ELSEVIER Journal of Experimental Marine Biology and Ecology

182 (1994) 49-64

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Symbiotic organisms increase the vulnerability of a hermit crab to predation

William J. Buckley*, John P. Ebersole

Department of Biology, University of Massachusetts at Boston, Boston, MA 021253393, USA

Received 18 January 1994; revision received 2 May 1994; accepted 12 May 1994

Abstract

The association between the hermit crab Pagurus Iongicarpus Say and an ectosymbiotic colonial hydroid of the genus Hydractinia was studied to determine whether the presence of Hydractinia affects the resistance of Pagurus Zongicarpus to predation. Observations of tethered hermit crabs confirmed the importance of predation by the blue crab, Callinectes sapidus Rathbun, on the Pagurus Zongicarpus population in Nantucket Harbor, Massachusetts. In a predation experiment, caged hermit crabs in Littorina Zittorea (L.) shells with and without Hydractinia were exposed to single blue crabs. Shell damage indicated that blue crabs attacked hermit crabs in both shell types in roughly equal proportions: 65% of hermit crabs in shells with Hydractinia were attacked compared to 69% of hermit crabs in shells without Hydractinia. Only 20% of hermit crabs in shells with the hydroid survived attack, however, compared to 54% in shells without Hydractinia. Continuous observation of predation in aquaria showed that hermit crabs in shells with Hydrac- tinia had significantly shorter survival times when attacked by a blue crab than hermit crabs in shells without the colonial hydroid. The crushing resistance of shells was measured with an InstronTM testing machine. A comparison of the regression equations of shell mass (g) vs. crushing resistance (N) between shell types showed that shells with Hydractinia had a lower slope than shells without Hydractinia, although because of a wide range in crushing resistance, this difference was not significant. Shells with Polydoran worm burrows, however, were significantly weaker than shells without burrows, and shells with Hydractinia were more likely to hold worms than shells without Hydractinia. The positive correlation between Hydractinia and shell-degrading worms explains the vulnerability of hermit crabs in shells with the colonial hydroid to predation by blue crabs. Other studies have shown that hermit crabs may benefit from having Hydractinia on their shells because the hydroid prevents large and potentially harmful ectosymbionts, such as Crepidula species, from colonizing. Thus, for Pagurus longicarpus the costs and benefits of the association with Hydractinia may change depending upon the presence of other organisms and this may shift the nature of the association with Hydractinia from mutualism to commensalism to parasitism.

* Corresponding author.

0022-0981/94/$7.00 0 1994 Elsevier Science B.V. All rights reserved SSDI 0022-098 1(94)00077-Q

50 W.J Buckley. J.P. Ebersole I 1. Exp Mar. Bid Eccol 182 (IYY4) 49-64

Keywords: Callinectes sapidtu; Hydractinia; Pagurus hgicarpus; Po!\~dorcr “pp.; Predation; Sym- biosis

1. Introduction

Hermit crabs are decapod crustaceans that live in empty gastropod shells. Lim- ited shell availability prevents many individuals in a hermit crab population from ob- taining an optimum shell and lowers hermit crab fitness, since various components of fitness including growth rate (Fotheringham, 1976; Bertness, 1981a), clutch size (Fotheringham, 1980; Bertness 1981a), and protection from physical stresses and pre- dation (Reese, 1969; Bet-mess, 1981b, 1981d, 1982) are directly correlated with certain shell characteristics (Vance, 1972). Heavy and thick-walled gastropod shells with nar- row apertures have been shown to mitigate predation (Vermeij, 1976, 1977, 1982), and hermit crabs exposed to predators prefer shells with these characteristics (Bet-mess 198 Lc,d, 1982; Borjesson & Szelistowski, 1989). Shell-choice experiments have shown that shell mass (Childress, 1972) volume (Conover, 1978), over& size (McChntock, 1985; Wilber, 1990), and protective properties (Reese, 1969; Bertness & Cunningham, 198 1) influence shell choice by hermit crabs. Shell features inducing the highest rate of shell exchange by Pagmupollicaris Say in Florida were those which increased the risk of predation, including small size,~aperture damage, and general weakness caused by Clionid sponges (McClintock, 1985). Lively’s (1988) research~suggests that shell char- acteristics that allow for retreat into the shell to avoid predators are preferred by the hermit crab Clibanarius digueti Bouvier.

P&ants and sessile animals colonize she&inhabited by hermit crabs (Conover, 1979) and the presence of these organisms can aher shell features and affect shell choice (Brooks & Mariscal, 1985a). For example, colonial hydroids of the genus Hydructinia, found almost exclusively on gastropod shells inhabited by pagurid hermit crabs, illus- trate the costs and benefits of such symbiotic associations.

Benefits of the association for Hydractika are clear and include access to “leftovers” from hermit crab feeding (Wright, 1973), and the facilitation~of sexual reproduction when the hermit crabs congregate (Buss & Yund, 1988). Additionally, hermit crab mobility into different habitats may increase feeding opportunities for the sessile hydroid (Rivest, 1978; Conover, 1979), and decrease the chances of suffocating burial by sedi- ments (Conover, 1975).

Pagurus longicarpus may benefit from the association with Hydructiniu if large ecto- symbionts are discouraged from colonizing the shell (Karison & Cariolou, 1982; McClean, 1983; Johnson, 1988). However, unlike hermit crab - sea anemone relation- ships, in which hermit crabs appear to benefit by gaining protection from predators (Ross, 1971; McLean, 1983; Brooks, 1989), the role that Hydractitiia plays relative to predation is not clear. Grant & Pontier (1973) found that a crab predator was deterred by hydroids; Brooks & Mariscal(1985b) found that hermit crabs in hydroid-colonized shells were protected from the stone crab Menippe mercenarzu but were more likely to be eaten by the crab Hepatus epheliticus than hermit crabs in shells without hydroids.

