erato
phyllis (Fahricius) (f.epidoptera: Nymphalidae). Neotro|)ical
Entomology 35: 192-200.
L. am.as, G. 2004. Checklist: Part lA. He.s|rerioidea-Pa|5ilionoidea.
In: Heppner, J.B., ed.. Atlas of Neotrojrical I,epido|3tera, Vol
.5A. Association for Tropical Lepidoptera/Scientific Publishers,
Gainesville, 439 jr.
l,.\w'RENCE, W. S. 1990. The eff ects of group size and host sjrecies
on develo|)ment and survivorship of a gregarious caterpillar
Halisidota caryae (Le|3idoptera: Arctiidae). Ecological
Fhitomolog)' 15: 5.3-62.
Lunwio, j. A. & J. F. Reynotd.s. 1988. Statistical ecology. A primer
on methods and computing. 1st ed. John Wiley and Sons,
Inc., New York, 337 p.
M. vckay, D. a. & M. C. SiNCiER. 1982. The basis of an apparent
preference for isolated host plants by ovipositing Enptychia lihye
btitterflies. Ecological Entomology 7: 299-303.
Nimer, E. 1989. Climatologia do Brasil. IBGE, Rio de Janeiro,
421 p.
P.M.ucH, M. 2006. Revisao das espccies de dc/wo/c Uiihner, [1819]
78
J. Res.Lepid.
(Lepidoptera, Nyniphalidae, Heliconiinae, Acraeini). PhD.
Thesis. Universidade Federal do Parana, Curitiba, Parana,
Brazil.
Pai.uch, M., M. M. Casagrande & O. H. H. Mielke. 2005.
Coinportaniento de agrega<;ao noturna dos machos de Actinote
surima surinia (Schaus) (Lepidoptera, Heliconiinae, Acraeini).
Revista brasileira de Zoologia 22: 410-418
Pai.uch, M., M. M. C.a,sagr.-\nde & O. H. H. Mielke. 2006. Tres
especies e duas siibespecies novas de Actinote Hiibner
(Nyniphalidae, Heliconiinae, Acraeini). Revista brasileira de
Zoologia 23: 764-778
Price, P. W. 1991. The plant vigour hypothesis and herbivore attack.
Oikos 62: 244-251.
Price, P. W. 1997. Insect Ecology. 3rd ed. John Wiley & Sons, Inc.,
New York, 874pp.
Price, P. W., H. Roininen &J. Tahvanainen. 1987. Wliy does the bud-
galling sawfly, Euura mucronata, attack long shoots? Oecologia
74: 1-6.
Rausher, M. D. 1978. Search image for leaf shape in a butterfly.
Science 200: 1071-1073.
Setzer, J. 1949. Contribuitiao para o estudo do clima do estado
de Sao Paulo. Edit. Escolas Profissionais Salesianas, Sao Paulo,
239 p.
Silva-BrandAo, K. L., N. W.ahi.berg, R. B. Francini, A. M. L. Azeredo-
Espin, K. S. Brown Jr., M. Pai,uch, D. C. Lees & A. V. L. Freitas.
2008. Phylogenetic relationships of butterflies of the tribe
Acraeini (Lepidoptera, Nymplialidae, Heliconiinae) and the
evolution of host plant use. Molecular Phylogenetics and
Evolution, 46; 515-531.
Stamp, N. E. 1980. Egg deposition patterns in butterflies: why do
some species cluster their eggs rather than deposit them singly?
American Naturalist 115: 367-380.
Strong, D. R.,J. H. Lawton & R. Solithw'ood. 1984. Insects on plants:
community patterns and mechanisms. Harvard University
Press, Cambridge, Massachussetts, USA, 330pp.
Ulmer, B., C. Gillott & M. Eriandson. 2003. Conspecifc eggs
and bertha armywonn, Mamestra configurata (Lepidoptera:
Noctiiidae), oviposition site selection. Environmental
Entomology 32; 529-534.
Ururahy, J. C.,J. E. R. CoLiARES, M. M. Santos & R. A. A. Barreto.
1984. 4. Vegetaijao, p. 553-61 1. /n: Projeto RADAMBRASIL,
levantamento de Recursos Naturais. Vol. 32. fls. SF 23-24. Rio
de Janeiro e Vitoria. Fundapao IBGE, Rio de Janeiro.
