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Frequencies of interspecific shell exchanges between hermit crabs
J. Exp. Mar. Biol. Ecol., 1982, Vol. 61, pp. 99-109
99
Elsevier Biomedical Press
FREQUENCIES
OF INTERSPECIFIC
SHELL EXCHANGES
BETWEEN HERMIT CRABS
PETER A. ABRAMS Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis. MN 55455. U.S.A.
Abstract: Frequencies of interspecific shell exchange due to shell fighting were determined for a number of species pairs of hermit crabs from several different locations. Frequencies were determined in the laboratory using a standardized experimental design. Results suggest that most individuals of most species are able to retain adequate or good quality shells in the presence of members of another species occupying poor quality shells. High frequencies of shell exchange always seem to be associated with very asymmetric relationships in which one member of the species pair is clearly dominant over the other. Dominant species usually attain larger sizes than subordinates, are found lower in the intertidal habitat, and are less abundant.
Shell fighting is a behavioral sequence which may result in an exchange of shells between two hermit crabs. Previous behavioral studies of shell fighting have shown that the probability of one crab initiating a fight may be influenced by the relative sizes of the crabs and their relative shell qualities (Hazlett, 1966, 1968, 1970; Vance, 1972; Bertness, 1981). The probability that a tight will result in a shell exchange (i.e. be successful) is influenced by the relative crab sizes, the defender’s (non-initiator’s) molt condition, the defender’s shell quality, and the attacker’s sex (Hazlett, 1966, 1970; Vance, 1972; Bertness, 1981; Abrams, 1981). As Hazlett (1978) has suggested the term “fight” may not always be appropriate because both the initiator and the noninitiator in a shell fight may obtain shells closer to their preferred size than the ones originally occupied. Not all lights result in mutual benefit, however, and if only one individual benefits from the exchange, it is always the initiator (Hazlett, 1978). The present paper is concerned with situations in which an exchange of shells can only benefit one individual of the pair. Such shell fights (and exchanges) will be referred to as competitive. Interspecific shell lights have been observed between many species pairs (Hazlett, 1972, 1980). Laboratory experiments on interspecific shell fighting (e.g. Hazlett, 1967, 1970; Abrams, 1981; Bertness, 1981) have shown that one species of a pair generally initiates a more successful shell exchanges than the other (in situations with equal numbers of both species). This species is generally referred to as the dominant. Several authors have suggested that shell fighting may play a prominent role in interspecific competition (Hazlett, 1970; Bach et&., 1976; Bertness, 1981). In addition to shell fighting, sympatric hermit crabs compete by mutual exploitation of a common supply 0022-0981/82/0000-0000/%02.75 0 1982 Elsevier Biomedical Press
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PETERA.ABRAMS
of empty shells. It is of considerable interest to know whether competitive shell exchanges via shell lighting can significantly alter the effect that one species has on the shell supply of another. Interspecific shell fighting would lessen the competitive impact of a subordinate on a dominant, but increase the impact of the dominant on the subordinate. In an area of sympatry between hermit crab species i and j, the following fates are possible for a new shell which becomes available in a hermit crab habitat. (1) A species i individual initially occupies and subsequently keeps the shell, or exchanges it with another i individual. (2) A species i individual initially occupies the shell, but loses it to a j individual in a shell tight. (3) A j individual occupies and keeps the shell. (4) A j individual occupies the shell, but loses it to species i. (5) The shell is destroyed or washed away before any individual occupies it. It is theoretically possible for multiple exchanges between i and j to occur. Given the results reported later in this article, however, this seems unlikely. Interspecific exploitative competition would be more important than interspecific shell fighting in determining shell supplies if alternatives (1) and (3) occur much more often than alternatives (2) and (4). Ideally, the relative importance of these pathways should be determined by frequent monitoring of the occupants of individually marked empty shells which were introduced into a hermit crab habitat. This has yet to be done. Laboratory experiments can provide suggestive evidence regarding the relative importance of the alternatives, however. If species i individuals occupying poor quality shells are seldom able to evict species j individuals occupying adequate or good quality shells (and vice versa), most crabs finding adequate or good shells will be able to keep them. Thus, shell fighting will have little impact on the level of competition determined by mutual exploitation of a common shell supply. The present study uses laboratory experiments to determine shell exchange frequencies for a number of hermit crab species pairs from several locations using a standardized experimental design. In addition to providing suggestive evidence regarding the relative importance of the different shell pathways explained above, the present study reveals a relationship between exchange frequencies and degree of dominance (defined on p. 105), as well as revealing common ecological characteristics of dominant and subordinate species.