W.J. Buckley, J.P. Ebersole /J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 51

In Nantucket Harbor, the presence of Hydructiniu did not affect predation on Pugurus longicarpus by green crabs, Carcinus maenus, or lady crabs, Ova&es ocellatus, and blue crabs were more likely to prey on hermit crabs in hydroid-colonized shells compared to hermit crabs in shells without hydroids (Johnson, 1988).

Two possible explanations for the higher vulnerability of hermit crabs in shells with Hydractinia to predation are distinct but not mutually exclusive. First, attack on her- mit crabs in shells with Hydractinia may succeed more often because these shells are older and, due to dissolution by seawater, weaker than shells without Hydractinia; or because Hydractinia or associated organisms degrade shell structure. Organisms that dissolve calcareous substrata such as limestone and mollusc shells are well known, and include bacteria, algae, and fungi, as well as numerous invertebrate taxa (Carriker & Smith, 1969). A positive correlation between Hydractinia and shell degrading organisms would mean that shells with Hydractinia tend to be weak.

The other potential explanation for higher vulnerability to predation is that preda- tors are more likely to attack when Hydructinia is present than when it is not present. The odor or color of Hydructiniu on a shell may serve as a cue, possibly making her- mit crabs easier for predators to detect. Blue crabs exhibit visual evaluation of potential prey (Hamilton, 1976; West & Williams, 1986) and also use tactile and olfactory clues to detect prey (Blundon & Kennedy, 1982). Alternatively, blue crabs might prefer to attack hermit crabs in shells with Hydractinia if the presence of the hydroid indicates a weaker shell, since this would conserve time or energy for the predator.

The observations and experiments of this study were designed to determine: (1) the importance of Callinectes sapidus predation pressure on the population of Pagurus longicarpus in Nantucket Harbor; (2) whether the presence of Hydructinia results in increased predation by Callinectes sapidus; (3) whether Hydractinia is a cue to Callinectes sapidus which leads to a higher attack rate on Pagurus longicarpus; and (4) whether shells with Hydructiniu are weaker than shells without Hydructinia.

2. Methods

All hermit crabs used in this study were Pagurus longikarpus inhabiting Littorina littorea (L.) shells. Hermit crabs were collected by hand from the intertidal and shal- low subtidal zone at the University of Massachusetts Field Station, Nantucket, during summer, 199 1. Blue crabs, Callinectes sapidus, were also captured here, or were netted from a nearby salt marsh.

Prior to experiments, hermit crabs were held in lobster keeper cages (90 x 55 x 35 cm) lined with 5 mm plastic mesh and placed in the shallow subtidal zone so that they were submerged throughout the tidal cycle. Blue crabs were held under the same conditions, in similar cages, but without the plastic mesh. Surviving experimental animals were returned to the study site at the end of each experiment.

2. I. Observation of tethered hermit crabs

Observations were made to determine whether predation of hermit crabs by blue crabs is important in Nantucket Harbor.

52 W J. Buckley. J.P Ebersole : J Exp. Mur. Bid. Ed. 182 11994) 49-04

A small hole was drilled through the apex of 50 empty Littorim littoreu shells and 40 cm of monofilament line was tied to each shell. Hermit crabs were added to an aquarium containing the tethered shells and allowed to switch into them. They were held in the aquarium as a supply for the duration of the experiment, and were fed periodically with ground shellfish or commercial fish flakes.

Eight hermit crabs were tethered to a ballasted 3 m length of 4.5 cm PVC pipe at intervals of 40 cm and the pipe was placed on the bottom in the subtidal study site in Nantucket Harbor (0.75 m deep at low tide, 1.75 m deep at high tide). Tethering in this way probably produces a density of hermit crabs higher than normal at this site, although Pagumcs longicarpus are sometimes found in aggregations similar to the den- sity produced by tethering.

Tethered hermit crabs were checked twice a day for the duration of the experiment, once in the morning soon after sunrise, and again twelve hours later in the early evening. The following categories, comprising all observations, were noted: (a) shell undamaged; (b) shell empty; (c) shell damaged, hermit crab present; (d) shell damaged, hermit crab missing; (e) shell missing.

Empty, damaged, and missing shells were immediately replaced. Damaged shells were kept for comparison with shells damaged by blue crabs in predation experiments. The position of the pipe and attached crabs was haphazardly shifted by roughly 2 m after each check to randomize its location on a small scale and prevent the possibil- ity of an individual predator learning its location.

Minimum and maximum average attack rates and mortality rates were determined at the conclusion of the 33-day observation period (July 24 through August 26, 1991). To calculate maximum rates, “shell empty” and “shell missing” observations were assumed to indicate fatal attacks, and all attacks were assumed to have happened at the very beginning of the between-check interval in which they occurred. Conversely, to calculate minimum rates, “shell empty” and “shell missing” observations were as- sumed to indicate survivorship with no attack, and all attacks were assumed to have taken place at the very end of the between-check interval. For all computations it was assumed that “undamaged” observations indicate no attack, “shell damaged, hermit crab present” indicate non-fatal attacks, and “shell damaged, hermit crab missing” indicate fatal attacks. Thus, the following formulas give the minimum and maximum average daily attack and mortality rates (crab-‘.day-‘):

c+d Minimum average daily attack rate = -

[(S crabs) (63 time intervals)]/2

Maximum average daily attack rate = b + c + d + e

I(8) (63) - (b + c + d + e)]/2

d Minimum average daily mortality rate = -

g(63)12

b+d+e Maximum average daily mortality rate =

I(8) (63) - (b + d + e)J/2

W.J. Buckley, J.P. Ebersole / J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 53

These rates were extrapolated to compute 30- and 90-day attack and mortality probabilities.