Williams, K. S. & L. E. Gilbert. 1981. Insects as selective agents on
plant vegetative morphology: egg mimicry reduces egg laying
by butterflies. Science 212: 467-469.
journal of Research on the Lepidoptna
42: 79-83, 2003 (2010)
Notes
A new subspecies of Argynnis nokomis from the Sacramento Mountains of
New Mexico (Nymphalidae)
The most vexing question in New Mexico butterfly
lore long was, “Did the Sacramento Mts. ever support
the Nokomis Fritillary?” At Paul Grey’s instigation,
I first started searching for colonies in 1963. The
next 44 years produced nothing. I still believed
that colonies had once existed at Bent, Otero Co.,
and at Ft. Stanton, Lincoln Co., but I had only utter
frustration to show for it. Eventually, I reasoned
where any museum specimens would most likely be,
and had the AMNH collection searched accordingly.
Eureka^two male Argynnis nokomis from Bent, Otero
Co. This success inspired John Rawlins to search the
Carnegie. Result: more specimens, including two of
the magnificently colored dark yellow-green females
(Holland, 2008).
Within the current concept of A. nokomis ssp., the
Sacramento Mts. population is distinctive. This case
deals with a most likely extinct, high-profile organism
that may come to be called by an English name in
town meetings. I would prefer that name be easily
translated into Latin, with the result being near its
actual Latin name. “The Tularosa Fritillary” seemed
reasonable in this context. My use of Argv«»Afollows
the recent phylogenetic placement by Simonsen et
al. (2006).
Argynnis nokomis tularosa R. Holland, new stibspecies
Diagnosis: The general shape of all markings, black and silver
resemble t\pical A. n. nokomis. Two known female spec imens lack
the fnlviis spot on DHW costa, DHW with redticed eycspots on
the PM band, silvered spots on disc redticed, DFW and DHW with
redticed black scaling along the veins.
Holotype: Female, Mescalero, Tularosa River, Otero County,
New' Mexico, ca. 7000', Atig. 13, 1931, leg. W. Huber, CMNH
collection, ex. Philadelphia Academy of Sciences Collection.
Paratypes: 2 males. Bent, Otero County, New Mexico, ca. 6000',
Ang. 12, AMNl 1 collection, ex Paul Grey coll., ex. Paul Ehrlich coll.
Year is not specified, but Paul Ehrlich was born in 1932, and Paul
Grey donated his collection to the AMNH in 1948. 1 female, tlata
as |ter hokitype.
Identification: The key below will distingtiish A. n. tularosa h am
all other subspecies based on females characters and provide my
diagnosis. Vlales are harder to separate.
Etymology: The name is feminine, as that of the nearest town
and oldest Eitropean settlemetit in the Tularosa Valley or Tularosa
Basiti. Tularosa itself is not a Spatiish root, btit is Nahuatl (Aztec),
tneaning “cattail” (|ulyan, 1996). One is tempted to spectilate it
has the satne etvmolog)' as the English word “toolies.”
Habitat: The past and present habitats are described iti detail
by Holland (2008).
Comments: The locality where the specitnens are from give
eticouragemetit to the possibility A. n. tularosa is tiot extinct. y\h
ktiown specimens were taken on the Mescalero A|iache Itulian
Reservation. The .VIescaleros were borti xenophobic and live in
alpine meadow's an hoitr outside El Paso which has done little to
tnake them trust clem city slicker Texan strangers. The Mescaleros
Key to the subspecies of Argynnis nokomis.
1.
la
2.
2a
3.
3a
4.
4a
5.
