ISSN 0038-3872
SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
BULLETIN
Volume 88 Number 2
L= SE1 EHT= 10.0. KV MAG= K 70.0 PHOTO= 911
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Hippothoa h alina
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BCAS-A88(2) 45-92 (1989) AUGUST 1989
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Bull. Southern California Acad. Sci.
88(2), 1989, pp. 45-60
© Southern California Academy of Sciences, 1989
Bryozoans, Hermit Crabs, and Gastropods: Life Strategies Can
Affect the Fossil Record
Penny A. Morris,! Dorothy F. Soule,” and John D. Soule?
‘Natural History Division, North Harris County College, Houston, Texas 77073
?Allan Hancock Foundation, University of Southern California,
Los Angeles, California 90089-0371
Abstract. —Epizootic associations among bryozoans, hermit crabs, and gastropod
shells are not chance occurrences, but constitute a relationship that may benefit
the bryozoan, and possibly the hermit crab. Gastropod shells from Recent Texas
gulf coast localities and fossil and Recent Pacific coast localities were examined.
Texas gastropod shells occupied by hermit crabs and their bryozoan epifauna were
compared with unoccupied shells. In summer all available shells were occupied
by hermit crabs, and all occupied shells found were encrusted by bryozoans.
In winter in Texas no bryozoans encrusted intact Polinices shells unoccupied
by hermit crabs; 33% of Thais shell fragments contained bryozoans and all Busycon
spp. shells or fragments contained bryozoans.
Distinctive differences were found in encrusting patterns of hermit crab occupied
and unoccupied shells. Similar bryozoan encrusting patterns were found on shells
occupied by hermit crabs from California and Texas. These data can be used for
interpreting the incidence of hermit crab occupation in both fossil and Recent
gastropod shells.
Epizootic associations among bryozoans, hermit crabs, and gastropods or gas-
tropod shells, represent a relationship that has existed since Jurassic times (Glaess-
ner 1969; Palmer and Hancock 1973; Taylor 1976). Such fossil associations have
also been described in more recent periods; e.g., by Roger and Buge (1947), Walter
(1969), Buge and Fischer (1970), Taylor and Cook, (1981) and Walker (1988).
Modern occurrences have been noted, for example, by Kirkpatrick and Metzelaar
(1922), Cook (1968), Gordon (1972), Taylor and Cook (1981), Baluk and Rad-
wanski (1984), and Bishop (1987). In west Africa, Cook (1968, p. 127) found that
one species of encrusting bryozoan, Membranipora commensale, was primarily
found on gastropod shells occupied by hermit crabs.
The preference of bryozoans for specific substrates has been well documented
(Pinter 1969; Rogick and Croasdale 1949; Ryland 1976; Winston and Eiseman
1980). In selecting substrates, larvae may explore and inspect sites before attach-
ment and metamorphosis (Woollacott and Zimmer 1971; Crisp 1974), and some
species exhibit preferential settling to the extent of selecting concave surfaces as
opposed to convex surfaces (Ryland 1959; Ryland and Gordon 1976; Bishop
1988). Walker (1988) found that bionts would not settle on tethered Olivella shells
that were not occupied by hermit crabs.
The purpose of the following study was to document whether bryozoans en-
crusting gastropod shells occupied by hermit crabs more frequently select one part
45
46 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
of the shell over another, and to provide further documentation on whether hermit
crab occupation can be determined in fossil gastropod assemblages. Interpretation
may then be made as to whether gastropod shells are in their original habitat, or
have been moved to other locations by hermit crabs (Frey 1987).
Materials and Methods
Modern gastropod shells inhabited by hermit crabs were collected in the spring
from California and summer from Texas coasts. Gastropod shells, unoccupied
by hermit crabs in winter, were collected from Texas. The assemblages of shells
were analyzed for the following:
(1) Identification of gastropod shells, epizootic bryozoans, and presence or
absence of associated hermit crabs.
(2) Encrusting sites of bryozoans.
(3) The presence of other epizootic species on shells occupied by hermit crabs.
The broken shells that were collected in December 1988 from Texas were
restricted to shells and fragments similar to those occupied by hermit crabs in the
summer months.
Pliocene and Pleistocene fossils from the Pacific coast of North American were
examined in collections of the University of California, Museum of Paleontology,
Berkeley (UCP).
Results
Fifteen trochid gastropod shells (Tegula funebralis) occupied by hermit crabs
were collected in the spring from Rockaway Beach, California (Fig. 1). The hermit
crab was Pagurus samuelis, a species which prefers rocky shores lacking sand,
mainly in upper and middle intertidal zones, from Vancouver to Baja California
(Reese 1969; Haig and Abbott 1980). The encrusting bryozoan was Hippothoa
hyalina (Table 1).
Sixty gastropod shells inhabited by the hermit crab Jsocheles wurdmanni, a
filter feeder living along exposed coasts (Fotheringham 1976), were collected in
the summer from the Texas coast (Figs. 2A, 2B). Of these, 15 were from the gulf
side of the Bolivar Peninsula, 20 were from the entrance to the Galveston Ship
Channel, and 25 were from the gulf side of San Luis Pass. The number and
identity of each gastropod species is listed in Table 2.
Fifty one gastropod shells were collected in the winter months from the gulf
side of Galveston Island. All of the shells lacked hermit crab occupants and were
trapped among the rocks composing the jetties. No hermit crab occupied shells
were found. The number and identity of each gastropod species is listed in Table 3.
Hippothon hyalina was found on all hermit crab occupied Tegul/a shells collected
in California in April 1972. Membranipora arborescens was found on all hermit
crab occupied shells collected in Texas in August 1985. In addition, the gastropod
Crepidula plana was found attached to the gastropod Polinices. Crepidula is fre-
quently found in association with hermit crabs (Abbott and Haderlie 1980).
In comparison, some of the broken and entire shells collected from Galveston
Island in the winter months in 1988 lacked encrustations of either bryozoans or
other epibionts. None of the Polinices shells were encrusted with, or had indi-
cations of the past presence, of bryozoans or any other encrusting organism. The
BRYOZOANS, HERMIT CRABS, AND GASTROPODS 47
ere
Fig. 1. Map of California. Region of Rockaway Beach is circled.
Fig. 2. Map of Texas. A. Region of Galveston and Bolivar Peninsula is circled. B. Galveston Island
(g), and Bolivar Peninsula (b) are indicated in respect to the mainland (m).
other shells or shell fragments collected did not yield the same concise results
(Table 3), but none contained burrowing bryozoans or the green alga Entero-
morpha, nor were they entirely covered on the exterio by Membranipora arbo-
rescens.
Burrowing bryozoans were found on two species of gastropod shells inhabited
by hermit crabs (Table 2). Others have found similar results: for example Gordon
(1972, Goat Island, New Zealand); J. D. Soule (unpubl., southern California tidal
pools); and Smyth (1988, Guam). Burrowers have also been found on the aperture
of the living infaunal gastropod Olivella biplicata at Bodega Bay, California (Walk-
er 1985, 1988). Therefore, burrowers apparently cannot offer conclusive evidence
that gastropods were dead and occupied by hermit crabs.
All Recent material has been deposited at Allan Hancock Foundation, Uni-
versity of Southern California, Los Angeles.
Ecology
California. —Rockaway Beach (Fig. 1) is a rocky intertidal environment char-
acterized by high energy waves. In the summer months the hermit crab Pagurus
samuelis, carrying the Tegula shell, can be seen among populations of living 7.
funebralis in the upper tidal pools which are isolated during low tide. Shell material
that is not utilized by hermit crabs seasonally is either trapped in rock crevices,
broken up in the surf, or carried into deeper water and buried. The availability
of gastropod shells is the single most important factor limiting hermit crab pop-
ulation size (Kellogg 1976).
Texas.—The sampled localities are on the gulf side of the Bolivar Peninsula
(an elongated extension of the coast forming a sand spit), and the gulf side of the
west and east end of Galveston Island, an offshore barrier island (Figs. 2A, 2B).
Prevailing longshore currents are east to west. The localities are high energy
48 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
Table 1. Encrusting sites on hermit crab occupied shells for California specimens.
Encrusting sites
Num- Her- Inner Inner
Gastropoda ber mit sur-_ lip:
species (total speci- crab face colu- Cover- Other
number of mens pres- Bryozoan_ outer mella ing Hum- — encrusting
specimens) (%) ent species lip area Apex shell mock species
Tegula funebralis 5 4 Hippothoa
(12) (42) hyalina x
2 x H. hyalina xX
(17)
2 xX H. hyalina 4 x x
(17)
| Xx H. hyalina x spirorbid
(8) encrusting
on colony
1 x H. hyalina xX x
(8)
1] Xx H. hyalina xX XxX x Balanus sp.
(8) on colony
X = Present.
environments with sediments varying from well sorted sand and silty sand to
shelly sand. Like the Rockaway Beach locality, shell material is rapidly broken
up. The absence of empty shells, and the occupation of broken shells by hermit
crabs in the summer months, is indicative of a limited supply (Back et al. 1976).
All of the shells occupied by hermit crabs were found in approximately the
same ecological zone as the living snail. Of the shells collected, Thais haemostoma
is found in shallow water on rocks and oyster reefs, Polinices duplicatus is found
from low tide to 15 meters and both Busycon spiratum and B. contrarium are
found intertidally.
Encrusting Bryozoans
The two species of bryozoans involved in the hermit crab association were
Hippothoa hyalina (Pinter 1973; Morris 1980) on the Pacific coast, and Mem-
branipora arborescens on the gulf coast (Lagaaij 1963, as Conopeum commensale:
fide Cook 1968). Hippothoa hyalina (Fig. 3) is found in shallow waters distributed
from Arctic to temperate waters in the northern hemisphere and in temperate
waters in the southern hemisphere (Morris 1980). Geologically the species has
been found as early as the Eocene. Along the Pacific Coast of North America the
species can easily be separated from other multiseriel species belonging to this
genus as it has a pleurilaminar growth form with both male and female zooids
produced on secondary and subsequent layers, never the primary layer (Pinter
1973). Membranipora arborescens (Fig. 4), also found in shallow water, ranges
from Morocco to the Gulf of Mexico. Cook (1968) stated that there had been a
great deal of confusion separating the encrusting stage of M. arborescens from M.
commensale. She also stated (1968, p. 123) that the encrusting stage of Mem-
branipora arborescens has cryptocystal denticles, abundant chitinous spinules on
BRYOZOANS, HERMIT CRABS, AND GASTROPODS 49
Fig. 3. Hipothoa hyalina (L). A multilaminar portion of the colony.