METHODS
A similar design was used for determining shell exchange frequencies for all species pairs studied. Groups of 10 to 30 similarly sized individuals of each of two species were selected for an experiment. The exact number of hermit crabs used depended on the number of crabs available and the size of the experimental tanks available. An attempt
INTERSPECIFIC
SHELL
EXCHANGE
101
was made to keep experimental crab population densities within a factor of two of the estimated field densities. Density did not appear to have a significant effect on exchange frequencies in a separate study which used similar methods (Abrams, 1982). The species pairs studied are listed in Table I. Most of the experiments were parts of more general studies of resource partitioning and competition in several intertidal hermit crab communities (Abrams, 1980, and unpublished). Species pairs used in shell fight experiments were generally common species which had relatively high overlap in shell and habitat use. The shell size and species of the experimental animals were those for which there appeared to be the greatest overlap between species. The shells occupied by all experimental animals at a given location were similar in size, with a maximum difference between largest and smallest shells equal to 20% of the length of the largest. The shell quality of one of the two groups of crabs was decreased by breaking off part of the shell in which the crab was collected. This consisted of either breaking off the apex of the shell (removing enough of the apex so that the crab’s abdomen was exposed) or breaking away the outer lip of the shell to a point where at least some part of the crab’s limbs extended beyond the lip, even when the crab was withdrawn completely. Either of these treatments resulted in a shell of much poorer quality than those occupied in the field. For each species of crab studied here (except Pagurus hemphilli (Benedict), for which too few specimens were available), preliminary experiments were carried out to confirm that the modified shells were in fact of poorer quality than the intact shells occupied by the other group. A group of 10 or more individuals was offered a large array (100 or more) of modified shells. In no case did a crab leave its original shell during the 24-h trial period. The original (occupied) shells were then modified, and the crabs were presented with a large array of the more commonly utilized species of intact shells. In every case, all of the crabs abandoned the modified for the intact shells. Because all of the shell species used in the shell fight experiment were represented in these preliminary selection experiments, modified shells would seem to be inferior to all intact shells of these species (provided that they were of an acceptable size). Other selection experiments (Abrams, 1982) on one of the species studied here, Clibanarius virescens (Krauss), showed that crabs would abandon modified shells for intact shells which were 20% smaller (in length) than the average shell size occupied by that sized crab in the field. A comparison of results obtained using the two different shell modification techniques did not reveal any significant differences in shell exchange frequencies for that species. Using 10 or more crabs of each of the two species meant that each defender (each crab in a good quality shell) had a large number of potential attackers (initiators). This was always true at the beginning of the experiment, and was true throughout the experiment unless there was a very high proportion of exchanges. In almost all of the experiments reported below, fewer than half of the attackers were successful in forcing defenders out of their shells, so there were always a number of potential attackers for each defender. Experiments were generally run for 48 h. Over 80% of the exchanges occurred in the first 24 h. Crabs in unmodified shells occupied the shells in which they
102
PETER A. ABRAMS TABLE I
Species pairs studied, locations, and shell species occupied by experimental animals. Crab species pair
Shells occupied
Location studied
Cal&us laevimanus Randall Clibanarius humilis (Dana)
Cerithium and Rhinoclaws sp., Morula grantdata (Duclos)
Pago Bay, Guam
Pagurus traversi (Filhol) Pagurus novaezelandiae (Dana)
Turbo smaragda, Lepsiella scobina, Cominella virgata (see Powell, 1979, for
Goat Island Bay, New Zealand
Calcinus tibicen (Herbst) Clibanarius tricolor (Gibbes)
Nerita sp., Cerithium litteratum Born
CARMABI, Curacao and West Indies Lab., St. Croix, U.S. Virgin Islands
Calcinus elegans
Cantharus undosus (Linnaeus), Drupa morum (Roding), Strombus sp.
Enewetak Island Marshall Islands
Rhinoclavus sp.
