The role of sea urchins in mediating fish predation on a commensal isopod (Crustacea: Isopoda)

J, Exp. Mar. Eiol. EC&, 1988, Vol. 124, pp. 97-113 Elsevier

91

JEM 01179

The role of sea urchins in mediating fish predation on a commensal isopod (Crustacea : Isopoda) Timothy D. Stebbins In~~ertebrateZoology Section, Natural History Museum of Los Angeles County. Los Angeles, ~al~ornia~ U.S.A. ; department of Bjolo~ca~ Sciences, Universj~ ofSouthernCa~~rnia, Los Angeles, Caf~miu, U.S.A. (Received 21 March 1988; revision received 22 August 1988; accepted 1 September 1988) Abstract: Colidoteu rostruta (Benedict, 1898) is a common isopod in low intertidal areas of the southwestern IJ.S.A. and Baja California, Mexico. This isopod is an obligate commensal, living on and mimicking the color of two Pacific coast sea urchins, Strongylocentrotuspurpuratus Stimpson and S. franciscanus Agassiz. Fish stomach analyses and a field caging experiment indicate that, although C. rostrata is preyed upon by fishes, fish predation has little effect on natural populations of this isopod. Most isopods escape detection due to their cryptic nature and, if detected, are protected from predators by an urchin spine response. In the laboratory, more isopods occur on the exposed aboral regions of urchins during nighttime hours than during daylight. This diurnal behavior may be an indirect antipredator response, since cryptic isopods are less visible to visual predators at night. Laboratory predator inclusion experiments reveal that urchins significantly reduce fish predator success on C. tostrata, regardless of host urchin species or size. Isopods escape predation better on larger urchins than on smaller urchins, although predator success is not affected by spine length in itself. Urchins provide C. rostrata with an important refuge from fish predation. This protection is mediated by several factors, including cryptic coloration, isopod behavior, urchin behavior, urchin size, and predator foraging behavior. Key words: Colidotea rostrata; Commensal; Fish predation; Isopod; Sea urchin INTRODUCTION

Predation is known to be an important structuring agent in many animal and plant communities. In recent years, many studies have examined the effects of fish predation in various aquatic co~u~ties (e.g., Nelson, 1979a, 1981; Stoner, 1979; Grossman et&., 1980; Russ, 198O;Coene~uZ., 198l;H~ck&Thoman, 198l;Boothet~~., 1985; Posey, 1986; Main, 1987). Crustaceans, especially amphipods, isopods, and decapods, are the dominant prey for many fish species in various marine habitats (e.g., Mitchell, 1953; Quast, 1968; Hobson, 1974; Hobson & Chess, 1976; Christensen, 1978; Nelson, 1979a; Stoner, 1979; Coen etal., 1981; Eschmeyer etal., 1983). A number of recent authors has examined the roles that factors, such as habitat complexity, cryptic coloration, prey behavior, and predator behavior, play in mediating fish predation (Kislalioglu & Gibson, Correspondence address: T.D. Stebbins, Invertebrate Zoology Section, Natural History Museum of Los Angeles County, Los Angeles, CA 90007, U.S.A. 0022-0981~88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