Fig. 4. Membranipora arborescens (Canu & Bassler). Opesial membrane is removed, showing thick
cryptocyst with small spines, and fused block-like tubercles.
the frontal wall, and a brown line generally separating the zooids. The gulf coast
colonies of Membranipora arborescens that were encrusted on hermit crab oc-
cupied shells in this study were pleurilaminar, never arborescent, had small cryp-
tocystal denticles and chitinous spinules, and the brown line separating the zooids
was irregularly present. The cryptocyst was thick, fused, and block-like tubercles
were present. A few kenozooids were produced where growing edges meet, and
sheets of zooids were large and regular. Occasionally the shell surface was etched.
Bryozoan Encrusting Patterns
Gulf Coast, Recent.—The initial sites of encrustation by the bryozoans are
oriented in relation to the position of the crab in the shell. On the shells from the
Gulf of Mexico (Fig. 5), the inner surface of the outer lip of the gastropod shell
was above the anterior end of the crab and the inner lip (base of the columella)
was below the anterior end (See Carleton and Roth 1975, for terminology). These
two areas are usually colonized initially; subsequently colonies expand outward
and over the gastropod shell surface (Fig. 6A, B). Analysis of colony edges indicates
that fusion may take place, due either to recognition of sibling colonies or to
fusing of single colony segments after growing apart (Chaney 1983). There were
also scattered indications of redirected growth between nonsibling zooids (Chaney
1983). The data on the bryozoan encrusting sites are listed in Table 2.
California, Recent.—The hermit crab Pagurus samuelis occupies Tegula fu-
nebralis shells. Initia! points of bryozoan encrustation are above and/or below
the anterior end of the crab, as indicated by the cheliped in Fig. 7B, C, after which
colonies may expand and coalesce (Chaney 1983), eventually covering the exterior
shell surface. Following the establishment of the bryozoan colonies, barnacles and
spirorbid worms may settle on the bryozoans. As in the Texas specimens, there
was either colony fusion of siblings or indications of redirected growth between
nonsibling zooids (Chaney 1983). Data on the bryozoan encrusting sites are listed
in Table 2.
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BRYOZOANS, HERMIT CRABS, AND GASTROPODS 38)
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Fig. 5. Thais haemostoma, Galveston Island, Texas showing position of the crab in the shell.
Fig. 6. Encrusting Bryozoan sites on gastropods from Galveston Island area. 6A. Initial encrusting
sites (coarse stippling) can be in either one or both places indicated. 6B. Subsequent colony expansion
indicated (coarse stippling) on shell surface.
Fig. 7. Shell and encrusting sites on gatropod from Rockaway Beach. Side view of Tegula funebralis
with apertural region (light stippling) indicated. 7B. Bryozoan encrusting (coarse stippling) near aperture
(light stippling). 7C. Bryozoan nearly covering apertural region (coarse stippling). Aperture is lightly
stippled. Anterior end of hermit crab indicated by chelipeds.
54 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
Oregon, California, fossil.—Pliocene and Pleistocene bryozoan material from
the Pacific Coast of North America was examined from the following localities:
Elk River, Cape Blanco, Oregon (Pleistocene, Baldwin 1945); Moonstone Beach,
near Arcata, California (Pliocene, Faustman 1964); Cape Blanco, (Pleistocene,
Addicott 1964). All localities contained some shallow water elements and were,
at least in part, characterized by an open coastline.
The Elk River sandstone (UCP-B7371) contained gastropod shells of Fusitriton
oregonensis and Nucella canaliculata; both had evidence of probable hermit crab
occupation. The bryozoan Hippothoa hyalina encrusted either on the apertural
region and/or the inside upper lip. In several specimens bryozoan etchings were
found on the interior upper lip as well as on the shell surface, indicating the
existence of a hippothoid (Morris 1975). Fusitriton oregonensis, as well as other
gastropods identified from this site but lacking bryozoans (Epitonium indianorum,
Olivella biplicata), are found in Recent environments living on sandy bottom
offshore, in shallow water, or on beaches. Nucella canaliculata prefers crawling
on rocks (Abbott 1974). The presence of these gastropods in the fossil environment
indicates that, before they were inhabited by hermit crabs and encrusted by H.
hyalina, at least some shells were transported from other areas.
Moonstone Beach (UCP-B5525) specimens Nucella canaliculata and N. la-
mellosa are both shallow water gastropods which in modern environments are
frequently found on rocks. In the area of Moonstone Beach that each was collected,
no evidence of rocks was found. The deposit was composed of poorly lithified
sandstone. The encrusting pattern of Hippothoa hyalina (inner upper lip, columella
region) indicates the probable presence of hermit crabs occupying a sandy beach.
Therefore it is reasonable to assume that there was some transportation of the
shells after death of the living gastropod before occupation by hermit crabs oc-
curred. Where parts of some colonies had been rubbed off, typical hippothoid
etchings were visible.
A poorly consolidated conglomerate south of the lighthouse at Cape Blanco is
primarily composed of the pelecypod Tresus (UCP-A8712). At this site the bryo-
zoan Hippothoa hyalina was found encrusting the gastropods Calyptraea fastigiata
and Cerithiopsis sp. The shells represent two different configurations; the former
is hat-shaped and the latter is spiral-shaped. The bryozoan encrusting pattern for
Calyptraea is similar to that of Tegu/a and the pattern for Cerithiopsis is similar
to Thais and Busycon. The presence of the aforementioned gastropods as well as
the pelecypods Tresus sp., Saxidomus giganteus and Macoma sp. indicates a low
intertidal to subtidal environment. The bivalves, particularly Tresus, were artic-
ulated and indicate the absence of sediment reworking. The presence of these
gastropods, as well as their probable hermit crab occupation, indicates that death
and burial occurred at the site of the living components.
Ideally in order to test a null hypothesis that there is no difference between
inhabited and non-inhabited shells, all shells would need to be collected at the
same time of year. This was not possible because there are no unoccupied shells
in Summer, as indicated by the occupation of broken shells, whereas only empty
shells were found in winter.
To test the hypothesis, a 2 x 2 contingency table was set up to measure the
significance using chi-square with N as | degree of freedom. A chi-square value
of 3.84 (1 degree of freedom or higher) indicates a 95% chance that the measured
BRYOZOANS, HERMIT CRABS, AND GASTROPODS 55
association was not random, thereby nullifying the hypothesis (Simpson et al.
1960).
In comparing winter and summer collections of Polinices duplicatus, the chi-
square was 4.7; Thais haemostoma collections had a chi-square of 13.3; results
of Busycon spiratum and B. contrarium yielded no significant differences. In the
case of the first two, the null hypothesis that there 1s no difference must be rejected
as there is a difference between inhabited and non-inhabited shells. As the latter
two do not yield the same results, it might be postulated that more robust shells
or shells with thicker walls (i.e., Polinices duplicatus, Thais haemostoma) could
survive in a relatively intact condition from summer to winter months while more
delicate shells Gi.e., Busycon spiratum, B. contrarium) would probably be lost.
Therefore the shells Polinices duplicatus, Thais haemostoma were probably avail-
able for habitation late in the hermit crab season while both species of Busycon
were available after the hermit crabs left the intertidal environment in winter.
The second null hypothesis to be tested is that there are no preferred settling
areas on the hermit crab occupied shell. Tables 1 and 2 list five potential encrusting
sites. Again a 2 x 2 contingency table was set up to measure the significance using
chi-square with N as | degree of freedom with a correction for small sample size.
In all the samples tested, there was no significant difference in selection of the
inner surface, outer lip or inner lip (columella area). The values for the outer lip
and bryozoan colony covering the shell varied from chi-square values of 2.194
to 2.4, or less than 75% but greater than 50% chance that the association was not
random. In one instance (Tegut/a funebralis, Busycon spiratum) there was less than
50% chance. The chi-square values for the inner lip (columella) and bryozoan
colony covering the shell were 2.5 to 5.5, or greater than 75% but less than 99%
chance.
The second null hypothesis figures are not as convincing in regards to prefer-
ential settling sites, but still indicate a greater than 50% chance that settling is not
random with the hypothesis not well supported. It may be that all we can state
is that there is a strong tendency for one site to be selected over another for
encrustation. }
Discussion
Results of the present study offer insights on several aspects of the biotic as-
sociations: crab and bryozoan behavior in selecting a shell or other substrate;
factors possibly influencing bryozoan encrusting sites; and identification of hermit
crab occupied shells in the fossil record.
Shell Availability
Hermit crab require a shell for protection from predation and environmental
stress, as well as a place to brood their eggs (Back et al. 1976). If a hermit crab
does not have a shell, it will not feed (Allee and Douglis 1945) and will subse-
quently die. In most environments suitable for hermit crabs, shells available for
occupation are limited (Bertness 1981) because empty shells are rapidly broken
up in the high energy environment. Hermit crabs will either occupy broken shells
(Fotheringham 1976) or shells that are too small (Conover 1976, 1978). Polinices
and Thais shells may survive into the winter but the more fragile Busycon shells
would not.
56 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
Shell Alternatives
Some hermit crab species have found an alternative to occupying a suboptimal
shell. The European species Pagurus prideauxii is found in association with the
cloak anemone Adamsia palliata, and as the crab grows the anemone spreads
itself like a cloak over the crab. In a west African association, the edge of the
bryozoan colony extends over the aperture (Cook 1964) and thus serves to cover
the crab as the crab grows.
Shell Preference
Hermit crabs were shown to prefer a clean shell over an encrusted shell if it is
available (Grant and Ullmer 1974). Clean shells would be lighter in weight than
heavily encrusted shells, but an eroded “‘second hand” shell, could be weakened
by burrowing invertebrates or algae, or by abrasion.
Bryozoan larval Settlement
Bryozoans do not haphazardly select a substrate (Rogick and Croasdale 1949;
Crisp 1973, 1974; Crisp and Ryland 1960; Ryland 1959, 1962, 1976; Pinter 1969;
J. D. and D. F. Soule 1977; Cancino 1986). Clean substrate is first conditioned
by the appearance of microflora (J. D. and D. F. Soule 1977); then if the substrate
is unusually slippery or rough, the bryozoan can alter the substrate to a limited
extent. Stebbing (1972) stated that a microbial surface flora could determine zones
of favorability, at least on algal fronds. In species such as Macrocytis (giant brown
kelp) which produce large amounts of mucus, it was noted that the area in front
of the growing colony is altered with apparent mucus removal (Morris 1975).
Bryozoans that encrust shells may etch the surface (Morris 1975) in an identifiable
manner. Although J. Soule (1973) analyzed the bryozoan adhesive of several
species, no worker has determined how the bryozoan cleans or etches the substrate.