5a
5b
5c
Sexually dimorphic . 2
Not .so . ivenona (dos Passos & Grey)
Dorsally yellow' green in the lighter wing portions . 3
These areas veity blue, discal cell of VEW black aticl silver . coerulesceiis (W. Holland)
DHW discal cell yellowish, silver spots large, dorsally the eyespots iti the PM batid reduced, fulvus spot on costa ol DHW
absent . apacheana (Skinner)
Not so . 4
Very black wings, terminal regions of bctth wings, bcjth stirfaces, ahnost solid black. DI IW wanting a fulvous sjtot, VI IW' silvering
of disc reduced . nitocris (W. 11. Edwards)
Not so . 5
The typical nokomis cluster i
DHW with ftilvtis .s|)ot on costa abotit 80%. DHW with large eyespots in p.m. band, silvered spots in disc large, DEW atid VEW
with heavy black scaling alotig veins, occtirs iti few large colotiies, fore wing > 41 turn, fulvous scaling not always presetit in DFW'
yellow-green areas, yellow-green does not invade DFW cell . Sangre de Gristo typical nokomis
DHW with ftilvtis spot on costa nearly always, DHW w’ith large eyespots in the p. m. band, silvered spots in disc large, DFW and
VFM' with heai'y black scaling along the veins, occtirs in a myriad of tiny colonies, fore wing > 40 mm, noticeable ftilvtis scaling in
DFW yellow-green areas, yellow-green may invade DFW' cell Chuska Mts., Navajo Res . nigrocaerulea (W. & T. Gockerell)
Two known specimens lack fulvits sjtot on DHW costa, DHW with redticed eyespots on the p.m. baiul, silvered spots on disc
reduced, DFW and DHW with reduced black scaling along the veins; not seen in 70 years and feared extinct, wingspread closer to
typical nokomis than nigrocaerulea, Sacramento Mts., Mescalero Res . Speyeria nokomis tularosa
80
/. Res.Lepid.
Figure 1. The Sacramento Mountains Argynnis nokomis tuiarosa population. Top two rows, males, Bent, Otero County, New
Mexico, ca. 6000’, Aug. 12, AMNH collection, ex Paul Grey coll., ex. Paul Ehrlich coll. Year is not specified, but Paul Ehrlich
was born in 1 932, and Paul Grey donated his collection to the AMNH in 1 948. Bottom two rows, females, Mescalero, Tuiarosa
River, Otero County, New Mexico, ca. 7000’, Aug. 13, 1931, leg. W. Huber, CMNH collection, ex. Philadelphia Academy of
Sciences Collection. The specimen in the third row is designated the female holotype. Of the two known females, it is the only
one with both antennae intact.
42: 79-83, 2003 (2010)
81
patrol ever)' inch t)f road like they were providing the Coliseum with
virgins; merely stopping is forbidden. Permits to collect, stirvey,
or just watch the wildlife are very nearly unobtainable: they don’t
want yon spotting anything endangered, the existence of which
could be cause for limiting the absolute control the tribe enjoys
on its land. The endemic Euphydryas anicia doudcrofti Ferris and
R Holland, is known right up to the reservation line, hut there is
not one report from on the re.servation anywhere in the |)ublic
domain. The only person I ever knew to negotiate sticcessftilly to
collect on the Mescalero Reservation posed au natural for a tribal
art class in exchange.
Acknowledgements
My sincerest thanks to Jocelyn Gill of the Canadian National
Museum for the magnibcent photo work that can protect an
irreplaceable national asset from pointless handling. All specimens
of Argynnis nokomis from Otero Co. in either the AMNH or the
Carnegie are paratypes, the holoty|je in the latter instittition.
Literature Cited
DOS P.-\s,sos, C. F. & L. P. Grkv. 1947. Systematic catalog oi Spryeria
(Lepidoptera, Nymphalidae) with designations of types and
fixations of type localities. Amer. Mus. Nat. 1 list. Novitates
1297: 1-30.
Holiand, R. 2008. The holv grail of New Mexico Lepidoptera:
Sacramento Motintains Speyeria nokomis (W. H. Edwards)
(Nymphalidae). j. Lepid. Soc. 62(3): 171-173.
Jui.VAN, R. 1996. The place names of New Mexico. Albuquer(]ue
SiMttN'SEN, T. J., N. W.AHI.BliRG, A. V. Z. BrOWKR &: R. [)E JttNG. 2006.
Morphokygv', molecules and Fritillaries: a|j]jroaching a stable
]>hylogenv for Argrnuini (Lepidoptera: Nvmphalidae). Insect
Systematics and Evohition 37:40.6-418.
Richard Holiand, 1625 Roma NE, .-Mbuqnerque, NM 87106
Use of Hippuris, an emergent aquatic plant, as a larval host by the buckeye, /Mwonm coenia,
in Northern California
Recent advances in DNA-seqnence-based phylogeny
have radically altered botanists’ concepts of the
relationships within the old family Scrophnlariaceae
and between the now-disaggregated components
of that family and others previously classified in a
variety of ways (Olmstead et al, 2001; Kadereit in
Kubitzki & Kadereit, 2004). In addition to DNA
evidence, the distribution of characteristic secondary
phytochemicals affords a partially-independent
indication of plant relationships. In that vein,
host-plant choices by oligophagous insects may
suggest underlying chemical, and thus potentially
phylogenetic, affinities among the taxa involved.