2.2. Aquarium predation experiment

This experiment tested the hypothesis that the presence of Hydractinia is a cue to blue crabs, leading to a higher attack rate on hermit crabs in shells with the hydroid. Dif- ferences in predator processing time between the two shell types was also recorded to test the hypothesis that shells with Hydractinia can be processed faster than shells without Hydractinia.

For each trial two hermit crabs in Littorina littorea shells, one with Hydractinia and one without Hydractinia, were introduced at the same time into a 75-l aquarium con- taining a single blue crab. Hermit crabs were matched for shell length to within 0.5 mm. All shells were in “good” condition, qualitatively defined as a less than perfect shell, but without holes, aperture damage, or apex damage, and every effort was made to use equivalent shells in each trial. Only hermit crabs that could withdraw completely into the shell were used in the experiment. There were 12 trials involving four male blue crabs (average carapace width = 125 mm, SD = 14.7) and 24 hermit crabs in shells ranging in length from 14.9 to 28.5 mm.

Each trial was observed until both hermit crabs were consumed by the blue crab. We noted which hermit crab was attacked first, and the time spent processing each her- mit crab (i.e., time elapsed after initial attack until the hermit crab was eaten). Time was calculated to the nearest minute; differences of less than one minute in process- ing time between the two shell types were scored as ties. The sequence in which her- mit crabs were attacked, either first or second, was analyzed with a binomial analysis, and differences in processing time were analyzed with a Wilcoxon signed-rank test.

2.3. Cage predation experiment

Cage predation trials were designed to test two hypotheses: (1) the presence of Hydractinia is a cue to the blue crab leading to higher attack rates, (2) once attacked, hermit crabs in shells with Hydractinia are more likely to be killed than hermit crabs in shells without Hydractinia.

Each trial began by introducing five pairs of hermit crabs in L. littorea shells, 5 with Hydractinia and 5 without, into a mesh-lined lobster keeper cage containing a single male blue crab (average carapace width = 115 mm, SD = 4.3). Hermit crabs, in shells ranging from 14.8 to 22.9 mm, were matched for shell length to within 2 mm. All shells of hermit crabs were in “good” condition as defined for the aquarium predation trials, and only hermit crabs that could withdraw completely into the shell were used. Cages were placed at the study site in Nantucket Harbor in the shallow subtidal zone.

Cages were checked hourly until four of the 10 hermit crabs had been eaten. Sur- viving hermit crabs and shell fragments were then examined to determine how many hermit crabs in each shell type had been: (1) not attacked; (2) attacked but survived (shell damaged); and (3) attacked and eaten. Attack rates for shells with Hydractinia were compared to those for shells without Hydractinia, to determine predator prefer-

54 W.J. Buckle!, J P Ebersole 1 J. E.xp. Mar Bid Ecol 18-7 (1994) 49-64

ence. The ratio of Pagurus iongicarpus consumed to P. longicarpus attacked was used to determine relative predator success with hermit crab prey in the two different shell types. In all, results for 15 trials were analyzed, involving 150 hermit crabs and five blue crabs.

A chi-square test for heterogeneity was applied to the pooled data to determine any difference in attack rates between hermit crabs in shells with Hydractinia and those in shells without Hydractinia. A second chi-square test was conducted on hermit crabs which were attacked, to determine any difference in survival between hermit crabs in the two shell types.

2.4. Microscopic examination

Littorina littorea shells with and without Hydractinia were examined with a Scanning Electron Microscope to determine any difference in microscopic structure between the two shell types. While examining the shells-and shell fragments the presence of shell- burrowing Polydoran worms was noted. The presence or absence of these poiychaetes was subsequently tabulated in the shells recovered from the predation experiments.

2.5. Shell strength experiment

To quantify strength differences between the two shell types the crushing resistance of 51 shells (25 with, 26 without Hydractinia) was measured using an InstronTM test- ing machine in July, 1991. A second Instron trial, designed~ to increase sample size and to determine the effects of Pdydoran worm burrows on shell strength, was performed

on 57 shells (28 with, 29 without Hydractinia) in September, 1993. Shells were oriented aperture down and crushed with a steel plate moving at

0.167 mm . s-l. Force was measured by computer; the highest force reached before major failure was recorded as the crushing force. Regression lines of shell mass (g) vs. crushing force (N) were fitted for shells with and without Hydractinia and analysis of covariance was used to compare slopes and elevations.

3. Results

3.1. Observation of tethered hermit crabs

For the 33-day period of observation, the final tally in the four categories used to determine attack and mortality rates was: shell abandoned = 4; shell damaged, hermit crab present = 5; shell damaged, hermit crab missing = 18; shell missing = 7.