T.D.STEBBINS

98

1976; Stoner, 1979, 1982; Heck & Orth, 1980; IIeck & Thoman, 1981; elements & Livingston, 1984; Main, 1985, 1987; Russo, 1987). The importance of predation to crustacean evolution has also been discussed (e.g., Heck & Wetstone, 1977; Brusca & Wallet-stein, 1979; Nelson, 1979a, b; Stoner, 1979; Wallerstein & Brusca, 1982). Symbiotic relationships are extremely important within the crustaceans, having evolved in virtually every major group (Ross, 1983). Predation pressure may have been an important force driving the evolution of many of these associations. Sea urchins provide a habitat for several types of small crustaceans, including amphipods (McCloskey, 1970, 1971), isopods (Harty, 1979; Lee & Miller, 1980), shrimp (Lewis, 1958; Hipeau-Jacquotte, 1965; Chace, 1969; Bruce, 1972, 1973, 1976; Criales, 1984; Patton et al., 1985), and crabs (Hyman, 1955; Schm~us, 1976; Ross, 1983). Although the degree of association between crustacean and urchin is often not well known, the urchins are generally assumed to provide their associates with a refuge from predation (McCloskey, 1970, 1971; Bruce, 1976; Schmalfus, 1976; Harty, 1979). However, this protection has not been empirically studied. Colidotea rostrata (Benedict, 1898) is a commensal isopod living on and mimicking the color of two eastern Pacific sea urchins, StrongylocentrotuspurpuratusStimpson and S. franciscanus Agassiz. The isopod ranges from southern California, U.S.A., to northwestern Baja California, Mexico (Brusca & Wallerstein, 1979). In spite of numerous ecological studies on the genus St~on~~ace~trotus (see Durham et al., 1980; Tegner & Dayton, 198 1; Coyer et al., 1987; Russell, 1987; and references therein), little attention has been paid to the isopod symbionts of these urchins. Pilot studies revealed that, although C. rostrata may be abundant in many low intertidal areas, the isopods are underrepresented in the diets of fish predators. The present study examines the effects of fish predation on the symbiotic relationship between Colidoteu rostrutuand its urchin hosts. It is the first study quantifying the effects of fish predation on a symbiotic isopod. Field and laboratory observations, and experiments, address several questions. (1) Which fish species may be significant predators on C. rostrata, and how do the foraging behaviors of these fishes affect predation? (2) Do isopods show any behavioral responses (e.g., microhabitat shift) to the presence of predators? (3) What role do urchins play in mediating fish predation on C. rostrata? (4) How do such factors as urchin species, size, and spine length affect predation on C. rostrata by fishes.

MATERIALS STUDY

AND METHODS

SITE

All collections and field studies were conducted at a rocky intertidal area at the southwestern end of Lunada Bay, Pales Verdes, southern California (33”40’N: 118”3O’W). The low intertidal zone at Lunada Bay consists of a rock bench with overlying basalt boulders. The specific study site is characterized by large

FISH PREDATION ON A COMMENSAL ISOPOD

99

aggregations of the purple sea urchin Strongylocentrotuspurputatus and the kelp Egregia menziesii (Turner) Areschoug. Red urchins S.~ancisca~us also occur but in low numbers. The adjacent seaward area from the study site is a rocky reef covered with the surfgrass Phyllospadix scouieri Hooker. Large forests of the giant kelp Macrocystis pyrifera (L.) C. Agardh occur offshore; this kelp bed is a constant source of drift algae to the intertidal zone. EXPERIM~~AL

ORGANISMS

Colidotea rostrata and sea urchins, Strongylocentrotusptqmratus, S. franciscanus, were

collected between March and August 1987 and were transported to the laboratory in buckets of seawater. Animals were maintained in a 285-l recirculating seawater table at 14-17 “C prior to expe~entation. Isopods and sea urchins were fed brown algae, primarily Egregib ~en~iesii or Macrocys~s pyrifera collected from the study site. Fresh algae were replenished as necessary and were available at all times. Intertidal fish collections were made periodically at the study site by adding at 10% solution of quinaldine in ethanol to tidepools. Anesthetized fishes were collected with dip nets and transported to the laboratory in buckets of clean seawater. Fishes of four species were collected: woolly sculpins Cli~ocot~s analis Girard, spotted kelpfish Gibbonsia elegans (Cooper), juvenile opaleyes Girelfa nigricans (Ayres), and rockpool blennies Hypsoblennius gilberti (Jordan). Fishes were maintained in the seawater system separate from the urchins and isopods by perforated Plexiglas partitions or in separate holding tanks. Prior to experiments, fishes were maintained on a diet of shrimp or squid. Fishes sacrificed for stomach analyses were preserved in a 10% formalin solution within 2 h of collection, at which time their stomachs were injected directly. After 2 days, these fishes were transferred to 70% ethanol. Stomachs were later dissected out and their contents examined using a dissecting microscope. LABORATORY OBSERVATIONS

Fishes used for laboratory observations were maintained in a 190-l aquarium at 17 ’ C and deprived of food for 24 h prior to each experiment. Observations of predator behavior were made from behind a blind to avoid disturbing the predators. Each trial consisted of adding a single urchin, Strongylocentrotus purpuratus or S. franciscanus, inhabited by seven to ten isopods to the experimental tank cont~ning two to three fish. Observations continued for 10 min during which time the foraging behavior and feeding success of each fish species were qualitatively recorded. Five trials were run for each urchin species with each of the four fish species. MICROHABITAT

SELECTION EXPERIMENT

The distribution of Colidotea rostrata on urchins was monitored to determine if isopods shift position (microhabitat) in response to predator presence or light cues.