Enewetak
Morula granulata (Duclos)
Enewetak
taxonomic authorities)
(H. Milne Edwards) Calcinus latens Randall Calcinus laevimanus Randall Clibanarius coralhnus
H. Milne Edwards Calcinus seurati Forest Clibanarius corallinus
H. Mime Edwards Calcinus latens Randall Clibanarius corallinus
Rhinoclavus sp.
H. Milne Edwards Clibanarius virescens (Krauss) Calcinus latens Randall
Planaxis sulcatus Born
One Tree Island, Great Barrier Reef, Australia
Calcinus laevimanus Randall Clibanartus virescens (Krauss)
Turbo sp.
One Tree Island
Clibanarius virescens (Krauss) Clibanatius corallinus
Planaxis sulcatus Born
One Tree Island
Cerithium stercumuscarum
Valenciennes, Planaxis planicostatus Sowerby
Venado Beach, Punta Paitilla, Flamenco Island (all in Bay of Panama)
Cerithium stercumuscarum
Venado Beach, Bay of Panama
H. Milne Edwards Calcinus obscurus Stimpson Clibanarius albidigitus Nobili Paguristes sp. (Abrams, 1980) Clibanarius albidigitus Nobili
Valenciennes
Calcinus obscurus Stimpson Pagurtstes sp.
Valenciennes
Cerithium stercumuscarum
Venado Beach, Bay of Panama
Pagurus granosimanus (Stimpson) Pagurus hirsutiusculus (Dana)
Tegula finebralis (A. Adams) Littorina sitkana Phillipi Olivella biplicata (Sowerby)
Bamfield, Vancouver Island, B.C. Friday Harbor, Washington Santa Barbara, California
Pagurus hemphilli (Benedict) Pagurus granosimanus (Stimpson)
Tegula funebralis (A. Adams)
Bamfield, Vancouver Island
Pagurus hemphilli (Benedict) Pagurus hirsutiusculus (Dana)
Tegula fiatebralis (A. Adams)
Barnfield, Vancouver Island
Pagurus granosimanus (Stimpson) Pugurus samuelis (Stimpson)
Tegula jiinebralis (A. Adams)
Pacific Grove, California
INTERSPECIFIC
103
SHELL EXCHANGE
were collected (“field” shells). Although these may have been smaller than the preferred size for their occupants, the selection experiments described above showed that they were preferred over the modified shells occupied by the other group of crabs. Thus, any exchanges which occurred in the shell fight experiments were competitive rather than mutualistic. For each species pair studied, at least two experiments were run concurrently, each with a different crab species occupying the modified shells.
RESULTS
Table II gives the average proportion of exchanges forced by each member of each species pair. When the same species pair was studied at several locations, average exchange frequencies are listed separately. There is clearly considerable variation in the ability of one species to evict another via shell fights, with exchange frequencies ranging from 0 to 0.65. For the majority of species pairs, very few shell exchanges occurred. 31 of the 42 average exchange frequencies given in Table II are < 10%. For 9 of the 2 1 pairs, neither species was able to evict > 10% of the individuals of the other species. For 15 of the 21, neither species evicted > 25% of the other. High frequencies of exchanges did occur between some species pairs, however. There does not seem to be any simple explanation for the variation in shell exchange frequencies observed. The cases of high shell exchange frequencies include both temperate and tropical species, as well as species from both major families of marine hermit crabs (Paguridae and Diogenidae). The cases in which a single species pair was studied at several locations reveal that shell fighting relationships may have pronounced TABLE
II
Shell exchange frequencies: *, f 1 SD; number of experiments in parentheses; **, r-test on arcsine transformed proportions with Bartlett’s correction for 0 and 1, 0.05 level; *** , for those species pairs without replicates, it was assumed that variances would have been similar to other species pairs.