Virtually all damaged shells had aperture damage like the damage inflicted by blue crabs in the predation experiments. Average daily attack and mortality rates were ex- trapolated to determine the probability of attack and mortality for 30 days and for a 90-day season (Table 1). The minimum average daily mortality rate, or the minimum probability that an individual hermit crab would be eaten on any given day, was p = 0.071. Extrapolating this minimum rate shows that there would be a very high

W.J. Buckley, J.P. Ebersole 1 J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 55

Table 1

Minimum and maximum average daily attack and mortality rates for the tether experiment

Attack rates

Minimum” Maximumb

Mortality rates

Minimum’ Maximum“

Daily 0.091 0.145 0.071 0.122

30 days 0.943 0.991 0.890 0.980

90 days 0.999 > 0.999 0.998 > 0.999

Extrapolating these rates gives the minimum and maximum probabilities of attack and survival for 30 days

and for a 90 day season (summer).

a Includes categories c and d.

b Includes categories b, c, d and e.

’ Includes category d.

d Includes categories b, d and e (see text).

chance of mortality during an entire 90-day season (p = 0.9987; Table 1). In fact, no hermit crab survived for the duration of the entire observation period of 33 days since at least one hermit crab was eaten at each of the eight tether stations on the pipe. The longest-living tethered hermit crab lasted for 16 days.

3.2. Aquarium predation experiment

Blue crabs seemed to attack the first hermit crab encountered, regardless of shell type. Hermit crabs in shells with Hydractinia were attacked first in 5 of the 12 trials, and those in shells without Hydractinia were attacked first in the remaining seven trials (binomial analysis; p = 0.613), indicating that blue crabs have no disproportionate tendency to attack prey in either shell type.

Hermit crab prey in shells with Hydractinia were processed faster by blue crab predators, allowing less time for the hermit crab to escape. In 9 of 12 trials the her- mit crab in a shell without Hydractinia survived longer than the matched hermit crab in a shell with Hydractinia; in only one of 12 trials did the hermit crab with Hydractinia survive longer (p = 0.0279; Table 2).

Direct observations during aquarium predation trials revealed consistent shell open- ing behavior of blue crabs. If the shell was relatively small, the initial effort was usu- ally a brief attempt to crush the shell across the body whorl or at the apex. Most shells resisted this method of attack. If this initial crushing attack failed, or if the shell was relatively large, an apertural attack was used, in which the blue crab chipped pieces of shell from the aperture by applying pressure with the dactyl molar of the crusher claw. Although all blue crabs used in the predation trials were able to complete attacks, some blue crabs were more efficient than others in attacks of this type (one individual had a mean processing time of only 1.5 min per attack, from two to seven times faster than the others). Less efficient blue crabs commonly fumbled the shell while attempting to open it, and even the most efficient crab occasionally dropped the hermit crab. When this occurred, the blue crab corralled the dropped hermit crab with its claws and walking legs and resumed the attack. Sometimes a hermit crab would escape when a

56 W.J. Buckley. J.P Ehersok / J. Exp Mar. Bwl Ecol 182 (19941 49-64

Table 1

Results of the aquarmm predation trlais ()I= 12); difference m survival trme for herrnIL crabs m matched shells

wtth and without H_vdrmtinia

Trial Survival time (min)

Without Hydractmu With Hydractmu Difference*

x 9

10 11 12

17 3 1-I

-I I 3 26 s 2

2 9 -1

36 9 21

5 3 2

2 2 0

15 I 14

I! I I 3 I 2 1 I 0 3 1 2

* Difference in survival time analyzed with a Wilcoxon signed-rank test (corrected for ties): p = 0.0279.

blue crab that had dropped a shell would retrieve a shell fragment or stone from the bottom of the aquarium similar in size to the Littorina fittorea shell, instead of the original prey. At other times a hermit crab would “bail out” of a shell that had been severely damaged by the attacking blue crab. This maneuver rarely worked because the blue crabs were alert to the prey, but hermit crabs occasionally escaped, if only briefly, within the aquarium.

3.3. Cage predation experiment

Overall results of the present study showed that 52% (39 of 75) of hermit crabs in shells with Hydractiniu were eaten, compared to 32% (24 of 75) in shells without the hydroid. Results obtained by Johnson (1988) from simiIar experiments showed that when shell conditions were equal, 70% of hermit crabs in shells with Hydractinia were eaten by blue crabs, compared to 30% of hermit crabs in shells without Hydractinia.

In 15 cage predation trials, 65 y0 (49 of 75) of hermit crabs in shells with Hydractinia were attacked by blue crabs compared to 69% (52 of 75) of hermit crabs in shells without Hydractinia (chi-square = 0.273, p = 0.6015). This findingofroughly equal attack rates for both shell types is consistent with the finding of the aquarium predation experiment.

There was a substantial and significant difference in mortality between hermit crabs in the two shell types, however. Only 20% (15 of 49) of hermit crabs in shells with Hydractinia survived attack, compared to 54% (28 of 52) of her-n&crabs attacked in shelis without Hydractinia (chi-square = 12.019, p = 0.0005). Thus, hermit crabs in shells withy Hydractinia are less likely to survive an attack than hermit crabs in shells with- out Hydractinia.

W.J. Buckley, J.P. Ebersole /J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 57

3.4. Microscopic examination

Microscopic examination revealed no evidence of shell dissolution beneath Hydrac- tinia colonies. However, many shells did show the presence of two species of burrowing worms, Polydora commensalis and Polydora websteri Hartman, known to weaken mol- lust shells (Zottoli & Carriker, 1974). Scanning electron micrographs of Polydoran worm burrows (Fig. 1) show that these worm burrows could weaken a shell, since a major portion of the calcium carbonate structure is removed.