100

T. D. STEBBINS

Four 19-1 seawater control

aquaria

were used, two experimental

tanks (fish present)

and two

a “light” treatment

and the

tanks (no fish). One tank of each was designated

other a “dark” treatment.

20-25 isopods were distributed

between four urchins in each

tank and allowed to acclimate for 24 h. Two fish predators (Clinocottus analis) were then added to each experimental tank. The “dark” treatment tanks were immediately covered while the “light” treatment tanks were left exposed to ambient light. After 2 h, the number of isopods was recorded on (1) the “protected” oral surfaces of urchins and (2) the “exposed” treatment. LABORATORY

aboral

FEEDING

regions

of urchins.

Five trials

were conducted

for each

EXPERIMENT

All laboratory animals were transferred to 55-1 holding tanks at least 2 days prior to experimentation. Experiments were conducted in rectangular 19-1 aquaria filled with seawater. All holding and experimental tanks were well aerated and maintained at 17 “C. A 12: 12 h light-dark regime was maintained throughout the experiments. Seawater was changed in all experimental tanks between replicate trials. In order to evaluate which fishes might be significant isopod predators, a series of feeding experiments was carried out. Fishes tested were Clinocottus analis, Gibbonsia elegans, Girella nigricans, and Hypsoblennius gilberti. For each fish species tested, five isopods were placed in an experimental tank and a single fish then introduced. The number of replicates per experiment varied from three to five depending on fish availability. Predators were allowed to feed for 24 h, after which time the number of isopods consumed was recorded. LABORATORY

PREDATOR

INCLUSION

EXPERIMENTS

A series of predator inclusion experiments were conducted to test several hypotheses: (1) that survivorship from predation is greater for isopods on host urchins (Strongyfocentrotuspurpuratus, S. franciscanus) than for isopods without hosts; (2) that survivorship under predation varies with host species and host size (Table I); and (3) that survivorship under predation is a function of host spine length. Clinocottus analis was the fish predator used in all predator inclusion experiments because of its availability. Fish ranged in size from 6.6 to 10.2 cm, with a mean length of 7.9 cm (SD = 0.9, N = 49). All fish were starved for 24 h before each experiment. No fish was used in more than three trials nor was any fish used in successive replicates. Rocks and kelp were provided in each treatment as an alternate substratum (refuge) and food for isopods and urchins. The number of isopods per treatment was determined based on natural isopod densities and availability. In order to determine the effect of host presence or absence, host species, and host size in mediating fish predation on Colidotea rostrata, there were five treatments, each with 15 replicates: two small or two large Strongylocentrotus purpuratus, two small or two large S. franciscanus, and no urchins. Each experiment began by adding eight

FISH PREDATION ON A COMMENSAL ISOPOD isopods

101

(length > 5 mm) to each of the experimental tanks. After 1 h, one Cl~nocott~s

analis was added to each of the 1.5replicate tanks. Experiments ran for 48 h, after which

the number of isopods surviving in each tank was counted. Six replicate controls (no fish) for each treatment controlled for isopod mortality due to natural death and predation by the urchins. TABLE

I

Sizes of sea urchins, StrongyZocentrotusspp.,used in laboratory predation experiments. Test diameter and spine length data are expressed as mean + 1 SD (mm). Numbers in parentheses = N. Total diameter = (mean test diameter) + (2 x mean spine length). Surface area estimates calculated based on total diameter values. Species

S. purpuratus

(small) S. purpuratus Wge) S. franciscanus

(small) S.franciscanu.7 (law)

Test diameter (mm)

Spine length (mm)