Species pair _._____ A. Cal&us laevimanus B. Clibanarius humilis
Average exchange frequency when species A in modified shells*
Average exchange frequency when species B in modified shells (7)
Are exchange frequencies significantly different?**
0.078 f 0.106
(9)
A. Pagurus traversi B. Pagurus novaezelandiae
0.45
+ 0.071
(2)
0 (2)
yes
A. Calcinus tibicen B. Clibanarius tricolor
0.65
k 0.071
(2)
0 (2)
yes
A. Calcinus latens B. Cal&us elegans
0.05
+ 0.071
(2)
0 (2)
no
A. Calcinus laevimanus
0.017 k 0.024
(2)
0 (2)
no
B. Clibanarius corallinus
0.037
+ 0.064
no
PETER A. ABRAMS
104
TABLEII (continued) Are exchange frequencies significantly different?**
Average exchange frequency when species A in modified shells*
Average exchange frequency when species B in modified shells
A. Calcinus seurati B. Clibanarius corallinus
0 (2)
0 (2)
IlO
A. Cal&us latens B. Clibanarius corallinus
0 (2)
0 (2)
no
A. Clibanarius virescens B. Calcinus Iatens
0.058 f 0.043 (4)
0.005 * 0.011 (5)
no
A. Clibanarius virescens B. Clibanarius corallinus
0 (1)
0 (1)
no
0 (1)
yes***
Species pair
A. Calcinus laevimanus B. Clibanarius virescens A. Calcinus obscurus
0.6
(1)
0.25 kO.132
(3)
0.0167 + 0.0288 (3)
yes
A. Calcinus obscurus B. Clibanarius albidigilus (Venado)
0.075 f 0.05
(4)
0.025 rtr0.0353 (2)
no
A. Calcinus obscurus B. Clibanarius albidigitus (Paitilla)
0.480 f 0.057 (5)
0.0125 k 0.025 (4)
no
B . Clibanarius albidigilus
(Flamenco)
A. Paguristes sp. B. Clibanarius albidigitus
0.05
(1)
0 (1)
no***
A. Calcinus obscurus B. Paguristes sp.
0.3
(1)
0 (1)
yes***
0 (2)
yes
A. Pagurus granosimanus B. Pagurus hirsutiusculus Santa Barbara)
0.40 & 0
A. Pagurus hirsutiusculus B. Pagurus granosimanus (Friday Harbor)
0.224 f 0.107 (2)
0.020 + 0.028 (2)
yes
A. Pagurus granosimanus B. Pagurus hirsutiusculus (Bamtield)
0.205 k 0.004 (3)
0 (3)
yes
(2)
A. Pagurus granosimanus B. Pagurus hemphilli
0.074 (I)
0.057 (1)
no***
A. Pagurus hemphilli B. Pagurus hirsutiusculus
0.138 (1)
0 (1)
yes***
A. Pagurus granosimanus B. Pagurus samuelis
0.15 kO.0578 (4)
0.075 ?; 0.05
(4)
no
INTERSPECIFIC
SHELL
EXCHANGE
105
geographical variation. The Venado and Paitilla sites in Panama were separated by a distance of < 15 km, and crabs studied at the two sites were of similar sizes and occupied the same shell species. Nevertheless, shell exchange frequencies were very different. The dominance relationship between Pagurus grunosimanus (Stimpson) and P. hirsutiusculus (Dana) is reversed in comparing Bamfield, British Columbia and Friday Harbor, Washington locations. This particular case may be explained by the fact that P. hirsutiusculus in Littorina sitkuna Phillipi shells at Friday Harbor are significantly larger than the Pagurus granosimanus occupying that shell species. At Bamlield, P. hirsutiusculus and P. granosimanus occupying similarly sized Tegula funebralis (A. Adams) shells do not differ significantly in size. Shell tighting is probably more important in some hermit crab communities than in others. Very low exchange frequencies were obtained for all species studied in the northern tropical Indo-Pacific at Guam and Enewetak. The results presented in Table II do show a correlation between the presence of a high frequency of exchange and a high degree of dominance. The two exchange frequencies associated with a species pair can be averaged to give a total exchange frequency. The degree of dominance may be measured by the following index, (higher exchange frequency - lower exchange frequency) higher exchange frequency This index varies from 0 (no dominance) to 1 (when only one species is successful in forcing exchanges). The index is very sensitive to sampling variation when both exchange frequencies are low, but it should be replicable when at least one of the frequencies is large. Of the 10 species pairs which have the highest total exchange frequency (of 21), 9 have a dominance index of 0.9 or greater. There was no case in which each member of a species pair evicted > 10% of the individuals of the other member of the pair. A closer examination of those species pairs in which one member was clearly dominant reveals that certain ecological characteristics are shared by most dominant species. This can be seen from Table III. Although there are some exceptions, dominants tend to attain larger sizes, be found lower in the intertidal habitat, and be less abundant than subordinate species. Pugurus hirsutiusculus at Friday Harbor is an exception in all three categories. As noted above, P. hirsutiusculus inhabiting Littorina sitkuna shells at Friday Harbor are significantly larger than Pagurus grunosimanus in similar shells. This is not the case at other locations, nor is there such a clear size difference for any of the other species pairs listed in Table I.