Nutrient Availability: Particulate and Dissolved Organic Matter
If microbial surface flora could determine favorable encrusting zones in shells,
then what factors would attract the microflora, at least on the inner surface of the
upper lip of the gastropod shell occupied by a hermit crab? As the crab is tearing
prey apart and feeding, or filtering out particulate matter, food debris could be
lodged inside the shell along with fecal material, and amino acids would also be
present (Ferguson 1982; Manahan 1983; Jaeckle 1985). These materials would
offer nutrition to various microbial groups and to bryozoans. In studies on bryo-
zoan nutrition (Summarized by Ryland 1976; Best and Thorpe 1986a, b), it has
been shown that bryozoans are capable of feeding on a variety of organic material.
Net accumulation of amino acids by gymnolaemate bryozoans has been dem-
onstrated by Stephens (1981).
It seems plausible then that bryozoans encrusting shells occupied by hermit
crabs would tend to settle where an optimal concentration of food is available.
As indicated in Tables 1, 2 and 3, as well as by the chi-square values discussed
above, this is very likely to be on the inner surface of the outer lip or on the inner
lip. A few bryozoans will settle elsewhere, although the variables which influence
site selection are not entirely understood.
BRYOZOANS, HERMIT CRABS, AND GASTROPODS Si
The Fossil Record
Hyden and Forest (1980) stated that hermit crabs are seldom preserved as
fossils due to poor calcification as well as the delicate skeletal structure and the
high energy environment in which they live. Although hermit crabs, as fossils,
are known to exist at least from the Jurassic (Glaessner 1969), the record is sparse.
Indications of hermit crab occupation by a bryozoan encrusted shell are as follows:
development of hummocks or monticules on the bryozoan colony surface; mul-
tialaminar growth that surrounds the shell, but does not completely cover the
aperture; and growth into the shell aperture [P. L. Cook formerly British Mus.
(Nat. Hist.), pers. comm. and P. Taylor, British Mus. (Nat. Hist.), pers. comm.].
Palmer and Hancock (1973) noted characteristic flat areas on the shell and dis-
continuities in the bryozoan colonies due to the hermit crab dragging the shell.
To this we add another factor, the position of the initial encrusting site, as an
indication of hermit crab occupation.
Fossil shells that have been inhabited by hermit crabs may also serve in inter-
pretation of paleoecology and stratigraphy. A fossil assemblage is not an intact
community, due either to nonpreservation (Lawrence 1968) or transport. Hermit
crabs modify shell assemblages by affecting the physical transport of the shell
(Frey 1987). Identification of a shell as having been occupied by a hermit crab
indicates a previously shallow water environment. Thus, even though the shell
may have been transported to or from deeper waters, its final resting place could
be considered shallow water if other associated fossil specimens also indicated
the same conditions.
Symbiosis?
Are there, then, mutually beneficial effects of the association between bryozoans
and hermit crabs? The bryozoan colonies, as they expand over the gastropod shell
surface, might serve as camouflage. The preferential selection by hermit crabs of
clean shells over shells containing epibiota mentioned above tends to negate the
concept of a symbiotic relationship (Palmer and Hancock 1973) in which the
bryozoans benefit the hermit crab by providing camouflage. The advantages for
the bryozoans are more compelling; the sessile colonies become mobile, thereby
providing them with protection from environmental changes in temperature,
dissolved oxygen, and salinity, or from siltation. The association offers a suitable
substrate with opportunities to reach new substrates for colonization. Bryozoans
may feed on organic debris produced by the hermit crab in the form of fecal
pellets, particles of food, microbiota, or dissolved organic matter. However, the
limited number of bryozoan species found on hermit crab occupied shells indicates
that they are restricted to those that can tolerate intermittent exposure to the air
by the intertidal movements of the hermit crabs in exchange for the benefits
provided.
Conclusions
There are distinctive differences in bryozoan settling patterns in hermit crab
occupied shells and non-occupied shells. Results were statistically significant for
Polinices duplicatus and Thais haemostoma, but not for the more fragile Busycon
Spp.
58 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
The hermit crab occupied shells of Tegula funebralis in California were colo-
nized exclusively by Hippothoa hyalina whereas Texas shells of Polinices dupli-
cata, Thais haemostoma and Busycon spp. were inhibited exclusively by Mem-
branipora arborescens, regardless of the presence of other epibiota. This further
confirms the ability of certain bryozoan species to select preferred substrates.
Pattern of encrustation can be used to determine whether fossil or Recent shells
were once inhabited by hermit crabs, indicating their shallow water habitat.
The benefits to the bryozoan species able to survive in the intertidal environ-
ment include access to a food supply, and mobility to protect from siltation or
poor environmental conditions. The relationship is probably not symbiotic since
predators are probably attracted to motion of the crabs rather than to the surface
appearance. As discussed, the hermit crab will provide organic detritus and amino
acids within the micro-habitat of the bryozoan in the apertural area of shell. These
factors can be helpful to paleontologists in interpreting the fossil records.
Acknowledgments
We wish to thank the following individuals for their help in completing this
manuscript: Patricia L. Cook, George Kennedy, F. K. McKinney, James H.
McLean, Paul D. Taylor, Marilyn Theiss-Kron, and John P. Thorpe.
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Accepted for publication 1 April 1989.
Bull. Southern California Acad. Sci.
88(2), 1989, pp. 61-79
© Southern California Academy of Sciences, 1989
Seaweeds and Seagrasses of Southern California: Distributional
Lists for Twenty-one Rocky Intertidal Sites
Steven N. Murray and Mark M. Littler
Department of Biological Science, California State University,
Fullerton, California 92634 and Ocean Studies Institute,
Long Beach, California 90840
Department of Botany, National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560
Abstract. — A total of 213 macrophyte taxa was identified from 21 rocky intertidal
sites in southern California, with 194 identified to the level of species, 14 to genus,
and 5 to family. Eight southern California taxa were added to distributional records
reported in the Marine Algae of California. The number of taxa ranged from 107
at Government Point, Santa Barbara County, to 51 at West Point, San Nicolas
Island. No significant differences (Mann-Whitney two-sample test) in number of
taxa were obtained between island and mainland or between sand-influenced and
sand-free intertidal sites. Similarly, no significant difference (Kruskal-Wallis non-
parametric ANOVA by ranks) was found in the numbers of taxa collected among
sites exposed to warm, intermediate and cold water masses. It appears that site-
specific combinations of environmental conditions determine species richness at
southern California intertidal sites rather than large-scale patterns in abiotic en-
vironmental parameters.
Southern California coastal waters are characterized by a rich flora of benthic
marine macroalgae and seagrasses. The relatively large coastal area, which includes
a total of ca. 917 km of shoreline distributed over a latitudinal range of only ca.
212 km, exhibits much variation in exposure to wave action, ocean water masses,
thermal regimes, and in substratum composition. This high degree of habitat
heterogeneity 1s believed (Murray et al. 1980; see also Abbott and Hollenberg
1976) to contribute strongly to the high diversity of macrophytes known to occur
in southern California waters.
Despite its taxonomic richness, knowledge of the southern California marine
macrophyte flora is still best described as being in the early stages of exploration
(see Murray 1974). Marine macroalgal floristics of southern California were ad-
vanced dramatically by Abbott and Hollenberg (1976) who provided taxonomic
descriptions, distributional data and taxonomic keys for 669 species of California
seaweeds. Unfortunately, little additional progress has been made in our taxo-
nomic understanding of southern California seaweeds since Abbott and Hollen-
berg’s (1976) classic work, and today floristic knowledge is poorly developed for
most of the southern California region. This is particularly true for the seaweeds
occurring on the relatively pristine and biogeographically 1mportant Southern
California Islands where taxonomic contributions during the last 12 years have
been limited to species lists provided with ecological (Littler 1979) and geograph-
ical (Apt et al. 1988) surveys. This situation contrasts greatly, for example, with
61
62 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
the considerable progress that has been made (e.g., Scagel et al. 1986; Gabrielson
et al. 1987) in advancing our understanding of the systematics of the seaweeds of
northern Washington, British Columbia and southeast Alaska.
This paper provides lists of marine macroalgae and seagrasses collected from
21 southern California intertidal sites during the 1975-1979 ecological sampling
program sponsored by the U.S. Department of Interior, Bureau of Land Man-
agement (now referred to as Minerals Management Services). Previous versions
of these records have been used for distributional analyses of macrophytes oc-
curring in southern California waters (Murray et al. 1980; Murray and Littler
1981). However, the species lists generated for these sites are currently available
only in unpublished governmental reports. These distributional data for intertidal
seaweeds and seagrasses are of particular value considering the paucity of recent
floristic information on southern California macrophytes.
Methods
Marine macroalgae and seagrasses were collected from 21 rocky intertidal sites
located in southern California between Point Conception and the United States-
Mexico border (Fig. 1; Table 1). Seven stations were located on the mainland and
14 were established on the eight Southern California Islands or Channel Islands
which have been divided (Philbrick 1967) into Northern (San Miguel, Santa Rosa,
Santa Cruz, and Anacapa) and Southern (San Nicolas, Santa Barbara, Santa Cat-
alina, and San Clemente) groups. A minimum of one station was established on
each island, with seven stations located on members of the Northern and seven
on members of the Southern Channel Island groups.
Study sites encompassed the geographic extent of the southern California region
and consisted of areas representative of protected or semi-protected rocky shore-
line. Collections were not made at sites that received consistently heavy wave
action, such as characterizes much of the central and northern California coast
(see Ricketts et al. 1985) which receives direct exposure to ocean swells. Similarly,
sites varied as to the composition and stability of the substratum, and exposure
to ocean currents and seawater temperature regimes.
The study sites (Fig. 1; Table 1) were visited from one to several times between
July 1975 and July 1979. Macrophyte collections at each site were made over a
period of at least three days and included not only taxa found in ecological samples,
but also specimens of conspicuous forms observed in the vicinity of the study
areas. Details of the ecological sampling program including the visitation dates
for each site are provided elsewhere (Littler 1977, 1978, 1979, 1980a, b; Littler
and Littler 1985) and, hence, will not be described here.