21.4 + 4.4 (12) 50.8 f 4.8 (12) 36.0 & 5.8 (8) 64.8 + 6.9 (8)

9.0 + 1.9 (30) 12.5 + 1.1 (30) 19.6 + 4.6 (30) 29.7 ?r 3.0 (30)

Total diameter (mm)

Surface area (mm*)

45.4

2158

75.8

6017

75.2

5922

124.2

16154

To test the hypothesis that urchin spine length may si~i~~~tly tiect predation by fish on isopod prey, isopods were placed in aquaria on sea urchins with or without intact spines. Only large Strongylocentrotus fpanciscanus (see Table I) were used as hosts. Experimental urchins had all of their spines clipped with scissors to < 10 mm in length, while control urchins had intact spines averaging z 30 mm in length. As a control for possible effects of clipping the spines, the “unclipped” urchins had the tips of their spines nicked with scissors. Urchins were monitored for 3 days prior to the experiment to determine if “clipping” caused any adverse effects. No effect was observed. Seven isopods were placed on one urchin in each of 10 replicates per treatment. Three replicate controls (no fish) per treatment controlled for isopod mortality not due to fish predation. After 2 h, one fish predator was added to each aqu~ium. The expe~ment ran for 48 h, after which the number of surviving isopods in each replicate was counted. FIELD PREDATION EXPERIMENT

A predator exclusion experiment was carried out in July and August 1987 at Lunada Bay in order to assess the significance of fish predation on field populations of Colidotea rostrum Cages were constructed of 0.5-cm mesh galvanized steel, 22.5 x 22.5 cm square, and 7.5 cm in height. The cages were bolted to square cement stepping stones (30 x 30 x 5 cm) and wedged between boulders at the study site (Fig. 1). The experiment consisted of two treatments: “closed” expe~ent~ cages (predator exclusion) and

102

T.D.STEBBINS

“open” control cages (predator exposure). The “open” cages had rectangular openings (4.3 x 3.2 cm) in their sides and tops which allowed access by tish predators, yet prevented escape of the enclosed urchins. Observations of cages in place for 2 wk prior to the experiment indicated that urchins could not escape, and that the cages had no

Fig. 1. Experimental (predator exclusion) and control (predator exposure) cages at Lunada Bay, Pales Verdes, California. Cages measure 22.5 x 22.5 x 7.5 cm with 0.5-cm mesh. Rectangular openings in control cages measure 4.3 x 3.2 cm.

adverse effects on the enclosed urchins and isopods. Also, intertidal fishes were observed freely entering and exiting the “open” cages. Four urchins (Strongylocentrolus purpuratus) with algae were placed in each cage and allowed to acclimate for 1 day. On the following day, 15 isopods (length > 5 mm) were placed in each cage, distributed between two of the four urchins. These numbers were chosen to simulate natural field habitation rates and isopod densities. The experiment was conducted for 11 days with 10 replicates per treatment. The caged urchins and isopods were collected at the end of the experiment and returned to the laboratory for counting.

RESULTS PREDATOR BEHAVIOR

The four fish species collected at the study site differed in their diets (Table II) and abundance. Most abundant were the sculpin CIin~co~~~ analis and juvenile opaleye

103

FISH PREDATION ON A COMMENSAL ISOPOD

Gire2lu nigricans. More rarely collected were the kelpfish Gibbonsia elegans and the blenny Hypsoblennius gilberti. Laboratory feeding experiments indicated that C. analis, G. elegans, and H. gilberti would be significant predators on Colidotea rostrata since they TABLE II Natural diets of four fish species collected at Lunada Bay, Palos Verdes, California: sculpin, Clinocottus analis; kelptish, Gibbonsia elegans; blenny, Hypsoblennius gilberti; opaleye, Girella nigricans. Data are expressed as the percentage of stomachs examined containing each prey type. Fish species

Prey S&pin (N = 36) Crustacea Amphipods Isopods Tanaids Decapods Decapod larvae Mollusca Chitons Limpets Polychaeta Echinode~ata Fish Algae Empty stomachs

69 25 (8)* 6 25

Kelpflsh (iv= 8)

2858(13)’