PETER A. ABRAMS
106
TABLE III
Ecological correlates of dominance: *, relative abundance measured in those areas in which the two species co-occur; **, refers to maximum size. Relative position of dominant in intertidal
Relative size of dominant**
Dominant species
Subordinate species
Relative abundance of dominant*
Pagurus Waversi Calcinus tibicen Cal&us laevimanus Calcinus obscurus Calcinus obscurus Pagurus hirsutiusculus
Pagurus novaezelandiae Clibanarius tricolor Clibanarius virescens Clibanarius albidigitus Paguristes sp. Pagurus granosimanus
less less less less less more
lower lower lo.wer lower lower higher
smaller larger larger larger larger smaller
more
lower
larger
less
lower
larger
less
lower
(Friday Harbor) Pagurus granosimanus
Pagurus hirsutiusculus
(Bamtield) Pagurus granosimanus
Pagurus hirsutiusculus
(Santa Barbara) Pagurus hemphilli
Pagurus hirsutiusculus
DISCUSSION
For most of the species pairs studied, crabs which occupied adequate or good quality shells initially were able to retain those shells. If this is also true in the field, it would suggest (by the argument in the introduction) that mutual exploitation of a common shell supply was more important than shell fighting in determining the impact of one species on another’s shell supply. It must be noted, however, that laboratory results may not always reflect interactions in the field. It is possible that the proportion of subordinates evicted in field situations is greater than indicated by these experiments, because of the larger number of dominant individuals which may encounter any given subordinate. However, dominants are generally less abundant than subordinates. In addition, most dominant individuals in the field would not have as high a motivation to exchange shells, because field quality shells are significantly preferred over the modified shells used in these experiments. Other work (Abrams, 1982) showed much lower exchange frequencies in the laboratory when both groups of crabs occupied unmodified shells. It should also be noted that experiments on intraspecific lighting in one species (Abrams, 1982) have suggested that crabs in newly occupied shells are more susceptible to eviction than those in field quality shells. If this is true in general, the significance of shell lighting in interspecific competition may be greater than indicated here. On the other hand, it is possible that this phenomenon is of little significance in the field because crabs of a subordinate species may be capable of moving to areas where they are unlikely to encounter any dominant individuals. Field experiments on shell exchanges between CIibnnnriusalbidigitus and Crrlcinusnbscunrs (Abrams, 198 1)
INTERSPECIFIC
SHELL EXCHANGE
107
and on intraspecific exchange in Clibff~~riMsvirescens (Abrams, 1982) resulted in exchange frequencies comparable to those determined in the laboratory using the methods described here. The experiments reported here were carried out over the course of several years in connection with more extensive studies of resource partitioning in a number of different hermit crab species assemblages. Availability of specimens and time available for experiments varied between locations. The latter was often too short to perform as many experiments as would have been desirable. It should be noted, however, that frequency of exchange showed very little variability at a given location for all species pairs for which there was extensive replication. I have therefore reported several cases in which the experiment was not replicated. It should be remember~~hat each potential initiator in an experiment had 10 to 30 defenders with which exchanges could have occurred, and each experiment involved 10 to 30 potential initiators. Based on observed rates of encounter, every individual in an experimental tank should have encountered every other individual many times during the normal 48-h course of the experiment. Observed frequencies of exchange in a single experiment are the result of many potential exchanges (if each encounter between a crab in a modified shell and a crab in a good shell represented a potential exchange). It is therefore not surprising that frequencies should not vary much between experiments. It was noted earlier that molt condition, sex, and crab size could influence the probabi~ty of an exchange occurring. These attributes were not controlled in the experiments. The shell sizes occupied by the two groups before shell modi~cation were similar, because shell sizes were matched (by eye) when selecting the