Because only 12 of the 21 study sites were sampled throughout the year (Summer,
fall, winter, spring), seasonally-occurring macrophyte taxa were likely missed at
the sites subjected to less intense seasonal sampling. Our observations at the 12
sites where seasonal sampling occurred suggest that relatively few intertidal mac-
rophytes are completely absent from the southern California shoreline during any
particular season. However, we did record significantly fewer numbers of taxa at
the 9 sites subjected to incomplete seasonal sampling (Crook Harbor, San Miguel
Island; Prisoner’s Harbor, Santa Cruz Island; South Coast and North Coast, Ana-
capa Island; West Point, San Nicolas Island; Catalina Harbor, Santa Catalina
Island; Northwest Coast, San Clemente Island; Paradise Cove, Los Angeles Coun-
INTERTIDAL SEAWEEDS AND SEAGRASSES 63
J ©
SAN
@
MIGUEL
CLEMENTE
Fig. 1. Locations of the 21 rocky intertidal sites. Refer to Table 1 for numerical key to sites.
ty; and, Dana Point, Orange County) compared with the 12 sites where collections
were made throughout the year (65.0 + 9.4 vs. 84.8 + 13.8 S.D.; Mann-Whitney
two-sample test, U = 94.0, n, = 12, n, = 9, P < .01). Analyses of taxa numbers
using only data from the 12 sites where seasonal sampling was performed produced
statistical results identical to those where all 21 sites were considered. Conse-
quently, the numbers of taxa reported herein and employed in statistical com-
parisons are the “raw” recorded values and have not been weighted to reflect
sampling frequency.
Macrophyte collections generally were preserved in 3—5% Formalin-seawater
as suggested by Abbott and Tsuda (1985) and returned to the laboratory for
identification and processing. Specimens were identified by the authors; most
identifications were confirmed by Dr. Isabella A. Abbott, currently of the Uni-
versity of Hawaii. For selected macrophytes such as crustose algae and members
of taxonomically difficult genera (e.g., Cladophora, Ceramium, and Polysiphonia),
identification to the species level usually was not performed due to time con-
straints. Instead these specimens have been categorized under higher taxonomic
units, i.e., genus or family. Herbarium specimens of most taxa were prepared and
deposited in the U.S. National Herbarium, National Museum of Natural History,
Smithsonian Institution.
Results
A total of 213 taxa was identified from the 21 rocky intertidal sites, with 194
identified to the species level, 14 to the level of genus and 5 to the level of family.
A list of the taxa and the sites at which they were collected is presented in Table 2.
64 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
Table 1. Names, locations, characteristics, and numbers of taxa for the 21 rocky intertidal sites.
Floristic affinities are derived from Murray and Littler (1981).
Sand or Number
Site Latitude and cobble of
number Site location longitude Floristic affinity influence taxa
Island sites
1 San Miguel Island, 34°02'55"N cold yes 85
Cuyler Harbor 120°20'08”W
2 San Miguel Island, 34°01'28"N cold no 62
Crook Point 120°22'43”W
3 Santa Rosa Island, 33°53 3,12N cold yes 78
South Point 120°06'3 1” W
4 Santa Cruz Island, 33°57'43"N intermediate no 89
Willows Anchorage 119°45'16”"W
5 Santa Cruz Island, 34°01'14"N intermediate no 61
Prisoners Cove 119°41'14"W
6 Anacapa Island, 34°00'19"N warm no 77
South Coast 119°25'05”"W
and
34°00'24"N
119°24’38"W
7 Anacapa Island, 34°00'31"N warm no 58
North Coast 119°24'21"W
8 San Nicolas Island, 33°12'54’"N cold yes 98
Dutch Harbor 119°28'22”"W
9 San Nicolas Island, 33°16'43'"N cold no Sil
West Point 119°34'41"W
10 Santa Barbara Island, 33°28'43'N intermediate no 92
Cave Canyon 119°01'36"W
11 Santa Catalina Island, 33°26'47'"N warm no 91
Fisherman Cove 118°29'04”"W
12 Santa Catalina Island, 33°25'42"N warm no 69
Catalina Harbor 118°30'42”W
13 San Clemente Island, 33°00'06"N warm no 79
Wilson Cove 118°33'03"W
14 San Clemente Island, 33°58'06"N warm no 80
Northwest Coast 118°34'18"W
Mainland sites
15 Government Point, 34°26'35’N cold yes 107
Santa Barbara County 120°27'06"W
16 Coal Oil Point, 34°24'27"N intermediate yes 95
Santa Barbara County 119°52’40”"W
17 Paradise Cove (Malibu), 34°00'42"N intermediate yes 68
Los Angeles County 118°47'30"W
18 Whites Point, 33°43'11"N warm yes 58
Los Angeles County 118°19'39"W
19 Corona Del Mar, 33°35'14"N warm yes 65
Orange County 117°51'54”"W
20 Dana Point, 33235) 250N warm yes 59
Orange County 117°42'44"W
21 Ocean Beach, 32°44'35’N warm no 80
San Diego County ESHA SE AW
65
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76 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
The number of taxa identified for each station varied from 107 (Government
Point, Santa Barbara County) to 51 (West Point, San Nicolas Island) and averaged
76.3 + 15.5 S.D.: no particular relationship between the number of species col-
lected and the main abiotic features of the sites were apparent. Statistically sig-
nificant differences were not obtained either between island and mainland (76.4
+ 14.3 vs. 76.0 + 18.9; Mann-Whitney two-sample test, U = 51.0, n, = 14,
n, = 7, P > .05) or between sites characterized (see Murray et al. 1980; Murray
and Littler 1981) as exposed to water masses of warm (71.6 + 11.5), cold (80.2
+ 21.2) and intermediate (81.0 + 15.4) seawater temperatures (Kruskal-Wallis
nonparametric ANOVA by ranks, H = 1.85, df = 2, P = 0.60). Similarly, no
significant difference in numbers of taxa was obtained (Mann-Whitney two-sample
test, U = 62.5, n, = 9, n, = 12, P > .05) when comparisons were made between
sites identified (Littler et al. 1989) as mostly receiving exposure to seasonal sand
inundation or cobble movements (79.2 + 18.0) and those essentially free of sand
or cobble influence (74.1 + 13.7).
Discussion
The results of this study significantly augment existing distributional records
of southern California macrophytes by providing lists of intertidal floras for 14
island and 7 mainland sites. Although floral lists for numerous southern California
mainland sites exist (e.g.. Dawson 1959, 1965; Widdowson 1971; Nicholson and
Cimberg 1971; Thom and Widdowson 1978; Thom 1980), prior to our study
intertidal floras of island stations were known for only San Clemente (Sims 1974;
Littler and Murray 1975; Murray and Littler 1977), Santa Cruz (Seapy and Littler
1982: Apt et al. 1988) and San Nicolas (Caplan and Boolootian 1967; Littler et
al. 1983) Islands. Additionally, this study adds eight new taxa (specimens are on
file at the National Herbarium) to the list of algae known to occur in southern
California waters based on distributional data provided by Abbott and Hollenberg
(1976). Two of these (Ceramium viscainoense and Carpopeltis divaricata) are not
listed for the California flora by Abbott and Hollenberg (1976), but appear in a
list of algae collected from Santa Cruz Island (Apt et al. 1988). They represent
species that appear to have more southerly distributions. Each of the remaining
six taxa (Besa papillaeformis, Hymenena flabelligera, Mastocarpus jardinii, Mi-
crocladia borealis, Monostroma zostericola, and Porphyra lanceolata) are species
with more northerly, cold water distributional centers. These species appear in
southern California waters at sites most proximal to the colder waters of the
California Current, i.e., on San Miguel and San Nicolas Islands or at Government
Point. With the exception of Porphyra lanceolata, which was found in southern
California waters by Nicholson and Cimberg (1971), none of these taxa has ap-
peared in recent species lists (e.g., Widdowson 1971; Thom and Widdowson 1978;
Thom 1980; Apt et al. 1988) of southern California intertidal seaweeds.
Prior to our research, few studies of intertidal algae on the relatively isolated
offshore islands had been performed (see Murray 1974). Consequently, we antic-
ipated that our study, besides providing new, site-specific lists, would result in
numerous additions to the southern California flora and perhaps, several new
species. Although we generated new distributional records for individual islands,
our sampling program produced only eight additions to Abbott and Hollenberg’s
(1976) list of species occurring in southern California waters. This suggests that
INTERTIDAL SEAWEEDS AND SEAGRASSES VY
the list of intertidal macrophytes comprising the southern California flora likely
will expand only after careful biosystematic study. However, it is probable that
many species as yet unreported for southern California waters, particularly those
with distributional centers north of Point Conception, eventually will be identified
from subtidal habitats in southern California. Stewart (1984) has observed that
several species common in the low intertidal zone along central California shores
occur in deep subtidal sites in southern California, indicating that colder water
seaweeds can survive at more southerly latitudes by occupying deeper water
habitats. Her observations are supported by Lewbel et al. (1981) who found that
the shallow subtidal (ca. 20 m) fauna and flora of Cortes and Tanner Banks, two
seamounts located ca. 180 km west of San Diego, had close affinity with the cold
water, central California biota.
In examining the distributions provided in Table 2, in conjuction with our own
observations and information provided by Abbott and Hollenberg (1976) and
Abbott and North (1972), it is possible to identify seaweeds that serve as potential
indicators of cold or warm water intertidal habitats in southern California. Cold
water sites, such as those at Government Point and on San Nicolas and San
Miguel Islands, appear to support populations of seaweeds such as Analipus ja-
ponica, Fucus gardneri, Laminaria setchellii, Callithamnion pikeanum, Iridaea
cordata var. cordata, Neorhodomela larix, and Laurencia spectabilis. In contrast,
intertidal habitats of sites characterized by exposure to warm water masses, such
as occur for much of Santa Catalina and San Clemente Island, are often uniquely
characterized by populations of Colpomenia sinuosa, Dictyopteris undulata, Ei-
senia arborea, Endarachne binghamiae, Halidrys dioica, Sargassum agardhi-
anum, Zonaria farlowii, Chondria californica, Jania tenella, Laurencia snyderiae,
and Pterocladia capillacea.
The abiotic environmental features of greatest importance in determining the
abundances of macrophyte populations and the structure of macrophyte com-
munities in southern California intertidal habitats appear to be the frequency and
extent of sand scouring and accumulation on the rocky substratum, and the
thermal characteristics of the water masses to which a site is exposed (Littler, et
al. 1989). However, our analyses indicate that there is no relationship between
species richness and the thermal regime or the degree of sand influence for in-
tertidal sites in southern California. Additionally, species richness does not vary
significantly between island and mainland sites. These findings suggest that the
richness of rocky intertidal macrophyte floras in southern California is controlled
by site-specific factors and does not conform to patterns based on large-scale
gradients of abiotic environmental features or insular geographical position.