Blenny (N=6)

Opaleye (N== 15)

33

13

33 17

7

33 33

60 33

6 3 6 11 6 3 6 8

13 13

* Colidotea rostrata.

all consumed between 87 and 100% of the available isopods (Table III). Of these three species, Colidotea rostrata occurred only in the natural diets of C. analis and G. elegans. ‘The predominately herbivorous opaleye, G. nigricans, consumed no isopods. The sculpin Clinocottus analis is a very abundant and opportunistic predator at the study site. Sculpins frequently captured isopods and other small invertebrates dislodged TABLE III Percentages of isopod prey (Colidotea rostrum) consumed by four fish species during laboratory feeding experiment. Fishes were collected from low intertidal sea urchin beds at Lunada Bay, southern California. Experiments ran for 24 h with one fish predator and five isopods per replicate. Species Clinocottw analis Gibbonsia elegans Hypsoblennius gilberti Girella nigricans

Prey consumed (%I

No. of replicates

100

5

100 87 0

3 3 4

T. D. STEBBINS

104

in the field. In the laboratory, sculpins readily attacked isopods living on either species of sea urchin. The frequency or success of attacks was not affected by urchin species. Sculpins would approach an urchin and swim around it until an isopod was visually detected. When attacking, a fish would make a short thrust from 1 to 2 cm beyond the urchin spine tips. Although fish strikes were frequently blocked by the spines, isopods on or near the spine tips were often captured. In contrast, isopods at the base of the spines or on the urchin’s tests were seldom captured. In addition, any isopods not captured or injured by a sculpin’s first strike were usually protected from further attacks by the urchin’s spine response. Once attacked, an urchin’s spines would converge towards the point of attack, thus shielding the area and any isopods from further fish strikes, Isopods crawling freely on the bottom of the aquarium or sinking through the water column were quickly eaten. Motionless or dead isopods were often ignored initiaiiy, although they would eventually be consumed. The kelp&h Gibbunsja ejegans was rarely collected at the study site, however, it was a very efficient predator on Colidotea rostrata in the laboratory. Virtually every isopod detected by a kelpfish was successfully captured. The attack behavior of G. elegans differed markedly from Clinocottus analis. When attacking, a kelpfish would wedge its head between the urchin’s spines until it was fi: I cm from the detected isopod. The kelpfish would then capture the isopod with a quick thrust. These attacks were virtually 100% efficient. Kelplish also readily consumed any isopods not on urchin hosts. The blenny Hypsoblennius gilberti is not a likely predator of Colidotea rostrata under natural conditions. Although H. gilberti consumed free-crawling isopods in the laboratory, blennies were never observed to attack isopods on urchins. In addition, no isopods were found in the natural diets of this fish (Table II). MICROHABITAT

SELECTION

The distribution of Colidotea rostrata on urchins was affected by light and not by the presence of predators (Fig. 2). Isopods showed no significant preference for either protected or exposed regions of urchins in the “light” treatments whether fish were present or not. However, slightly more isopods occurred on protected areas than exposed areas in both of these light treatments. In contrast, isopods occurred on exposed urchin surfaces significantly more often when in the dark, regardless of predator presence or absence. > 70% of the isopods occurred on these exposed surfaces in both “dark” treatments. LABORATORY

PREDATION

EXPERIMENTS

No significant mortality of Colidotea rostrata (< 2%) was observed in the control tanks during the 48-h laboratory experiments. Thus, differences in isopod survival between treatments is attributed to predation by the predatory fish Ciinocott~sanalis and not to natural death or predation by urchins. Sculpins fed readily on isopods in all of the laboratory predation experiments,

105

FISH PREDATION ON A COMMENSAL ISOPOD

although predator success varied between treatments. There were highly significant differences in the mean numbers of isopods surviving predation among treatments (no urchin, small or large Strongylocentrotus purpuratus or S. franciscanus) in the predator X2=61.6 + (117) -

100 90 80 70 60

x2 =I.3 (114)