The chemical basis for host selection in various
Melitaeiui (Nymphalidae) is the presence of the
bitter compounds called iridoid glycosides (Bowers
&: Puttick, 1986; Gardner & Sternitz, 1988). Shapiro
and Hertfelder (2009) recently reported the iridoid-
selecting variable checkerspot, Euphydryas clialcedona,
feeding spontaneously, repeatedly and successfully
on the exotic garden shrub butterfly bush, Buddleja
davidii, historically placed in the Loganiaceae or its
ow'ii family Buddleiaceae but now incorporated into
Scrophnlariaceae.
The common buckeye, Junonia coenia is also a
Nymphalid but not a Melitaeine, and its host range
in California embraces Scrophnlariaceae, the very
Figure 1. The Biggs garden pond. Emergent stand of
mare’s tail at right.
Figure 2. Two buckeye larvae, Junonia coenia, feeding
on mare’s tail in situ.
82
/. Res.Lepid.
closely-related Plantaginaceae, and the genus Phyla
{=Lipj>ia) in the Verbenaceae (Shapiro & Manolis,
2007). The chemical basis for host selection in
this species has been shown to involve the presence
of iridoid glycosides (Bowers, 1984) although the
story must be more complicated insofar as some
Verbenaceous genera known to produce iridoids,
such as Lantana (Rimpier & Sauerbier, 1986)
are common in buckeye environments but never
utilized.
Mare’s tail, Hippiiris vulgaris, is an emergent
aquatic flowering plant with a superficial resemblance
to a horsetail (Equisetaceae); it is widely distributed
in the cooler parts of both North and South
America but rather rare and local in California
where, however, it is occasionally grown in garden
ponds. It has been classified in the monotypic family
Hippuridaceae, whose affinities have been obscure
until recently although several authors placed
it near the Scrophulariaceae. Iridoid glycosides
were reported in mare’s tail by the pioneering
phytochemist Hegnauer in the 1970s and confirmed
by Damtoft et at (1994). Their importance for
plant systematics was emphasized by Jensen et al.
(1975) and El-Naggar and Beal (1980). Grayer et
at (1999) noted the convergence of phytochemical
and molecular-phylogenetic data in the group of
families around Scrophulariaceae, and subsequent
autliors have treated Hippuridaceae as a member of
the “Scroph” dade (Kadereit, 2004).
Given these facts it was not completely surprising
when one of us (KB) found common buckeye
larvae feeding on mare’s tail in her home pond at
Sebastopol, CA (see photo) — twice in the pond’s
12-year existence. We subsequently learned that
Mr. Michael Koslosky found buckeye larvae on the
same plant “about ten years ago while shopping at
Gonnie’s Pond Supply in Castro Valley [CA]” and
reared them out successfully on it (M. Koslosky, pers.
comm.). This is the only emergent aquatic plant
known to be a buckeye host. It is not dear whether
a larva can complete development on a single shoot
or has to access an adjacent one at least once in its
development; KB has seen them use downed stems
as “bridges.” The stems are tall enough to permit
pupation and edosion well above the water line.
The distribution of iridoid glycosides is such that
many otlier plants not known to be buckeye hosts
are potentially usable. One of us (AMS), based on
the confirmed presence of iridoids in princess tree,
Pauloumia (Bignoniaceae) foliage (Lino von Poser A
ai, 2000) , has on several occasions confined buckeye
females on it, obtained eggs easily, and reared the
larvae througli to the adult on it. The same is true on
both Catalpa speciosa3.nd C. hignonioides (currently but
shakily placed in Bignoniaceae or Scrophulariaceae),
which also produce iridoids (Sha’ban et al, 1980;
Iwaga et al, 1991). All of these are trees, and there
are no records of the common buckeye using any
tree as a host. However, the tropica! buckeye,
Junonia genoveva, feeds on black mangrove, Avicennia
(Avicenniaceae, sometimes put in Verbenaceae) and
occasionally on Lippia (Scott, 1986), and these are
iridoid producers. There is a suggestion that host
selection by these butterflies is mediated by both
apparency (growth form) and, at dose range, iridoid
chemistry. Clearly, we have a lot to learn.
Acknowledgements
We thank Mr. Jeffrey Caldwell for getting us in touch, and Mr.
Michael Koslosky for sharing his record with us.