Acknowledgments
We thank Dr. Isabella A. Abbott for sharing with us her vast knowledge of
Pacific coast marine algae. Also, we are especially grateful for the assistance of
Robert H. Sims who was responsible for maintaining and organizing the collec-
tions of macrophyte materials and to Diane S. Littler who served as administrative
coordinator for the project. Special acknowledgments are also given to Roger R.
Seapy who contributed greatly to the success of the entire study. Funding for this
research was provided by the U.S. Department of Interior through contract No.
AA 550-CT6-40. The completion of this paper was facilitated by a California
78 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
State University, Fullerton, Senior Faculty Research Award made to SNM. This
paper is Southern California Ocean Studies Institute Contribution No. 62.
Literature Cited
Abbott, I. A., and G. J. Hollenberg. 1976. Marine algae of California. Stanford University Press,
California, x11 + 827 pp.
, and W. J. North. 1972. Temperature influences on floral composition in California coastal
waters. Proc. Int. Seaweed Symp., 7:72-79.
, and R. T. Tsuda. 1985. Collecting, handling, preservation, and logistics. Pp. 67-86 in
Handbook of phycological methods. Ecological field methods: macroalgae. (M. M. Littler and
D. S. Littler, eds.), Cambridge University Press.
Apt, K., C. D’Antonio, J. Crisp, and J. Gauvain. 1988. Intertidal macrophytes of Santa Cruz Island,
California. The Herbarium, Department of Biological Science, University of California, Santa
Barbara, California. Publ. No. 6, vii + 87 pp.
Caplan, R. I., and R. A. Boolootian. 1967. Intertidal ecology of San Nicolas Island. Pp. 203-217 in
Proceedings of the symposium on the biology of the California Islands. (R. N. Philbrick, ed.),
Santa Barbara Botanic Garden, Santa Barbara, California.
Dawson, E. Y., 1959. A primary report on the benthic marine flora of southern California. Jn An
oceanographic and biological survey of the continental shelf area of southern California. Publs.
Calif. St. Wat. Poll. Contr. Bd., 20:169-264.
1965. Intertidal algae. Jn An oceanographic and biological survey of the southern California
mainland shelf. Publs. Calif. St. Wat. Qual. Contr. Bd. 27:220-231, 351-438.
Gabrielson, P. W., R. F. Scagel, and T. B. Widdowson. 1987. Keys to the benthic marine algae of
British Columbia, northern Washington and southeast Alaska. Dept. Botany, Univ. British
Columbia, Vancouver, ui + 197 pp.
Lewbel, G. S., A. Wolfson, T. Gerrodette, W. H. Lippincott, J. L. Wilson, and M. M. Littler. 1981.
Shallow-water benthic communities on California’s outer continental shelf. Mar. Ecol. Progr.
Ser., 4:159-168.
Littler, M. M. (ed.). 1977. Spatial and temporal variations in the distribution and abundance of
rocky intertidal and tidepool biotas in the Southern California Bight. Bureau of Land Man-
agement, U.S. Department of the Interior, Washington, D.C.
(ed.). 1978. The annual and seasonal ecology of southern California subtidal, rocky intertidal
and tidepool biotas. Bureau of Land Management, U.S. Department of the Interior, Washington,
D.C.
(ed.). 1979. The distribution, abundance and community structure of rocky intertidal and
tidepool biotas in the Southern California Bight. Bureau of Land Management, U.S. Department
of the Interior, Washington, D.C.
1980a. Overview of the rocky intertidal systems of southern California. Pp. 265-306 in The
California Islands: proceedings of a multidisciplinary symposium. (D. M. Power, ed.), Santa
Barbara Museum of Natural History, Santa Barbara, California.
—. 1980b. Southern California rocky intertidal ecosystems: methods, community structure and
variability. Pp. 565-608 in The shore environment. Vol. 2: ecosystems. (J. H. Price, D. E. G.
Irvine, and W. H. Farnham, eds.), Academic Press, London.
,and D.S. Littler. 1985. Nondestructive sampling. Pp. 161-175 im Handbook of phycological
methods, ecological field methods: macroalgae. (M. M. Littler and D. S. Littler, eds.), Cambridge
University Press.
,and S. N. Murray. 1975. Impact of sewage on the distribution, abundance and community
structure of rocky intertidal macro-organisms. Mar. Biol. (Berl.), 30:277-291.
, D. R. Martz, and D. S. Littler. 1983. Effects of recurrent sand deposition on rocky intertidal
organisms: importance of substrate heterogeneity in a fluctuating environment. Mar. Ecol. Progr.
Ser., 11:129-139.
,D.S. Littler, S. N. Murray, and R. R. Seapy. 1989. Southern California intertidal ecosystems.
In Ecosystems of the world. (P. Nienhuis and A. C. Mathieson, eds.), Elsevier Science Publishers,
Amsterdam. /n press.
Murray, S. N. 1974. Benthic algae and grasses. Pp. 9.1-9.61 in A summary of knowledge of the
southern California coastal zone and offshore areas. Vol. II. Biological environment. (M. D.
INTERTIDAL SEAWEEDS AND SEAGRASSES 79
Dailey, B. Hill, and N. Lansing, eds.), Bureau of Land Management, U.S. Department of the
Interior, Washington, D.C.
, and M. M. Littler. 1977. Seasonal analyses of standing stocks and community structure of
macroorganisms. Pp. 7-32 in Influence of domestic wastes on the structure and energetics of
intertidal communities near Wilson Cove, San Clemente Island. (M. M. Littlerand S. N. Murray,
eds.), Calif. Water Res. Ctr., Univ. Calif., Davis Contrib. No. 164.
,and M. M. Littler. 1981. Biogeographical analysis of intertidal macrophyte floras of southern
California. J. Biogeogr., 8:339-351.
——.,, M. M. Littler, and I. A. Abbott. 1980. Biogeography of the California marine algae with
emphasis on the Southern California Islands. Pp. 325-339 in The California Islands: proceedings
of a multidisciplinary symposium. (D. M. Power, ed.)., Santa Barbara Museum of Natural
History, Santa Barbara, California.
Nicholson, N. L., and R. L. Cimberg. 1971. The Santa Barbara oil spills of 1969; a post-spill survey
of the rocky intertidal. Pp. 325-399 in Biological and oceanographic survey of the Santa Barbara
Channel oil spill 1969-1970, Vol. I. (D. S. Straughan, comp.), Allan Hancock Foundation,
Univ. S. California.
Philbrick, R. N. 1967. Introduction. Pp. 3-8 in Proceedings of the symposium on the biology of the
California Islands. (R. N. Philbrick, ed.), Santa Barbara Botanic Garden, Santa Barbara, Cal-
ifornia.
Ricketts, E. F., J. Calvin, J. W. Hedgpeth, and D. W. Phillips. 1985. Between Pacific Tides, fifth
edition. Stanford University Press, Stanford, California. xxvi + 652 pp.
Scagel, R. F., D. J. Garbary, L. Golden, and M. W. Hawkes. 1986. A synopsis of the benthic marine
algae of British Columbia, northern Washington and southeast Alaska. Dept. Botany, Univ.
British Columbia, Vancouver, vi + 444 pp.
Seapy, R. R., and M. M. Littler. 1982. Population and species diversity fluctuations in a rocky
intertidal community relative to severe aerial exposure and sediment burial. Mar. Biol. (Berl.),
71:87-96.
Sims, R. H. 1974. Macrophytes. Pp. 13-17 in Biological features of intertidal communities near the
U.S. Navy sewage outfall, Wilson Cove, San Clemente Island, California. (S. N. Murray and
M. M. Littler, eds.), U.S. Naval Undersea Center Technical Paper No. 396.
Stewart, J.G. 1984. Algal distributions and temperature: test of an hypothesis based on vegetative
growth rates. Bull. Southern California Acad. Sci., 76:5—-15.
Thom, R. M. 1980. A gradient in benthic intertidal algal assemblages along the southern California
coast. J. Phycol., 16:102-108.
, and T. B. Widdowson. 1978. A resurvey of E. Yale Dawson’s 42 intertidal algal transects
on the southern California mainland after 15 years. Bull. Southern California Acad. Sci., 77:
1-13.
Widdowson, T. B. 1971. Changes in the intertidal algal flora of the Los Angeles area since the survey
by E. Yale Dawson in 1956-1959. Bull. Southern California Acad. Sci., 70:2-16.
Accepted for publication 8 February 1989.
DESERT ECOLOGY 1986
A Research Symposium
Twelve papers from the Desert Studies Consortium at the Academy 1986 Annual
Meeting comprise a new publication now available. Subjects include the Coachella
Valley Preserve, Water Rights, Late Pleistocene Mammals, Chemical Defense
Patterns of Certain Desert Plants, Off-Road Vehicle disturbances, Desert Pupfish,
Plant Communities, Desert Bats, etc.
Send name, address, and $29.00 per copy in check made out to The Southern
California Academy of Sciences, 900 Exposition Blvd., Los Angeles, CA 90007.
Bull. Southern California Acad. Sci.
88(2), 1989, pp. 80-87
© Southern California Academy of Sciences, 1989
A New Species of Early Pleistocene Cotton Rat from the
Anza-Borrego Desert of Southern California
Robert A. Martin! and Robert H. Prince?
'Department of Biology and *Department of Mathematics and Computer Science,
Berry College, Mount Berry Station,
Rome, Georgia 30149
Abstract. — Fossil cotton rats, genus Sigmodon, were recovered from the super-
posed Vallecito-Fish Creek beds of the Palm Spring Fm. in Anza-Borrego State
Park, California. Sigmodon minor is the common cotton rat species throughout
the late Pliocene Layer Cake and Arroyo Seco faunal intervals. A new species, S.
lindsayi, characterized by large size and a suite of features of the first lower molar,
appears first in the early Pleistocene Vallecito Creek faunal interval, extending
from collecting zone 53.8 to zone 58.8, from approximately 610 to 305 meters
from the top of the sequence. Sigmodon lindsayi is replaced in zone 57.8, at about
the 366 meter level, by Sigmodon minor, but appears once again in zone 58.8, at
approximately the 305 meter level, above which it is not recorded. There is no
evidence that the two species were sympatric in the Anza-Borrego sequence, but
it is likely. The replacement pattern is interpreted as either 1) incorrect strati-
graphic assignment of some specimens or 2) the result of competition and possibly
habitat modification.