Tabulation of the presence or absence of these polychaetes in 112 shells from the predation experiments revealed that 66% (37 of 56) of shells with Hydractinia contained Polydoran worm burrows compared to only 20% (11 of 56) of shells without Hydrac- tinia (chi-square = 24.646; p = 0.0001). In the 57 shells from the second shell strength trial, 68 y0 (19 of 28) of shells with Hydractinia contained worm burrows compared to only 38 y0 (11 of 29) of shells without the hydroid (chi-square = 5.117; p = 0.0237).

3.5. Shell strength

Shells ranged from 0.56 to 4.61 gin mass; shell lengths ranged from 10.6 to 25.8 mm. The force required to crush the shells ranged from 49.8 N to 769.4 N. Data from the two shell strength trials were pooled to analyze the effects of Hydractinia (Fig. 2).

Shells without Hydractinia showed a close correlation between crushing force and mass (R* = 0.515), whereas shells with Hydractinia showed a less predictable relation- ship between the two variables (R* = 0.232). This wider range in the force required to crush hydroid-colonized shells, combined with a lower slope, suggests that at least some of the shells with Hydractinia were weaker than those without Hydractinia, although the difference between the slopes and elevations of the two regression lines was not sig- nificant (Table 3). The presence of worms was not tabulated in the first shell strength trial so the data from the second trial was used to analyze the effects of Polydoran worms (Fig. 3). Shells with worms present (R* = 0.552) and worms absent (R* = 0.560) both showed a close correlation between mass and crushing force. There was no dif- ference in the slopes of the two regression lines but there was a highly significant dif- ference in the elevations (Table 3), showing that shells with worms are weaker than shells without worms.

4. Discussion

4.1. Blue crab predation

The results of the tether observation demonstrate that predation was an important pressure on the Nantucket Harbor population of P. longicarpus during the summer of 1991. Blue crabs may not have been the only predator responsible, since green crabs, lady crabs, and toadfish, Upsanus tau (L.) are other possible predators. However, Johnson (1988) found that green and lady crabs ate only a fraction of hermit crab prey, compared to blue crabs, and a laboratory observation found that toadfish would not

58 W.J. Buckley, J. P. Ehersule 1 J. Exp. Mar. Bid. Ecol. I82 (I 994) 49-64

W.J. Buckley, J.P. Ebersole 1 J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 59

Table 3

Regression data for mass vs. crushing force for shells with (n = 53) and without (n = 55) Hydracrinia and

Polydoran worms present (n = 30) or absent (n = 27)

Regression R2 P

Hydractinia

Polydora

with I’= 63.87x + 152.75 0.232 without y = 117.63~ + 116.70 0.515

Difference between slopes (p> 0.10) and between elevations (p> 0.05)

present y = 114.76x + 20.77 0.552

absent y = 148.38x + 121.73 0.560

Difference between slopes (p> 0.50) and between elevations (p<O.OOl)

0.0003

0.0001

0.0001

0.0001

x = mass (g); y = force (N).

8001 . . . - . - . -. . t

700.

600.

- t

500.

= s 400.

IL

300.

200.

100.

0 0

0 0 I

0 00 t

1

0 0 With

. 0 Without

-0 .5 1 1:5 i 2:5 3 -3:5- i ~4:s.. i

Mass (9)

Fig. 2. Data from both trials of the In&on shell strength experiment are plotted as mass (g) vs. force (N); with Hydructinia (n = 53); without Hydractinia (n = 55).

eat hermit crabs at all (J.E., unpubl. data). Also, shell damage to tethered hermit crabs was the same as that inflicted by blue crabs in the predation trials. The rates in Table 1 are presented to indicate that predation of hermit crabs by blue crabs occurs in Nantucket Harbor but are not suggested to be estimates of natural predation rates. It is possible that the presence of the pipe enhanced blue crab activity, leading to a higher predation rate. Also, certain behavioral responses of hermit crabs to predation,

Fig. 1. Scanning electron micrographs of Littorina littoreu shells with Hydructiniu which were formerly occupied by Pagurus longiuxpus. (a) Two Polydora websteri burrows (x 0.5 mm in diameter). The segmented remains of one worm can be seen in the bottom burrow. (b) A Polydora commensab burrow (z 1 mm in diameter) opens near the aperture of a shell. Note the chitinous remains of a Hydructinia colony on the outer surface of the shell. (c) The exposed interior of a shell showing the columella and Polydoran worm burrows (= 0.5- 1 mm in diameter).

60 W.J. Buckley, J.P. Ebersole i J E.Yp Mur. Bwl. Ed 182 IlYY4I 49-M

such as seeking shelter in seagrass (Heck & Thoman, 1981; Heck & Wilson, 1987) or staying in shallow water at high tide (Bertness, 1982), are precluded by tethering, though other behaviors known to be important in mitigating predation, such as burying (Kuhlman, 1992) are presumably still available to tethered hermit crabs. In any event, the evidence points to the blue crab as an important predator of hermit crabs at this site.

Callinectes sapidus individuals large enough to be important predators begin appear- ing in Nantucket Harbor in late June and remain through September, with the height of breeding activity in August. Pagurus iongicarpus appear as early as April, and stay in shallow waters until October, although the highest numbers occur from June through September. Blue crab density fluctuates from year to year, and blue crabs may have been more abundant in Nantucket Harbor during the 1991 season than during any season in the previous 12 years (pers. obs. J.E.). As the summer season progressed, hermit crab density declined with increasing blue crab density, and aperture-damaged shells were commonly noted (pers. obs., W.B. and J.E.), further attesting to the im- portance of this predator.