LQZQ Protected x2=21.0

60 50 40 30 20 10 0

L

(116)

l

m

Exposed

FISH PRESENT

Dark

,ight TREATMENT

Fig. 2. Results of microhabitat selection experiment. Data are expressed as the relative frequency ofisopods (Colidotea rostrata) occurring on protected (oral) and exposed (aboral) surfaces of sea urchins in experimental (fish present) and control (no fish) tanks during light and dark treatments. xy values are indicated; * significant at P < 0.05. N, numbers in parentheses.

inclusion experiment (P < 0.001, one-way ANOVA; Fig. 3). The presence of an urchin host resulted in increased survivorship of Colidotea rostrata. Only 10% of those isopods without a host survived predation, and all of these isopods were restricted to refuges under rocks. The size of the urchin host and not host species affected isopod survival. Survivorship was 40% for isopods on the smallest sea urchins (small S. purpuratus), which was significantly less than the 64-73 y0 survival for isopods on large S. purpuratus or small or large S. franciscanus (P < 0.05; Student-Newman-Keuls test). There were no significant differences between these three latter urchin treatments (P > 0.05; Student-Newman-Keuls test).

106

T. D.STEBBINS

Differences in isopod survival on urchins of different sizes is a function of overall size (Table I) and not of spine length. The mean numbers of isopods consumed on large red urchins, Strongylocentrotus franciscanus, with intact spines vs. clipped spines did not

m

:

Et

(5 1

60so40-

T

i

r

T

NU

SSP

LSP

SSF

LSF

TREATMENT Fig. 3. Comparisons of mean isopod (Colidotea rostruta) survival for predator inclusion experiment. Treatments represent host urchin manipulations: NU, no urchin; SSP, small S~ongylocentrotuspurpuru~s; LSP, large S. purpuratus; SSF,small S.~anciwznus;LSF,large S. franciscanus. Data are expressed as mean percent survival of isopods + 1 SE. Intervals which do not overlap are significantly different (P < 0.05; Student-Newm~-Keuls test).

differ from one another (Fig. 4); this result was unexpected. In addition, large “clipped” S. franciscanus had spines approximately equal in length to spines of small S. pulpuratus (x 10 mm). However, 8 1% of the isopods survived predation in the S. franciscanus experiment compared to only 40% in the small S. pulpuratus experiment.

Q

100 90

z

80

5 5 z

70

g 8

40 30

vr . 4

20

50 60

IO 0

CTRL

EXPT

TREATMENT Fig. 4. Mean number of Colidotea rostrata surviving fish predation on sea urchins (S. fran&canus) with intact spines (GIRL) and with clipped spines (EXPT). Data are expressed as mean percent survival of isopods + 1 SE.

FISH PREDATION ON A COMMENSAL ISOPOD

107

FIELD PREDATION EXPERIMENT

Results of the field predator exclusion experiment are shown in Table IV. There were no significant differences in the numbers of isopods surviving in the experimental (predator exclusion) vs. control (predator exposure) cages (t = 0.50; P = 0.62). Thus, predation does not significantly atfect field populations of C. rostruta. Not only was TABLE IV

Number of isopods (Colidoteu rostrutu) surviving in field predator exclusion experiment. Experimentals = “closed” predator exclusion cages; Controls = “open” predator exposure cages. Replicate

1

2 3 4 5 6 7 8 9 10 ?iilSE

Number of isopods surviving Controls

Experimentals

14 11 15 16 22 15 14 9 20 15

17 21 7 22 21 15 10 15 13 20

15.1+ 1.2

16.1 f 1.6

predation insignificant, but no evidence of isopod mortality occurred during the I l-day experiment. Although both experimental and control treatments showed slight, but negligible, net increases in total number of isopods, analysis of individual replicates indicated that isopod movement did not differ between experimental and control cages.