Literature cited
Bowers, M. D. 1984. Iridoid glycosides and host-plant specificity in
larvae of the buckeye butterfly, /Mtionta coenia (Nymphalidae).
J. Chem. Ecol. 10: 1567-1577.
Bower.s, M. D. & G. M. Plittick. 1986. Fate of ingested iridoid
glycosides in Lepidopteran herbivores. J. Chem. Ecol. 12:
169-178.
DM'Itoft, S., S. R.Jensen,J. Thorsen, P. Molgard & C. E. OitiEN. 1994.
Iridoids and verbascoside in Callitrichaceae, Hippuridaceae and
Lentibulariaceae. Phytochemistry 36: 927-929.
E[,-N.4GG.4R, L.J. &J. 1.. Beal. 1980. Iridoids: a review. J. Nat. Prod.
43: 649-707.
G.ardner, D. R. & F. R. Sternitz. 1988. Hostplant utilization and
iridoid-glycoside sequestration by Etiphydryas (Lepidoptera:
Nymphalidae). J. Clieni. Ecol. 14: 147-168.
Grayer, R. J., M. W. Chase & M. S. J. Simmonds. 1999. A
comparison between chemical and molecular characters for
the determination of phylogenetic relationships among plant
families: an appreciation of Hegnauer’s “Chemotaxonomie der
Pflanzen.” Biocheni. Syst. and Ecol. 27: 369-393.
Iwaga, T., T. H.amada, S. Kurogi, T. H.ase, T. Okubo & M. Kjm. 1991.
Iridoids from Catalpa bignonioides. Phytochemistry 30: 4057-
4060.
Jensen, S. R., B.J. Nielsen & R. D/Wlcren. 1975. Iridoid compounds:
their occurrence and systematic importance in the Angiosperms.
Bot. Not. 128: 148-180.
Kadereit, J. W. 2004. Lamiales: introduction and conspectus, hr.
K. Kiibitzki and J.W.Kadereit, eds., The families and genera of
flowering plants, Vol.7. Springer-Verlag.
Lino von Poser, G., J. Sghripsema, A. T. Henriques & S. R. Jen.sen.
2000. The distribution of iridoids in Bignoniaceae. Biochem.
Syst. and Ecol. 28: 351-366.
Oemstead, R. G., C. W. DePamphilis, A. D. Wolfe, N. D. Young,
J. W. El. ISONS & P. A. Reeves. 2001. Disintegration of the
Scrophulariaceae. Am. j. Bot. 88: 348-361.
Rimpler.H. and H. Sauerbier. 1986. Iridoid glucosides as taxonomic
markers in the genera Lantana, Lippia, Aloysia and Phyla.
Biochem. Syst. and Ecol. 14: 307-310.
Sc:oTr,J. A. 1986. The butterflies of North America. Stanford.
Siia’ban, R., S. F. Ei.-N.aggar & R. K. Doskotch. 1980. Spedoside:
a new iridoid glycoside from Catalpa speciosa. J. Nat. Prod. 43:
524-526.
42: 79-83, 2003 (2010)
83
SiiAPiRfi, A. M. & K. Uertfki.dkr. 2009. Use of Buddleja as host
plant by Euphydryas chalcedonn in the Sierra Nevada foothills,
California. News Lep. Soc. 51: 27, 39.
Shapiro, A. M. & T. Manoi.is. 2007. Field guide to the butterflies
of the San Francisco Bay and Sacramento Valley Regions,
California. Univ. of Calif. Fre.ss.
Arthur M. Shapiro, Center for Population Biology', University of
California, Davis, California 95616
a mshapi ro@u ala vh.edii
Kathy Biggs, 308 Bloomfield Road, Sebastopol, California 95472
big;snesl@sonk. net
Journal of Research on the LepiclojHera
42: S5, 2003 (2010)
Editorial
Auf Wiedersehen Gutenberg
The recent trends of disappearing print media - words and images on paper - is disturbing. Many newspaper
are already extinct, and excepting parts of the financial press, more are seriously endangered. Scientific print
publications are also threatened by the global financial crisis as budgets everywhere are being drastically cut
back. More distressing is serious economic analysis that indicates the situation is likely to become much worse,
or not much better for quite some time. University and research institution libraries are shiny targets as
bureaucratic managers scramble to save their jobs by demonstrating “waste.” After all we can get many things
on line for almost free, and if Google gets its way we might be able to abandon whole libraries with attendant
savings. Who needs books? Especially as one analyst claims $130 billion a year will be saved by going wholly
on line.