Cotton rats are by far the most commonly recovered small mammals in many
deposits of late Pliocene and Pleistocene age throughout the southern United
States. Because there are often enough specimens for statistical treatment, and
additionally because there is a large body of neontological data from extant species
for consultation, cotton rats make ideal subjects for evolutionary and paleoeco-
logical study (Martin 1979, 1984, 1986). The occurrence of cotton rats in the
Palm Spring Formation of the Anza-Borrego Desert is important, as this is one
of the few rock sequences in the United States where cotton rat remains have
been recovered in stratigraphically superposed beds that span a considerable amount
of time. Consequently, macroevolutionary and macroecological patterns can be
documented. This paper represents the results of an initial taxonomic study of
the Palm Spring Fm. cotton rat remains, and reports the presence of a new species
from the upper, early Pleistocene Vallecito Creek faunal zone. The geology, col-
lecting horizon information, and magnetostratigraphy of the Vallecito-Fish Creek
sequence was described by Downs and White (1968) and Opdyke et al. (1977).
The planed and prismatic dentition of cotton rats is more akin in function to
that of their northern ecological analogues, the arvicolines, and rather than use
the cumbersome cricetine dental terminology of Hershkovitz (1962), we have
chosen to use instead the arvicoline terminology of Van der Meulen (1978) for
the first lower molar. Homologies are given in Fig. 1. Measurement methods
(ollow Martin (1979) and Czaplewski (1987). Both occlusal and basal lengths are
80
NEW PLEISTOCENE COTTON RAT 81
Fig. 1. Topography of a Sigmodon hispidus \eft first lower molar. BRA = buccal reentrant angle,
LRA = lingual reentrant angle, acd = anteroconid, pro = protoconid, met = metaconid, hyp =
hypoconid, ent = entoconid, post = posterior cingulum or posterolophid. Homologies of reentrant
angles to folds, as published by. Hershkovitz (1962) and others, are as follows: BRAI = major fold,
BRA2 = first minor fold, LRA1 = second primary fold, LRA2 = first primary fold, LRA3 = first
secondary fold.
provided for consistency (see Tomida 1987:103). Abbreviations are as follows:
LACM = Los Angeles County Museum, MSU = Michigan State University, L =
left, R = right, upper and lower molars (M) indicated by super- and subscript
numbers, respectively. The term “zone” as used throughout this paper refers to
a specific collecting horizon (level) of Downs and White (1968) in the Vallecito-
Fish Creek sediments.
Systematic Paleontology
Order Rodentia Bowdich, 1821
Family Cricetidae Rochebrune, 1883
Sigmodon Say and Ord, 1825
Sigmodon lindsayi, new species
Holotype. —LACM 124161, LM,, from zone 57.6 (Locality LACM 1114).
Paratypes.— Zone 57.6 (Locality LACM 1114): LACM 124276, LM?; 124136,
RM,; 124117, RM,; 3402, LM,; 124154, RM!; 124144, RM!; 124122, LM,;
124146, RM!; 124139, LM?; 124123, LM,; 124132, LM,; 124278, LM?; 124280,
LM?; 124260, RM?; 124270, RM’; 124266, LM,; 124263, RM?; 124261, RM7?;
124166, RM,; 124282, RM; 124268, RM’; 124168, RM; 124283, LM’; 124169,
82 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
LM?; 124272, LM?; 124265, RM?; 124264, RM?; 124129, RM?; 124148, RM;;
124187, LM’; 124130, RM?; 124190, LM?; 3400, RM; 3397, LM,; 124126, LM,;
124120, LM,; 124135, RM?; 124111, RM,; 124140, LM?; 124188, RM!; 124138,
LM?; 124191, RM,; 124134, RM3?; 124193, LM,; 124192, LM,; 124152, LM!;
124157, LM!; 124162, RM;; 124153, LM!; 124143, RM’; 124133, RM3?; 124124,
LM,; 124155, LM!; 124131, RM>.
Horizon and type locality.—Collecting zone 57.6 (Locality LACM 1114) of
Downs and White (1968), approximately 366-305 meters from top of the Val-
lecito-Fish Creek sequence, Palm Spring Formation, Anza-Borrego Desert State
Park, San Diego Co., California; early Pleistocene (early Irvingtonian land mam-
mal age).
Referred specimens.—The following specimens were also recovered from the
Vallecito Creek-Fish Creek sequence of the Palm Spring Formation.
Zone 53.8 (Locality LACM 4963): LACM 122964, RM,.
Zone 55.5 (Locality LACM 1615): LACM 124242, RM!; 124238, LM,; 124251,
LM!-M?; 124257, LM;; 124258, LM?; 124248, part R mandible with M,-M,;
124252, L maxillary fragment with M!-M?-M?; 124233, RM?; 124249, part L
mandible with M,-M,-M;; 124234, LM,; 124259, LM,; 124235, RM?; 124236,
LM?; 124241, LM!; 124240, RM,.
Zone 55.9 (Locality LACM 1297): LACM 6940, part R mandible with M,-M3.
Zone 57.7 (Locality LACM 1461): LACM 124197, part R mandible with M,-
M,-M,.
Zone 58.8 (Locality LACM 1114): LACM 3396, RM!; 7037, RM,; 3399, LM;;
3401, RM.
Diagnosis. —Size large, teeth hypsodont (Table 1, Fig. 2): anteroconid of M,
wide, anteroposteriorly flattened, symmetrically extended both labially and lin-
gually, and with an occasional enamel atoll in teeth with little wear; metaconid
often bulbous and posteriorly directed; protoconid often triangular; lingual reen-
trant angle (LRA) 2 deep and anteriorly directed; first lower molar with either
three or four well-developed roots.
Etymology.—Named in honor of Everett H. Lindsay, whose research on the
correlation of upper Pliocene and Pleistocene North American sediments provides
a modern framework for evolutionary studies.
Description. — The following description applies to both the holotype and para-
type material. Measurements of the dentition are presented in Table 1.
M,: The anteroconid is large and, in teeth with moderate wear, anteroposteriorly
flattened (Fig. 3). It has both labial and lingual extensions. Reentrant angles are
narrow and similar to most other cotton rat species except modern Sigmodon
leucotis, in which the reentrant angles are wide and the M, appears long and
narrow. In teeth with little or moderate wear, LRA3 and BRA2 directly abut,
with only a thin isthmus of dentine connecting the anteroconid and protoconid.
This isthmus may widen in heavily worn teeth. Lingual reentrant angle 2 is often
deep and anteriorly extended, where it may nearly touch the enamel wall of BRA2.
In specimens from Zone 57.6, the metaconid is bulbous and posteriorly directed,
and the protoconid may appear triangular in outline. An enamel atoll is present
in the anteroconid of two of eight specimens, lying just above the junction of
BRA2 and LRA3. The atoll is lost with moderate wear. In one specimen, LACM
124111, the anteroconid is isolated from the protoconid-metaconid complex (Fig.
83
NEW PLEISTOCENE COTTON RAT
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84 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
HS
ow
HEIGHT My
2.0 3.0 4.0 5.0
LENGTH X WIDTH My,
Fig. 2. Crown height (mm) of the first lower molar as a function of occlusal area (mm?) in Sigmodon
and Prosigmodon species (modified from Martin 1979 and Czaplewski 1987). Inset shows method of
taking measurements: | = occlusal length, ll = occlusal width, lll = crown height at metaconid. V =
S. minor medius (Verde Formation), A = S. minor medius, Rexroad Loc. 3, B = S. curtisi, Inglis IA,
C = S. libitinus, Haile XVIA, D = S. bakeri, Coleman IIA, E = S. ochrognathus (extant), F = S.
leucotis (extant), G = S. hispidus, (Reddick IA), H = S. lindsayi, Vallecito Creek. Horizontal and
vertical lines represent the observed ranges of both measures as they pass through the grand mean.
Open circles = Prosigmodon holocuspis, x = P. chihuahuensis.
3). This is unusual, but it 1s also occasionally expressed in teeth of extant cotton
rat species.
The first lower molar of S. /indsayi has either three or four roots. The labial
root is well developed, but the lingual root may be absent. Five of eight specimens
in which the root pattern could be determined had three roots, the others four.
The single first lower molar from zone 53.8 (LACM 122964) is similar to S.
lindsayi in size and overall morphology, but two features set this particular spec-
imen apart from those typical for the species. First, the anteroconid, although
large and somewhat laterally expanded, is not developed in this regard to the
extent as in those from zone 57.6. Secondly, the tooth has only a tiny third (labial)
accessory root. This is in contrast to the teeth in zones above 53.8, in which at
least three, and occasionally four roots are well developed. It is only provisionally
referred to S. lindsayi.
Additionally, in one very lightly worn M, from zone 55.5 (LACM 124238)
NEW PLEISTOCENE COTTON RAT 85
Fig. 3. First lower molars of Sigmodon lindsayi, new species, and S. mascotensis. S. lindsayi: A,
LACM 124161, holotype LM,, 19.2; B, LACM 124124, unworn, possibly embryonic LM,, x 16.9;
C, LACM 124111, RM, with slightly eroded anteroconid-notice separation of metaconid from an-
teroconid, x 17.0; D, LACM 124117 RM,, <18.6; E, LACM 124123 LM,, heavily worn, x 18.6. S.
mascotensis: F, MSU 12531, LM,, from a female, collected 6 mi. W Autlan, 4400 ft, Jalisco, Mexico,
x 15.0.
LRA2 is more perpendicular to the midline of the tooth and the tip of the meta-
conid does not, as a result, appear to extend posteriorly. This may be a function
of wear or it could represent a slight morphological change within S. lindsayi
populations through time.
M,-M;: These teeth do not differ in any appreciable way from those of most
cotton rats, such as S. curtisi nd S. hispidus. Reentrant folds are relatively deep
and narrow, and the anterior cingulum is moderately to well developed on both
teeth, as it is in all cotton rats except S. bakeri and S. peruanus (Martin 1979).
M!-M?-M?: Likewise, the upper dentition is not diagnostic. These teeth are
relatively large (Table 1), but demonstrate no specific characters which would
allow separation from other middle Pleistocene species, such as S. curtisi or S.
hudspethensis.
Comparisons. —Sigmodon lindsayi was approximately the size of S. curtisi (Mar-
tin 1979, 1986). Utilizing Martin’s (1984) formula for estimating body mass in
cricetine rodents from M, length, S. /indsayi averaged 76.6 g, with a range of
55.9-116.2 g. Occlusal length was used for these calculations.
The enlarged, symmetrically flattened and laterally extended anteroconid on
M, is a feature that we have seen only on one specimen of the extant Sigmodon
mascotensis, the Jaliscan cotton rat. The M, of MSU 12531, from Jalisco, Mexico,
shows a great deal of similarity to the holotype of S. lindsayi (Fig. 3). However,
the anteroconid is not as greatly extended laterally in two other specimens available
for study. A fourth specimen of S. mascotensis, with the anterior portion of M,
broken off, could be added to the analysis for a study of root count. Four well-
developed roots are present on all specimens. This is in contrast to the condition
in S. lindsayi, in which three roots are present in more than half the specimens.