individuals for the experiment. A relatively narrow range of shell sizes was present in both modified and field quality groups. Shell size was matched (rather than crab size) because competition (if it occurs) will occur between crabs which use similarly sized shells, regardless of whether the crabs themselves are of the same size. Sex was not controlled, so the sex ratio of each species in an experiment should have been approximately that present in the field. The length of an experiment was sufficiently short that there was very little chance of more than one field quality individual molting during the experiment. Different shell exchange frequencies might have been obtained if larger individuals of one species had been selected for the expe~m~t, or if only one sex had been used. However, sex and size are not controlled in the field, and the method used here seemed most appropriate for estimating average shell exchange frequencies. It is only possible to speculate about the reason for the correlation between high exchange frequencies and a high degree of dominance. It may ,be that a crab will not leave a desirable shell when attacked unless there is a significant chance of injury. Injury by the other individual may be unlikely between two morphologically similar crabs of similar size. Hazlett (1980) noted a case in which a Pag~rus impressus was killed by a Clibunarius vittatus in a shell fight, but does not report any injuries in tights between the more closely related P~~~spo~li~a~~ and P. impressus. In the present study, the cases with the highest exchange frequencies involve a dominant species with a very large
108
PETER A. ABRAMS
major cheliped and a subordinate with two small chelipeds (i.e. Calcinus tibicenClibanarius tricolor; Calcinus obscurus-Clibanarius albidigitus; Calcinus laevimanusClibanarius virescens). This morphological difference may result in asymmetries in
abilities to attack or defend. If a dominant and a subordinate species had extensive habitat overlap, and if the subordinate was readily evictable by the dominant, it would seem likely that the dominant would competitively exclude the subordinate. This result could be avoided if there were relatively little habitat overlap between the two species, if the subordinate had a refuge in shell or habitat use, or if the dominant’s population density were regulated by intraspecific competition. The fact that the dominant species are found lower in the intertidal suggests that the subordinate often does have a refuge in the upper intertidal. Dominant species tend to attain larger sizes, and large dominant individuals only experience intraspecific competition. This, together with the fact that the dominant species tend to be less abundant, suggests that there is no “problem of coexistence” created by the dominant’s superior shell fighting abilities. Hazlett (1978) has suggested that many shell tights are mutualistic. The experiments described above were designed to determine maximum shell exchange rates in a competitive situation. They are consistent with the actual effect of most shell tights being mutualistic. In general, the difference in shell qualities between interacting individuals in the field is likely to be smaller than the difference between the modified and the unmodified shells used in the experiments here. In fact, one might expect shell selection behaviors to evolve in such a way that crabs could make use of shell exchange to obtain a better shell. Thus, a small crab may be willing to move into a too-large shell if it can expect to exchange shells with an individual in a more suitably sized shell in the near future. ACKNOWLEDGEMENTS
Field work was made possible by the hospitality of a number of marine laboratories: Hopkins Marine Station, Bamtield Marine Station, Friday Harbor Laboratories, The Marine Science Institute of the University of California, Santa Barbara, University of Auckland Marine Laboratory, University of Guam Marine Laboratory, Caribbean Marine Biological Intitute, West Indies Laboratory, the Smithsonian Marine Laboratory at Naos Island, and the Mid-Pacific Marine Laboratory. Support was provided by a Canada Council Killam postdoctoral fellowship, a NATO postdoctoral fellowship, and a grant from the Graduate School of the University of Minnesota. REFERENCES ABRAMS, P.A., 1980. Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia (Berlin), Vol. 46, pp. 365-319. ABRAMS, P.A., 1981. Shell fighting and competition between two Panamanian hermit crabs. Oecologia (Berlin), Vol. 51, pp. 84-90.