The sculpin Cl~n~~tt~s ankle and the kelpfish Gj~~ns~u elegans are natural predators of Colidotea rostrata. Both fishes consumed C. rostrata in the field and laboratory and are known predators of small crustaceans (Mitchell, 1953; Fitch & Lavenberg, 1975). Although observations indicate that these fishes detect their prey visually, their attack behavior differs markedly from one another. Successful predation is largely dependent upon striking behavior, and this behavior is related to predator morphology. Gibbonsia elegans has a narrow and angular head which it can wedge easily between an urchin’s spines before striking. Thus, few isopods detected by G. elegans escape predation. Clinocottus analis, on the other hand, has a much broader and rounded head which cannot be wedged between the spines. Thus, sculpins are largely restricted to capturing

108

T. D. STEBBINS

isopods they can pick off near the spine tips. Despite this restriction, C. analis was capable of preying upon a significant number of isopods during laboratory predation experiments (Fig. 3). Urchin spines provide the isopods with an adequate barrier to fish predation. Even if an isopod is detected by a fish, the predator’s first strike is often repelled by the spines. Subsequent attacks are further thwarted by the urchin spine response, which not only serves to protect the urchin, but also any isopods trapped beneath the converging spines. This spine response has been suggested as serving a protective function for the isopod Manna halei (Harty, 1979) and may protect other urchin associates as well. Results of the predator inclusion experiments show that urchin hosts provide Colidotea rostrata with a significant refuge from predation. Isopods were quickly consumed in experiments when no urchin hosts were present. Although a few isopods did find alternate refuge under rocks, this refuge can only be temporary since isopods without hosts do not feed (Stebbins, 1988, in press a). Also, isopods dislodged from hosts in the field are quickly captured by opportunistic predators. Predation experiments demonstrate that Colidotea rostrata escaped predation better on larger urchins (large Strongylocentrotus purpuratus or S. franciscanus of either size) than on smaller S. purpuratus (Fig. 3). In addition, isopods rarely occurred on small S. purpuratus in the field. Small urchins have shorter spines than larger urchins. Consequently, it was thought that the increased vulnerability to fish predation with decreasing host size was a function of spine length. However, an experiment which tested the effect of spine length on predator success demonstrated that spine length had no significant effect on isopod survival from predation. Thus, one can conclude that C. rostratu living on small hosts are more susceptible to predation because these urchins provide less surface area on which isopods can find refuge. For example, small S. purpuratus have a surface area of x22 cm’, which is considerably less than the 60 cm2 of large S. purpuratus and small S.franciscanus or the 162 cm2 of large S.franciscanus (see Table I). In other words, small urchins represent a less complex microhabitat than do large urchins; isopods are more easily detected and captured in these microhabitats. These results agree with those of others who have shown that the risk of predation increases with decreasing habitat complexity (Heck & Wetstone, 1977; Stein, 1977; Nelson, 1979b; Virnstein, 1979; Russ, 1980; Coen et al., 1981; Heck & Thoman, 1981; Crowder & Cooper, 1982; Stoner, 1982; Leber, 1985; Main, 1987; Russo, 1987). The selection of prey by predators is largely determined by prey accessibility. Many studies have shown that prey accessibility is often affected by prey visibility (e.g., coloration and size), prey behavior, and microhabitat choice (Zaret & Kerfoot, 1975; Kislalioglu & Gibson, 1976; Stein & Magnuson, 1976; Vinyard & O’Brien, 1976; Werner et al., 1977; Vimstein, 1979; Peckarsky, 1980; Vinyard, 1980; Main, 1985, 1987). That cryptic coloration reduces a prey’s vulnerability to predation has been documented in a number of systems (Ruiter, 1952; Robinson, 1969; Den Boer, 1971; Endler, 1978; Main, 1987). Many small invertebrates have evolved cryptic coloration patterns (reviewed in Wicksten, 1983).