Elimination of transitory matter, novels, magazines and so forth will save many trees, yet all print media share
one basic issue that cannot be overlooked - permanence. A good friend of mine made a documentary film a
decade ago. Slow fires: on the preservation of the human record, which focused on the issue of questioniug
the data loss in the storage media. We all know papyrus texts survived thousands of years. There is no test of
reliability of any other information storage system. As Prof. J. E Blanchette of UCLA put it “Imagine of the
only copy left of Imaging in Oncology were the Kindle version, with its garbled tables and lost color coding?
Or, a more likely scenario, if several copies of the book existed in different formats, each with a different
visual presentation?” Then there is long range political stability. A luddite dictatorship would have a grand
following for a data farm auto de fe.
So science presses face an increasing problem of how to pay for printed copy when there is increasing
resistance concerning cost. Our subscription base does not begin to cover costs and the base is shrinking.
Instittitional sub.scribers are also canceling. No funds. We are investigating on line publishing, whereby a
small print run by a Docutecb system will provide a limited press run for archival pitrposes, along the lines of
“Zootaxa.”
Lastly, and perhaps most disturbing is an observation by an academic colleague in Europe that students no
longer are interested in joining scientific societies. Now if this becomes the postmodern world view, where are
we headed and what is to be done? If rape is inevitable, should we relax and enjoy it?
Rudi Mattoni, Editor
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Instructions to authors
Submission of Manuscripts. Papers must be written in English. Yonr initial manuscript must be submitted as an
electronic version by e-mail to the editor, preferably as a WORD document, double-spaced. Do not format the text
and do not justify the right margin. Use only the regular and italic fonts, with the italic font only for the scientific
names of the genus and species. Do not itse boldface or vary type size (12 point preferred) for any sections or
headers. Put returns only at the end of paragraphs, not at the end of each line. Use one tab to indent each
paragraph. At the time of initial submission, all images (black and white or color) should be sent in digital form,
preferably in medium-high qualityJPEG format.
Upon acceptance of a paper, higher quality images will be requested. Eiles may be submitted by e-mail, or CD. At
this stage digital images should be TIEF, or maximum qnalityJPEG files with at least 2700 x 4000 pixels resolution.
Should yon have further queries on this subject, please contact the technical editor.
Title material. All papers must include complete title, author’s name(s), institution (s), and address for
correspondence, including e-mail address. A family citation must be given in parentheses (Lepidoptera: Hesperiidae)
for referencing.
Abstract. Max. 300 words. No citations or figure references.
Keywords. Max. 10 words in addition to those in the title.
Text. The text of a regular research paper shottld be clearly structured: e.g. introduction, material and methods,
results, discitssion, etc. with acknowledgements and literature cited at the end. Papers to be cotisidered as Notes,
Opinion pieces, or Book Reviews need not follow this stritctitre. A note with four or fewer references should have
these cited in the body of the text.
Name citations and Systematic works. The first tnention of any organism should include the full scientific name
with unabbreviated name of author(s) and year of description. Taxonotnic descriptions must comply with the rules
of the ICZN (4th edition).
Tables. Present tables in the simplest form possible. Tables nutst be numbered serially with Arabic mtmerals
independent from illustrations. Tables shottld be provided at the end of the paper on separate pages and not
embedded in the body of the text. Put the legends for tables on a separate page. Tables should not repeat
information that is already given in the text of ilhtstrations. When formulating tables, keep in mind that the final
table will fill 1 columti (width 8 cm or 2 columns (16,5 cm).
Illustrations are numbered serially with Arabic numerals. References to figures in both text and captions should
be as fig. and Fig. respectively. Do not spell out. Figure captious should be listed on a separate page. Maps are
considered figures and should be so captioned. Do not use plate designations; multiple figttres in a single grouping
may be individually mtmbered or subdivided alphabetically (e.g. fig la, lb, etc). Line drawings in black and white
should include a metric scale. Both color and black and white images in high quality may be iucluded. When
arranging your plates consider that they may appear either iti 1 coltunn (width 8 cm) or iti 2 colitmns (17 cm).
References. All citations in the text mitst be alphabetically and chronologically listed under Literature Cited. In
the text, references should be cited in the form "... Wilson (1998a)...”, (Wilson, 1988a), (Soitthwood et al., 1979),
or (Thomas 8c Thomas, 1994). Please give full name of journals and confortu to the following style:
Atkins, A. F. 1975. The life history of Anisynta ////ymrfi Waterhouse and Lyell (Lepidoptera:Hersperiidae:
Trapezitinae). Australian Entomological Magazine 2: 72-75.