4.2. Shells with Hydractmia incur more predation

Results of the cage predation experiment were similar to those of Johnson (1988) who found that Pagunrs longicarpus in shells with Hydractinia were more likely to be eaten by C. sapidus than Pagurus langicarpus in shells without the colonial hydraid. Additional non-experimental observations support this finding. Pagurus Iongicarpus in shells with Hydractinia were relatively easy to find during daily snorkeling surveys in June, but by August, when blue crabs were abundant, it often took long periods of time to find even one hermit crab in a shell with the hydroid. Cage and aquarium predation experiments

A 700. A

A

600. A

BA A

Q 500. A V %% z AA .

k 400.

IL A@ A A

300. $”

+ i(r

A 200. r&f

A *i&A A A

A

100.

.A 0.

0 .5 1 1.5 2 2.5 3 3.5 4

Ma= (9)

edvdora WP. 4 Present AAbSWtt

5

Fig. 3. Data from the second shell strength trial plotted as mass (g) vs. force (N): P&&m spp. present (n = 30); Polydora spp. absent (n = 27). Note that shells with worms are weaker

W.J. Buckley. J.P. Ebersole 1 J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 61

showed that this higher vulnerability of hermit crabs in shells with Hydractinia is not because shells with the hydroid are more conspicuous or more attractive to blue crabs. Blue crabs attacked hermit crabs in shells with and without Hydractinia in equal pro-

portions (cage predation trials) and as they were encountered (aquarium predation trials). Predation rates on hermit crabs in shells with Hydractinia are higher compared to hermit crabs in shells without the hydroid because attacks by blue crabs are more likely to succeed (cage predation trials), and because hydroid-colonized shells are destroyed in less time (aquarium predation trials). Shell strength trials suggest that shells with Hydractinia are weak because they often contain shell-burrowing Polydoran worms.

4.3. Shell strength

The plot of all hermit crab shells tested for mass vs. force shows a fairly wide range of crushing resistance for shells of similar weight (Fig. 2), resulting in a large standard error for the slope of each regression. Other investigators have also reported variabil- ity in the force required to crush shells or shell sections of a single species of similar weight, whether they are from the original gastropod (Currey & Kohn, 1976; Blundon & Vermeij, 1983) or have been subsequently occupied by hermit crabs (LaBarbera & Merz, 1992). This may be explained by noting that some gastropods, such as Littorina Zittorea, lack defenses against colonizing organisms, including burrowing polychaetes (Wahl & Sonnichsen, 1992) so that shell degradation may start with the original gastropod occupant. Additionally, LaBarbera & Merz (1992) found that Calliostoma ligatum shells occupied by hermit crabs were significantly weaker and showed greater variability in crushing resistance than shells occupied by the original gastropods. They note that unlike most gastropods, hermit crabs cannot repair progressive shell disso- lution or shell damage caused by predators or endobionts. Thus, differences in origi- nal condition, age, and the degree of colonization by endobionts could explain the variability in crushing resistance of the shells tested in this and other studies. Despite

this variability, shells with Polydoran worms were significantly weaker than shells without worms, and most shells with worms also had Hydractinia.

Observations of escape behavior by hermit crabs in the aquarium predation experi- ment point to the importance of a shell which resists crushing and takes a predator longer to open, thus increasing the chances of an escape. Although escapes within the aquarium provided only a brief reprieve, a hermit crab escaping in the field could seek cover and perhaps avoid further attack.

4.4. A mutualism-commensalism-parasitism continuum

Why would hermit crabs in this population continue to inhabit hydroid-colonized shells if this represents a cost in the form of increased vulnerability to predation?

One reason is that scarcity of shells may limit the alternatives. Numerous studies demonstrate that hermit crabs inhabit less than preferred shells (Scully, 1979; Abrams, 1980; Bertness, 1980). Personal observation (W.B. and J.E.) indicates that the shell resource is limited for the population of Pagurus Zongicaqws in Nantucket Harbor

62 W J Buckley. J.P. Ebersole /J Esp. Mu. Biol. Ecol I82 119941 49-64

as well. During daily snorkeling surveys it was uncommon to find any empty gastro- pod shells, and Pagurscs Zongicarpus were often noted inhabiting shells in poor condi- tion.

A second reason that Pagurus longicarpus is found in shells with Hydractinia is that there may be certain benefits in cohabiting with the colonial hydroid. Although crab predators at this site are not deterred by Hydractinia, it is possible that fish predators, which were not used in predation experiments, are deterred. Another benefit is that heavy ectosymbionts may be discouraged from colonizing the shell (Karlson &z Cariolou, 1982). For example, although Pugunts longicarpus from Nantucket Harbor usually show an aversion for shells with Hydractinia, Johnson (1988) found that Pagurus Iongicarpus had an increased preference for shells with the hydroid at two times of the year, once in late spring and again in early fall.

These periods of increased preference coincided with the presence of large Crepidula convexa Say, an ectosymbiont which can adversely weight and unbalance hermit crab shells. Shells which are too heavy or unbalanced have been shown to have a negative effect on hermit crab fitness in the form of reduced mobility and reduced fecundity (Conover, 1976; Brooks, 1989). In Johnson’s study there was a negative correlation between the presence of Hydractinia and the presence of Crepidula convexa on Pagurus longicalpus shells; laboratory observations showed that Crepidulu convexa actively avoided contact with Hydractinia colonies. Thus, the hydroid keeps this other more harmful ectosymbiont off the shell, providing a benefit to the resident hermit crab.