FISH PREDATION ON A COMMENSAL ISOPOD

109

Colidotea rostrata closely mimics the dark red to purple pigmentation of its host urchins throughout its entire life cycle. This crypsis is further enhanced by the position and posture of isopods on urchins. Colidotea rostrata spend their time either on the host test where they blend in well with the background, or on the urchin spines. When on spines, the isopods align themselves parallel to the spines with their antennae projecting outwards. Similar parallel orientation has been shown for shrimp living on urchins (Criales, 1984; Patton et al., 1985) or seagrasses (Main, 1987). Furthermore, the terminal flagellar article of the isopod second antennae is usually unpigmented; when viewed from above these antennae resemble the pale tips of the urchin spines. Cryptic coloration is a common occurrence among other isopods (e.g., Moreira, 1974; Kuris & Carlton, 1977; Buss & Iverson, 1981; Wicksten, 1983), and especially amongst other idoteids including Colidotea jkdleyi (Brusca, 1980), Erichsonella attenuata (Wicksten, 1983) and several species of Idotea (Lee, 1966a, b, c, 1972; Lee & Gilchrist, 1972; Salemaa, 1978, 1979; Brusca & Wallerstein, 1979; Lee & Miller, 1980; Kroer, 1986). Brusca & Wallerstein (1979) and Wallerstein & Brusca (1982) have discussed the possible importance of camouflage in the evolution of the Idoteidae. Prey behavior is important in escaping predation. For example, Main (1987) has shown that shrimp in seagrass meadows move around seagrass blades to avoid detection by predatory pinlish. Patton et al. (1985) have found that shrimp, commensal on sea urchins, quickly shift their position amongst the spines in response to sudden movements. A number of other workers have also demonstrated that many prey switch to less vulnerable microhabitats in the presence of predators (Kitching & Lockwood, 1975; Zaret & Suffern, 1976; Major, 1977; Stein, 1977; Sih, 1982). In this study, Colidotea rostrata displayed no obvious behavioral responses to the presence of predatory fishes. However, laboratory experiments did reveal that isopods shift their microhabitat position in response to diurnal cues. Regardless of whether predators are present or not, more isopods occur on the “exposed” aboral regions of urchins during nighttime hours than during daylight (Fig. 2). This is in agreement with the fact that most cryptic invertebrates are more active at night (Wicksten, 1983). This diurnal behavior may be an indirect antipredator response, since cryptic isopods are less visible to visual predators at night. Although fishes preyed upon Colidotea rostrata in the laboratory, a field caging experiment indicated that predation had no significant effect on natural populations of this isopod. In addition, feeding analyses revealed that few local intertidal fishes consume C. rostrata, but primarily eat other small invertebrates, especially amphipods (see Table II, and Mitchell 1953). Several factors help explain the relative absence of predation on field populations of C. rostrata. First of all, it is probably more difficult for fishes to detect isopods occurring amongst dense field aggregations of sea urchins, compared to the less dense laboratory situation. I have only found these isopods living in dense urchin beds. Furthermore, in this environment, any isopod dislodged from its host in the field is likely to end up on another nearby urchin. Secondly, many more easily accessible prey are present in the field; these prey make up the major portion of natural.

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fish diets (see Table II). Thirdly, the kelpfish Gibbonsia elegans, which was a highly efficient predator on C. rostrata in the laboratory, occurred only rarely at the study site. It is possible that fish predation has an effect on populations of C. rostrata at areas where G. elegans is more common. Several other types of organisms may be indirect predators of Colidotea rostrata. These predators include other urchins, seastars, crabs, fishes, and seabirds, all of which are known predators of C. rostrata’s host urchins (Durham et al., 1980; Lindberg, 1985; Coyer et al., 1987). Colidotea rostrata may succumb to these indirect predators more often than to direct predation by intertidal fishes. Cofidotea rostrata suffers little predation under natural conditions. This escape from predation pressure is especially pronounced for younger and smaller isopods. Aquarium observations revealed that small isopods, especially juveniles and mancas, were seldom preyed upon by foraging fishes. Several other workers have shown that prey size affects predator success (O’Brien et al., 1976; Nelson, 1979a; Wallerstein & Brusca, 1982; Main, 1985). The evolution of certain life history traits in C. rostrata, such as low fecundity and low juvenile mortality (see Stebbins, 1988, in press b) reflect this reduced predation pressure.

ACKNOWLEDGEMENTS

This paper is based on part of a Ph.D. dissertation submitted to the Department of Biological Sciences at the University of Southern California. I thank R. C. Brusca, G. J. Bakus, G.F. Jones, J.N. Kremer, D. J. Bottjer, and two anonymous reviewers; and L. A. Powers, P. M. Delaney, M. H. Temkin, and J. Stebbins. Partial financial support was provided by a Grant-In-Aid of Research from Sigma Xi, the Scientific Research Society.

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