- 1987. The life history of Trapezites Waterhouse and Tmpezites /i/hgrt/iotV/c.s Waterhouse
(Lepidoptera: Hesperiidae: Trapezitinae). Australian Entomological Magazine 13: 53-58.
Larsen, T. B. 1990. The butterflies of Egypt, Apollo Books, Svendborg. 112 pp. Figurny-Pttchalska E., R. M.
E. Gadeberg &J. J. Boomsma. 2()()0. Comparison of genetic population structure of the large bltte btitterflies
Maculinea ytausithous 'awA M. teleius. Biodiversity Conservation 9: 419-432.
Thomas, J. A., R. T. Clarke, G. W. Elmes & M. E. Hochberg. 1998a. Population dynamics in the genus Maculinea
(Lepidoptera: Lycaenidae), pp. 262-290. In: Dempster, J. P. 8c 1. F. G. McLean (eds.). Insect popitlations.
Kltiwer Academic Publishers, Dordrecht.
Reprints. We will provide authors with a high quality PDF file of their paper by e-mail. Authors can produce au
arbitrary number of reprints identical to the printed manuscripts u.sing these files.
Page charges. We have no page charges nor charges for color plates. However, contributions toward color plates
would be appreciated. Please use color only where necessary as the format is expensive.
The Journal of research
ON THE LEPIDOPTERA
SMITHSONIAN LIBRARIES
3 9088 01964 3899
VOLUME 42 2003 (2010)
IN THIS ISSUE
Date of publication: January 31, 2010
PAPERS
Differences in thermal responses in a fragmented landscape: temperature affects the sampling of diurnal, but not nocturnal
fruit-feeding Lepidoptera
Danila H. Riheiro and Andre V. L. Freitas 1
Use of sound and aerial chases in sexual recognition in Neotropical Hamadryas butterflies (Nymphalidae)
Onildo J. Marini-FiUw and Woodruff W. Benson . 5
Ecobiology of the common castor hutterfly Ariadne merione merione (Cramer) (Lepidoptera: Rhopalocera: Nymphalidae)
Janaki Bai Alluri, Samatha Bodapati, Bhupathi Rayalu Matala, Sandhya Deepika Devara and Subba Reddi Chilakala 13
Larval feeding behaviour and myrmecophily of the Brenton Blue, Orachrysops niobe (Trimen) (Lepidoptera: Lycaenidae)
David A. Edge and Huih van Hamburg 21
Life history of the Imperial Moth Eacles imperialis (Drury) (Saturniidae: Ceratocampinae) in New England, U.S.A.: distribution,
decline, and nutritional ecology of a relictual islandic population
Paul Z. Goldstein 34
Association of three species of Strymon Hiibner (Lycaenidae: Theclinae: Eumaeini) with bromeliads in southern Brazil
Simone Schmid, VolkerS. Schmid, Rafael Kamke, Josefina Steiner and Anne ZJllikens 50
Temporal and spatial segregation of Battus devilliers und B. polydamas cubensis (Papilionidae) in La Habana, Cuba
Ormaily Madruga Rios and Alejandro Barro Caiiamero 56
A tale of two species: detritivoiy, parapatry, and sexual dimorphism in Lamprospiliis collucia and L. orcidia (Lycaenidae:
Theclinae: Eumaeini)
Robert K. Robbins, Annete Aiello, Julie Femstein, Amy Berkov, Astrid Caldas, Robert C. Busby and Marcelo Duarte 64
Aggregated oviposition in Actinote pelU>neci pellenea}r{nhi\ev (Lepidoptera: Nymphalidae)
Ronaldo Bustos Francini and Andre Victor Liicci Freitas 74
NOTES
A new subspecies of Argynnis nokomis from the Sacramento Mountains of New Mexico (Nymphalidae)
Richard Holland 79
Use of Hippuris, an emergent aquatic plant, as a larval host by the buckeye, coenia, in Northern California
Arthur M. Shapiro and Kathy Biggs 81
EDITORIAL
Auf Wiedersehen Gutenberg
Riidi Mattoni 85
Cover: adult of Eacles impericdis, 7 August, 2004. © M. W. Nelson/MtissachusetLs Natural Heritage & Endangered Species Program.
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