86 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
An enamel atoll appears on the anteroconid of other cotton rat species, but is
generally rare. We have not, in any case, seen it developed to the same extent in
any other species as it was in the two specimens of S. /indsayi.
Discussion
Sigmodon lindsayi is an extinct member, along with S. curtisi, S. hudspethensis
and S. /ibitinus, of the /eucotis species group of cotton rats (see Martin 1979, 1986
for details of taxonomy), characterized by only three or a combination of three
and four roots on the first lower molar. All extant cotton rats in North America
except S. /eucotis have four well-developed roots on M, and are members of the
hispidus species group. Species exclusively with four roots on M, are first seen in
the fossil record during the late middle Pleistocene. The evidence suggests that
the four-rooted M, evolved from the three-rooted form.
The teeth of S. /indsayi are more high crowned than other extinct members of
the /eucotis species group (Table 1; Fig. 2). Coupled with the high percentage of
first lower molars having four roots, it is conceivable that S. /indsayi was close
to the hispidus species grade of dental evolution.
One of the more interesting questions is whether or not the hispidus species
group evolved from a single common ancestor of the /eucotis group, or if hispidus
species group members evolved independently from two or more /eucotis group
species. If the latter, then it may be that S. /indsayi is ancestral to S. mascotensis.
Specimen LACM 122964, a lower right M, from zone 53.8, which we have
tentatively referred to S. /indsayi, deserves further comment. It is, unfortunately,
the only cotton rat specimen recovered from zone 53.8. Zone 53.8 occurs at
approximately the 610 meter level in the Vallecito-Fish Creek sequence, well
within the Vallecito Creek faunal zone. Zone 55.5, the next overlying interval
which contains S. /indsayi, is at about the 427 meter level. We do not know how
much time occurred during those 183 meters of sedimentation, because there 1s
some doubt about the entire duration of the Vallecito Creek interval (Opdyke et
al. 1977). However, if further collecting confirms the dental characters of the
cotton rat at zone 53.8, then it may be that this zone represents the transition
from a smaller, more generalized species such as S. minor to a member of the
leucotis species group. In size and hypsodonty, LACM 122964 is similar to small
specimens of S. /indsayi from higher zones. It is for this reason that we provisonally
refer the specimen to the latter species. However, accessory roots are minimally
developed on M,, as in S. minor, and the anteroconid of M, is also not as
exaggerated as it is in typical S. /indsayi first lower molars.
We will present a detailed analysis of morphometric change in cotton rat den-
titions from the Anza-Borrego sequence elsewhere, but it is interesting to note
that Sigmodon minor, which is ubiquitous through more than 3048 meters of
sediment representing 2.0 million years prior to the first appearance of S. lindsayi,
is not simply replaced by the latter species during the time represented by the
Vallecito Creek sediments. Sigmodon lindsayi appears at zone 55.5 (or 53.8), and
persists through zone 57.7, but it then is absent from zone 57.8, at which level
only S. minor is encountered (14 isolated teeth and one mandibular fragment with
M.-M,). At the next highest level, zone 58.8, S. /indsayi occurs once again, without
S. minor.
Although we have no inherent reason to doubt the stratigraphic data associated
NEW PLEISTOCENE COTTON RAT 87
with the specimens that we have studied, the pattern above has not been recorded
from other depositional basins in North America, and we are suspicious that the
S. minor specimens at zone 57.8 may belong to a lower unit. However, if this is
not the case, then the pattern can be explained easily by a combination of com-
petition and climatic modification. Martin (1986) summarized the research on
competition among living cotton rats and their arvicolid analogues, and noted
that one species of cotton rat rarely tolerates the presence of another Sigmodon
or Microtus species, especially if it is small. Those small cotton rats that have
evolved are now extinct, including S. minor. Therefore, it seems likely that as
populations of S. /indsayi became established in the Anza-Borrego area, those of
S. minor diminished. Zone 57.8 could represent a limited area in which S. lindsayi
became locally extinct due to an unknown climatic event, allowing S. minor to
return temporarily. At the periphery of their ranges in Kansas, an interplay of
this sort occurs between Sigmodon hispidus and Microtus ochrogaster (Martin
1986). When winters are cold, populations of S. hispidus die off, allowing M.
ochrogaster to repopulate the area. However, because S. hispidus is the more
dominant species, wherever they are sympatric, S. hispidus generally replaces M.
ochrogaster.
Acknowledgments
We greatly appreciate the loan of specimens facilitated by S. A. McLeod from
the Los Angeles County Museum, and the helpful information, maps and insights
provided by T. Downs and J. A. White. The comments of an anonymous reviewer
also greatly improved the manuscript. This research was supported in part by a
faculty development grant from Berry College.
Literature Cited
Czaplewski, N. J. 1987. Sigmodont rodents (Mammalia; Muroidea; Sigmodontinae) from the Plio-
cene (Early Blancan) Verde Formation, Arizona. Jour. Vert. Paleo, 7:183-199.
Downs, T., and J. A. White.. 1968. A vertebrate faunal succession in superposed sediments from
Late Pliocene to Middle Pleistocene in California. Pp. 41-47 in ‘“‘Proceedings X XIII Interna-
tional Geol. Congress, Sec. 10, Tertiary-Quaternary Boundary,’’ Academica Press, Prague.
Hershkovitz, P. 1962. Evolution of neotropical cricetine rodents (Muridae) with special reference
to the phyllotine group. Fieldiana:Zoology, 46:1-524.
Martin, R. A. 1979. Fossil history of the rodent genus Sigmodon. Evolutionary Monographs, 2:1-
36.
1984. The evolution of cotton rat body mass. Pp. 179-183 in Contribs. Quater. Paleo.: a
volume in memorial to John E. Guilday. (M. H. Genoways and M. R. Dawson eds.), Carnegie
Mus. Nat. Hist., Special Pub. No. 8, Pittsburgh.
1986. Energy, ecology and cotton rat evolution. Paleobiology, 12:370-382.
Opdyke, N. D., E. H. Lindsay, N. M. Johnson, and T. Downs. 1977. The paleomagnetism and
magnetic polarity stratigraphy of the mammal-bearing section of Anza Borrego State Park,
California. Quat. Research, 7:316—329.
Tomida, Y. 1987. Small mammal fossils and correlation of continental deposits, Safford and Duncan
Basins, Arizona, USA. National Sci. Mus., Tokyo, 1-141.
Van der Meulen, A. J. 1978. Microtus and Pitymys (Arvicolidae) from Cumberland Cave, Maryland,
with a comparison of some New and Old World species. Annals Carnegie Mus., 47:101-145.
Accepted for publication 5 January 1989.
Bull. Southern California Acad. Sci.
88(2), 1989, pp. 88-92
© Southern California Academy of Sciences, 1989
Research Note
Collective Vigilance Enhances Feeding Rates of The Opaleye
Girella Nigricans (Girellidae)
The benefits of schooling for both predator and prey fish have been well doc-
umented. Fish in schools are preyed upon less frequently than solitary individuals,
and schools of predatory fish feed more efficiently (Neill and Cullen 1974; Bertram
1978; Major 1978; Pitcher 1986). The benefits of collective vigilance in schooling
fish have been that their members are able to feed, clean, and conduct other
behaviors in relative safety (Pitcher 1986). Collective vigilance in birds has been
studied extensively (Vine 1971; Powell 1974; Siegfried and Underhill 1975; Laz-
arus 1979). These studies indicate that individuals in groups are preyed upon less
frequently than solitary individuals. These findings are similar to those of anal-
ogous fish studies (e.g., Neill and Cullen 1974; Major 1978). Additionally, Sullivan
(1984) found that Downy woodpeckers feed at higher rates in flocks than while
solitary. It follows that schooling prey fish would also benefit from the survival
value of collective vigilance to enhance feeding rates.
Girella nigricans, a facultative schooling fish (as defined by Breder 1967 and
Shaw 1970), was studied in the field to determine if collective vigilance of aggre-
gated conspecifics enhanced the feeding rates of facultative schools when compared
to solitary fish. G. nigricans is an abundant herbivorous fish (Mitchell 1953) found
in the intertidal zone and kelp beds from Baja California to San Francisco (Miller
and Lea 1972). G. nigricans is a natural prey item for such predators as the sea
lion, Callorhinus ursinus (Smith et al. 1980, 1981) and the cormorant, Phalocro-
corax pelagicus (Ainley et al. 1981 and personal observation).
To test the hypothesis of enhanced feeding rates, I observed individual Girella
nigricans in groups of various compositions: solitary, small groups (2—6 members),
and facultative schools (more than 6 members). G. nigricans of 6 to 9 cm total
length (TL) were observed because they consistently maintained a smaller home
range than the larger conspecifics (pers. obs.). The observations were made while
snorkeling at depths of | to 3 m at the rock jetty in Big Fisherman’s Cove, Santa
Catalina Island. Data were collected in the morning and afternoon during two
weeks in November 1985, and one week in May 1986. A solitary individual G.
nigricans or an individual within a facultative school was chosen for observation,
approached slowly, with a minimum of surface disturbance, and followed. Feeding
rates were measured in bites per minute (bpm) and collected during 3 to 5 minute
periods. Data were recorded at pre-measured distances of 1.0, 1.5 and 3.0 m to
determine diver-induced feeding interference. I speculated that a diver in a dark
wet suit would imitate the appearance ofa predator which could inhibit the feeding
rates of the fish.
To confirm dietary composition and food abundance, foregut analysis was
performed on 15 G. nigricans. Foregut contents were preserved in a 10% formalin
solution within one hour of capture, and analyzed under Baush and Lomb dis-
88
RESEARCH NOTE 89
Table 1. Feeding rates of solitary Girella nigricans at different distances from a diver. DISTANCE
= the distance from observer to G. nigricans, AVG. BPM = the average bites per minute for an
individual, S.D. = standard deviation, N = number of observations.
DISTANCE (m) AVG. BPM S.D. N
1.0 12.60 5.25 9
1.5 17.10 3.37 9
3.0 21.10 6.09 9
secting microscopes. Algae were identified with the use of Abbot and Hollenberg
(1982).
Correlation analysis was employed to analyze feeding rates of aggregated G.
nigricans. Two way analysis of variance without replication, was used for deter-
mining diver-induced effects on feeding rates of solitary individuals and facultative
schools at specific distances. Additionally, unpaired t-tests were employed to
compare feeding rates of solitary and aggregated fish.