As an obligate symbiont. Hydractinia always benefits from the relatianship with Pagurus longicarpus. However, since Hydractinia is positively associated with Polydoran worms, but negatively associated with large Crepidulu, there are conflicting effects on Pagurus longicarpus depending on changing selective pressures. For example, when large CrepiduZa are present in Nantucket Harbor the association is best defined as mutual- ism; Pagurus longicalpus benefits because large Crepidula are excluded from colonizing their shells. In July and August, when blue crabs are active in the Harbor, hermit crabs are at a greater risk of predation and hermit crabs in shells with the hydroid are less likely to survive an attack. This represents a cost to P. longicarpus, and the associa- tion with Hydructinia becomes an example of parasitism. In early spring and late fall, when neither large Crepidula nor Callinectes sapidw are present, the association is best defined as commensalism, since the effect on &gurus bngicarpus is probably negligible. Thus, the nature of the Pagurus longicarpus-Hydructinia association shifts from mutu- alism to commensalism to parasitism, depending upon changing~ biotic factors.

Acknowledgements

Thanks to W. Tiffney for the use of the facilities at the University of Massachusetts Field Station. M. Rex and R. Stevenson provided criticism of the manuscript and M. Smith assisted with the micrographs. A. Nussinovitch from the Food Science Laboratory at the University of Massachusetts ate Amherst and K. York from the Instron laboratory at Canton, MA generously helped with the shell strength testing.

W.J. Buckley, J.P. Ebersole / J. Exp. Mar. Biol. Ecol. 182 (1994) 49-64 63

References

Abrams, P.A., 1980. Resource partitioning and interspecific competition in a tropical hermit crab commu-

nity. Oecologia. Vol. 46, pp. 365-319. Bertness, M.D., 1980. Shell preference and utilization patterns in littoral hermit crabs of the Bay of Panama.

J. Exp. Mar. Biol.Ecol., Vol. 48, pp. 1-16.

Bertness, M.D., 1981a. Competitive dynamics of a tropical hermit crab assemblage. Ecology, Vol. 62,

pp. 751-761. Bertness, M.D., 1981b. The influence of shell type on hermit crab growth rate and clutch size. Crustaceana,

Vol. 40, pp. 197-205.

Bertness, M.D., 198 lc. Predation, physical stress, and the organization of a tropical rocky intertidal hermit

crab community. Ecology, Vol. 62, pp. 411-425. Bertness, M.D., 1981d. Conflicting advantages in resource utilization: the hermit crab housing dilemma. Am.

Nat., Vol. 118, pp. 432-431. Bertness, M.D., 1982. Shell utilization, predation pressure, and thermal stress in Panamanian hermit crabs:

an interoceanic comparison. J. Exp. Mar. Biol. Ecol., Vol. 64, pp. 159-187.

Bertness, M.D. & C. Cunningham, 1981. Crab shell crushing predation and architectural defense. J. Exp.

Mar. Biol. Ecol., Vol. 50, pp. 213-230.

Blundon, J.A. & V.S. Kennedy, 1982. Refuges for infaunal bivalves from blue crab, Callinectes sapidus, predation in Chesapeake Bay. J. Exp. Mar. Biol. Ecol., Vol. 65, pp. 67-8 1.

Blundon, J.A. & G.J. Vermeij, 1983. Effect of shell repair on shell strength in the gastropod Littorina irrorata.

Mar. Biol., Vol. 41, pp. 41-45.

Borjesson, D.L. & W.A. Szelistowski, 1989. Shell selection, utilization, and predation in the hermit

crab Clibanarius panamensis in a tropical mangrove estuary. J. Exp. Mar.Biol. Ecol., Vol. 133, pp. 213-

228. Brooks, W.R., 1989. Hermit crabs alter sea anemone placement patterns for shell balance and reduced

predation. J. Exp. Mar. Biol. Ecol., Vol. 132, pp. 109-121.

Brooks, W.R. & R.N. Mariscal, 1985a. Shell entry and shell selection of hydroid-colonized shells by three

species of hermit crabs from the northern Gulf of Mexico. Biol. Bull., Vol. 168, pp. 1-17.

Brooks, W.R. & R.N. Mar&al, 1985b. Protection of the hermit crab Paguruspollicaris Say from predators

by hydroid-colonized shells. J. Exp. Mar. Biol. Ecol., Vol. 87, pp. 111-118.

Buss, L.W. & P.O. Yund, 1988. A comparison of recent and historical populations of the colonial hydroid

Hydractinia. Ecology, Vol. 69, pp. 646-654.

Carriker, M.R. & E.H. Smith, 1969. Comparitive calciobiocavitology: summary and conclusions. Am. Zool.. Vol. 9, pp. 1011-1020.

Childress, J.R., 1972. Behavioral ecology and fitness theory in a tropical hermit crab. Ecology, Vol. 53,

pp. 960-964.

Conover, M.R., 1975. Prevention of shell burial as a benefit hermit crabs provide to their symbionts.

Crustaceana, Vol. 29, pp. 3 1 l-3 13.

Conover, M.R., 1976. The influence of some symbionts on the shell selection behavior of the hermit crab

Pagurus pollicaris and Pagurus longicarpus. Anim. Behav., Vol. 24, pp. 191-194. Conover, M.R., 1978. The importance of various shell characteristics to the shell-selection behavior of hermit

crabs. J. Exp. Mar. Biol. Ecol., Vol. 32, pp.131-142.

Conover, M.R., 1979. Effect of gastropod shell characteristics and hermit crabs on shell epifauna. J. Exp. Mar. Biol. Ecol., Vol. 40, pp. 81-94.

Currey, J.D. & A.J. Kohn, 1976. Fracture in the crossed-lamellar structure of Conus shells. J. Materials Sci., Vol. 11, pp. 1615-1623.