Solitary Girella nigricans were wary, easily alarmed, and difficult to observe.
Some were quick to join small groups or nearby facultative schools. Solitary G.
nigricans fed at the fastest rate (21.1 bpm) when diver distance was 3.0 m (Table
1). As observation distance decreased, the feeding rate decreased significantly (two
way analysis of variance, P < 0.05., Table 2). Solitary fish would flee or hide
among the rocks when approached to 1.0 m. Therefore, subsequent data were
collected at 3.0 m.
Small groups (2-6 members) of G. nigricans formed when one or two individuals
separated from a facultative school, frequently attracting one or two others. Group
size varied constantly. Small groups were usually joined by a facultative school,
another small group, or an individual. The small groups would remain distant
from the original school for one to two minutes. Accurate data could not be
recorded because group size was never consistent for the length of time required
to adequately collect data.
Facultative schools of G. nigricans (7 to 37 members) were less wary than
solitary individuals or small groups and could be approached to approximately
0.6 m before diver-induced interference disrupted feeding behavior. All subse-
quent data were collected at 3.0 m, to be consistent with solitary data. There were
no significant difference between feeding rates of individuals within facultative
schools at varying distances; i1.e., two way analysis of variance, 1.0 m, 1.5 m, and
3.0 ma, JP SOLOS!
Individual members of facultative schools fed at significantly higher rates than
Table 2. Two way analysis of variance, without replication, for solitary Girella nigricans. Distances
were 1.0, 1.5 and 3.0 m. F-tests were calculated at the 0.05 level.
Source df SS MS F P.
Fish 8 265.0 33.1 1.46 >0.05
Distances D) 321.2 160.6 7.A1 <0.05
Error 16 360.8 22.6
Total 26 947.0
90 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
40
ey
O
Dw)
O
Bites per minute
O
O 10 20 30 40
Group size
Fig. 1. Group size or numbers of individual Gire//a nigricans per group and bites per minute. Each
dot represents an average bites per minute for individual within the group.
solitary individuals (t-test, P < 0.05, N = 30, Table 3). As facultative schools
increased in size, the average bpm for individuals within the school increased
(Fig. 1). Group size significantly affected individual feeding rates within the school
(r = 0.475, P < 0.05, N = 18, Fig. 1).
The analysis of foregut contents determined that the food source for G. nigricans
was readily abundant during the study. The diet of G. nigricans consisted of algae
within the following genera: Ralphsia, Pseudolithoderma, Giffordia, Gelidium,
Enteromorpha, and Ulothrix. Due to the semi-digested nature of the algae, iden-
tification to species was impossible. These algae were consistent with the seasons
and location of the study.
The data in this study clearly demonstrated that feeding rates increased signif-
icantly as group size increased in facultative schools of Girella nigricans. Addi-
tionally, the feeding rates of solitary G. nigricans were significantly lower than
those within facultative schools (Table 3). These results imply that the collective
vigilance of facultative schools of G. nigricans allowed individual members to
spend more time feeding as compared to solitary fish. These findings are consistent
with those of Pitcher (1986), who found that members of a group reduced their
vigilance level and allocated more time to feeding, and Sullivan (1984), who found
Downy woodpeckers fed at higher rates in flocks. In addition, Godin et al. (1988)
found that, in the laboratory, individual vigilance decreased as group size in-
creased. Previous studies performed to determine the benefits of schooling in fish
focused on: The preventing of territoriality (Robertson et al. 1976); the deflection
of predation (Neill and Cullen 1974; Bertram 1978; Major 1978; Pitcher 1986);
and collective vigilance (Godin et al. 1988). The study of enhanced feeding rates
RESEARCH NOTE 91
Table 3. Feeding rates for Girella nigricans, observed at a distance of 3 m. FISH # = the fish
number, #/GROUP = the number of fish in a group, either | or more, AVG. BPM = average bites
per minute, S.D. = the standard deviation, N = the number of observations per fish.
#/GROUP AVG. BPM S.D. N
Solitary
1 11.30 D5 4
1 11.50 1.00 4
1 9.30 5.50 3
1 16.80 3.59 4
1 13.30 4.57 4
1 8.00 1.73 3
l 23.80 4.21 5
1 12.70 6.25 6
1 13.70 1.89 ff
1 15.80 3.49 5
l 17.20 4.87 5
1 11.50 5.97 4
Grouped
Dy 29.30 3
20 27.30 6.65 3
15 31.00 6.02 2
25 26.00 2.83 1
30 35.50 — 4
7 25.50 4.79 4
37 34.60 1.29 5
17 13.00 9.02 2
8 24.00 6.00 3
9 19.00 6.70 2
34 29.50 3.87 2
15 27.00 7.65 2
35 20.80 2.50 4
30 29.20 4.29 9
10 . 25.40 D2} 8
23 22.60 4.88 5
13 26.00 _ 1
7 19.20 1.79 5
as an additional benefit of schooling in prey fish is a relatively new concept;
paralleled, however, by those studies performed on birds (Vine 1971; Sullivan
1984) which draw similar conclusions of enhanced feeding rates as a direct benefit
of collective vigilance. Therefore, the results of those studies support the hypoth-
esis and results of this study indicating that the collective vigilance of a facultative
school of G. nigricans significantly enhanced the feeding rates of individuals within
the school.
Acknowledgments
I wish to thank William Hamner for his support during the project. I thank Lin
Shannon, William Hamner, and Brian White for their comments on earlier drafts
of this paper. I additionally would like to thank the reviewers for their comments
on the manuscript.
92 SOUTHERN CALIFORNIA ACADEMY OF SCIENCES
Literature Cited
Abbott, I. A., and G. J. Hollenberg. 1982. Marine alae of California. Stanford University Press.
Stanford, California.
Ainley, D. G., D. W. Anderson, and P. R. Kelly. 1981. Feeding ecology of marine cormorants in
south western North America. Condor, 83:120-131.
Bertram, B. C. R. 1978. Living in groups: predators and prey. Pp. 64-96 in Behavioural ecology:
and evolutionary approach. (J. R. Krebs and N. B. Davies, eds.), Blackwell Scientific Publi-
cations, Oxford.
Breder, C. M. Jr. 1967. On the survival value of fish schools. Zoologica, 52:25—40.
Godin, J.-G. J., L. J. Classon, and M. V. Abrahams. 1988. Group vigilance and shoal size in a small
characin fish. Behaviour, 104:29-40.
Lazarus, J. 1979. The early warning function of flocking in birds: an experimental study with captive
quelea. Anim. Behav., 27:855-865.
Major, P. F. 1978. Predator-prey interactions in two schooling fishes, Caranx ignobilis and Stole-
phorus purpures. Anim. Behav., 26:760-777.
Miller, D. J., and R. N. Lea. 1972. Guide to the coastal marine fishes of California. Cal. Fish &
Game. Fish. Bull. 157.
Mitchell, D. F. 1953. An analysis of the stomach contents of California tide pool fish. Am. Midl.
Nat., 49:(3)862-871.
Neill, S. R. St. J., and J. M. Cullen. 1974. Experiments on whether schooling by their prey affects
the hunting behavior of cephalopods and fish predators. Zool. Lon., 172:549-569.
Pitcher, T. J. 1986. Functions of shoaling behaviour in teleosts. Pp. 294-337 in The behavior of
teleosts fishes. (T. J. Pitcher, ed.), John Hopkins University Press, Baltimore.
Powell, G. V. N., 1974 Experimental analysis of the social value of flocking by starlings (Sturnus
vulgaris) in relation to predation and foraging. Anim. Behav., 22:501-505.
Robertson, D. R., H. P. A. Sweatman, E. A. Fletcher, and M. G. Cleland. 1976. Schooling as a
mechanism for circumventing the territoriality of competitors. Ecology, 57:1208—1220.
Shaw, E. 1970. Schooling in fishes: critique and review. Pp. 452—480 in Development and evolution
of behavior. (L. R. Aronson, E. Tobach, D. S. Leharman, and J. S. Rosenblatt, eds.), W. H.
Freeman and Co., San Francisco.
Siegfried, W. R., and L. G. Underhill. 1975. Flocking as an antipredator strategy in doves. Anim.
Behav., 23:504—505.
Smith, A. W., D. E. Skilling, and R. J. Brown. 1980. Preliminary investigation of a possible lung
worm (Paragilaroides decorus), fish (Girella nigricans), marine mammals (Callorhinus ursinus)
cycle for San Miguel seal lion virus type 5. Am. J. Vet. Res., 41(11):1854-1850.
—., D. E. Skilling, and A. H. Dardiri. 1981. Calcivirus pathogenic for swine: a new serotype
isolated from opaleye Girella nigricans, an ocean fish. Science (Wash.), 209(4459):840-841.
Sullivan, K. A. 1984. The advantages of social foraging in downy woodpeckers. Anim. Behav., 32:
16-22.
Vine, I. 1971. Risk of visual detection and pursuit by a predator and the selective advantage of
flocking behaviour. J. Theor. Biol., 30:405-422.
Accepted for publication 3 March 1989.
Michael Mishima Shannon, Department of Biology, California State University
Long Beach, Long Beach, California 90840.
ta
sh
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CONTENTS
Bryozoans, Hermit Crabs, and Gastropods: Life Strategies Can Affect the
Fossil Record By Penny A. Morris, Dorothy F. Soule, and John D.
SOULE. SOE ONT RIE NA 7A VOR oi BUN Wea eee eC 45
Seaweeds and Seagrasses of Southern California: Distributional Lists for
Twenty-one Rocky Interridal Sites By Steven N. Murray and Mark
U.S Cae SL | SRE NU OS antetn AOE, GRAAL aN UNNI aMur cen ee 61
A New Species of Early Pleistocene Cotton Rat from the Anza-Borrego
Desert of Southern California By Robert A. Martin and Robert H.
PETC O iiss decay 1 ehh cd Ne OE Ns se ee toad AR Ne dE 80
Research Note
Collective Vigilance Enhances Feeding Rates of the Opaleye Girella Nigricans (Girellidae) By
Michael’\Mishima: Shannon 222) AE ee ee 88
LIBRARY
APR - 2 1996
NEW YORK
BOTANICAL GARDEN
COVER: Hippothoa hyalina, a cheilostome bryozoan which encrusts gastropod shells of Tegula
funebralis inhabited by the hermit crab Pagurus samuelis. Colony shows large females with
perforate brood chambers (ovicells), autozoids with apartures having a U-shaped proximal
sinus, and miniature male zooecia.
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