Fotheringham, N., 1976. Population consequences of shell utilization by hermit crabs. Ecology, Vol. 57,

pp. 570-578.

Fotheringham, N., 1980. Effects of shell utilization on reproductive patterns in tropical hermit crabs. Mar. Biol., Vol. 55, pp. 287-293.

Grant, W.C. & P.J. Pontier, 1973. Fitness in the hermit crab Pagurus acadianus with reference to Hydractinia echinata. Bull. Ml. Desert Island Biol. Lab., Vol. 13, pp. 50-53.

64 W.J. Buckley. J.P Ebemoie 1 J. E.rp Mar. Bioi. Ecol. IN2 ilsiY4i 49-64

Ham&on, P.V., 1976. Predation of Lmmna mmtu (Mollusca.Gastropoda) by Cbl/ut~~ tes .rrrprdus (Crusta-

cea:Portuntdea). Bull. Mur Sri.. Vol 26. pp. 403-409.

Heck, K.L. & T.A. Thoman, 1981. Experiments on predator-prey mteracttons m vegetated aquatic habitats.

.I E.up. Mur Blol Ecol Vol. 53. pp. 125-134.

Heck. K.L. & K.A. Wilson, 1987. Predation rates on decapod crustaceans m tatttudmally separated seagrass

communities: a study of spatial and temporal vartation usmg tethermg techniques. .I Eup Mur Biol. Ecol Vol 107, pp. 87-100.

Johnson, R.W.. 1988. The nature of the relattonshtp between the hermtt crab, Prrguruts Imgrcarpu~. and one of its ectosymbionts, ff_vdractiniu echinara. Master’s Thests, Umversrty of Massachusetts, Boston, MA.

Karlson, R.H. & M.A. Cariolou, 1982. Hermit crab shell cotonization by Creptdulo conve~a Sq. J Exp. Mar. Bml. Ecol., Vol. 65, pp. l- 10

Kuhlman, M.L., 1992 Behavioral avotdance of predation in an mterttdal hermit crab. ./ b XP Mar. &ol. I%ol.

Vol. 157. pp 143-158.

LaBarbera. M. & R.A. Mere, 1992. Postmortem changes m strength of gastropod shells, evoluttonary tm-

phcations for hermit crabs, snails. and their mutual predators. PuleobiologJ; Vol. 18. pp. 367-377.

Ltvcly. C.M., 1988. A graphical model for shell-species selection by hermit crabs. I%‘~ologr. Vol. 69. pp. 1233-

t238.

McClean, R., 1983. Gastropod shelfs. A dynamic resource that helps shape benthtc community structure

J Exp. Mar. BIoI. Ecol.. Vol. 69, pp. 151-174.

McChntock. T.S., 1985. Effects of shell condition and sue upon the shell chotce behavior of a hermrt crab.

J E-up Mar. Biof. Ecol., Vol. 88, pp. 271-285

Reese. E S., 1969. Behavtoral adaptations of intertidal hermtt crabs. 4m ZO~I/., VOL. ‘1. pp. 343-355.

Rtcest. B.R., 1978. Development of the eolid nudibranch Cuthonrr nana and its rclattonshtp with a hydroid

and hermit crab. Biol. Bull., Vol. 154, pp. 157-175.

Rosa. D M.. 1971. Protection of hermit crabs (Dardunus spp.) from octopus hy commensal sea anemones

(Calliacfis spp.). Nuture, Vol. 230, pp. 40 l-402.

Scully. E P.. 1979. The effects of gastropod shell availabthty and habitat charactcrtsttcs on shell utthzatron

by the mtertrdal hermit crab Pagurus longicurpus Say. J. E.tp. Mar. Blol. Ec~rl.. Vol 37, pp 139-152

Vance. R.R., 1972 The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology,

Vol. 53. pp. 1075-1083.

Vermctj, G.J.. 1976. Interoceanic differences m vulnwabtlity of shelled prey to crab prcdatron. N&we. Vol. 260, pp. 135-136.

Vcrmet.j, G.J., 1977. Patterns m crab claw- size: the geography of crushrng. S):tf. .%~~1.. Vol. 1, pp. 138-

151.

VermetJ, G.J., 1982. Gastropod shell form.breakage. and repair in relatton to predatton by the crab Cafrppo Ahlacologla. Vol. 23, pp. 1-12.

Wahl, M. & H. Sonnichsen. 1992. Marme epibiosts. IV. The pertwinkle Lrrrorrrw lirtorecl lacks typical antt-

fouhng defences - why are some populations so little fouled? Mar. Ecol Prog. Ser. Vol. 88. pp. 225-

2 3 5

M’est, D.L. & A.H. Wrlhams, 1986. Predation by Cul1mecre.s srcptdus wnhm Sporrma cdtertujoru marshes. J E_xp Mar Blol. Ecnl.. Vol. 100, pp. 75-95.

Wilber. T.P., 1990. Influence of size, species, and damage on shell selectton by the hermtt crab Pugurus /mgrcurpu~ Mar. Btol. Vol. 104, pp. 31-39.

Wright. H.O., 1973. Effect of commensal hydroids on hermtt crab competttton m the littoral zone of Texas.

Vurure. Vol 241. pp. 139-140. pp. 971-982.

Zottoli, R.A. & M.R. Carriker, 1974. Burrow morphology, tube formatron and mtcroarchttecture of shell

dtssolution by the Sptomd polychaete Po!vdora websreri. Mm Biol., Vol. 27. pp. 307-316