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SHELL EXCHANGE
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ABRAMS,P.A., 1982. Intraspecific shell exchange in the hermit crab Clibanarius virescens (Krauss). J. Exp. Mar. Biol. Ecol., Vol. 59, pp. 89-101. BACH,C. B., B. HAZLETT& D. RITTSCHOF,1976. Effects of interspecific competition on the fitness of the hermit crab Clibanarius tricolor. Ecology, Vol. 57, pp. 579-586. BERTNESS,M.D., 1981. Interference, exploitation, and sexual components of competition in a tropical hermit crab assemblage. J. Exp. Mar. Biol. Ecol., Vol. 49, pp. 189-202. HAZLE~, B.A., 1966. Social behavior of the Paguridae and Diogenidae of Curacao. Stud. Fauna Curacao, Vol. 23, pp. 1-143. HAZLEJT, B.A., 1967. Interspecific shell fighting between Pagurus bernhardus and Pagurus cuanensb. Sarsiu, Vol. 29, pp. 215-220. HAZLETT,B.A., 1968. Size relationships and aggressive behavior in the hermit crab Clibanarius vittatus.Z. Tierpsychol., Vol. 25, pp. 608-614. HAZLETT, B.A., 1970. Tactile stimuli in the social behavior of Pagurus bernhardus. Behaviour, Vol. 36, pp. 20118. HAZLETT,B.A., 1972. Shell fighting and sexual behavior in the hermit crab genera Pagwistes and Cal&us, with comments on Pugurus. Bull. Mar. Sci., Vol. 22, pp. 806-823. HAZLE~, B.A., 1978. Shell exchange in hermit crabs: aggression, negotiation, or both? Anim. Behav., Vol. 26, pp. 1278-1279. HAZLETT, B.A., 1980. Communication and mutual resource exchange in North Florida hermit crabs. Behav. Ecol. Sociobiol., Vol. 6, pp. 177-184. POWELL,A. W. B., 1979. New Zealand Mollusca. Collins, Auckland. VANCE,R.R., 1972. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology, Vol. 53, pp. 1075-1083.
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Elsevier Biomedical Press
FREQUENCIES
OF INTERSPECIFIC
SHELL EXCHANGES
BETWEEN HERMIT CRABS
PETER A. ABRAMS Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis. MN 55455. U.S.A.
Abstract: Frequencies of interspecific shell exchange due to shell fighting were determined for a number of species pairs of hermit crabs from several different locations. Frequencies were determined in the laboratory using a standardized experimental design. Results suggest that most individuals of most species are able to retain adequate or good quality shells in the presence of members of another species occupying poor quality shells. High frequencies of shell exchange always seem to be associated with very asymmetric relationships in which one member of the species pair is clearly dominant over the other. Dominant species usually attain larger sizes than subordinates, are found lower in the intertidal habitat, and are less abundant.
Shell fighting is a behavioral sequence which may result in an exchange of shells between two hermit crabs. Previous behavioral studies of shell fighting have shown that the probability of one crab initiating a fight may be influenced by the relative sizes of the crabs and their relative shell qualities (Hazlett, 1966, 1968, 1970; Vance, 1972; Bertness, 1981). The probability that a tight will result in a shell exchange (i.e. be successful) is influenced by the relative crab sizes, the defender’s (non-initiator’s) molt condition, the defender’s shell quality, and the attacker’s sex (Hazlett, 1966, 1970; Vance, 1972; Bertness, 1981; Abrams, 1981). As Hazlett (1978) has suggested the term “fight” may not always be appropriate because both the initiator and the noninitiator in a shell fight may obtain shells closer to their preferred size than the ones originally occupied. Not all lights result in mutual benefit, however, and if only one individual benefits from the exchange, it is always the initiator (Hazlett, 1978). The present paper is concerned with situations in which an exchange of shells can only benefit one individual of the pair. Such shell fights (and exchanges) will be referred to as competitive. Interspecific shell lights have been observed between many species pairs (Hazlett, 1972, 1980). Laboratory experiments on interspecific shell fighting (e.g. Hazlett, 1967, 1970; Abrams, 1981; Bertness, 1981) have shown that one species of a pair generally initiates a more successful shell exchanges than the other (in situations with equal numbers of both species). This species is generally referred to as the dominant. Several authors have suggested that shell fighting may play a prominent role in interspecific competition (Hazlett, 1970; Bach et&., 1976; Bertness, 1981). In addition to shell fighting, sympatric hermit crabs compete by mutual exploitation of a common supply 0022-0981/82/0000-0000/%02.75 0 1982 Elsevier Biomedical Press
100
PETERA.ABRAMS
of empty shells. It is of considerable interest to know whether competitive shell exchanges via shell lighting can significantly alter the effect that one species has on the shell supply of another. Interspecific shell fighting would lessen the competitive impact of a subordinate on a dominant, but increase the impact of the dominant on the subordinate. In an area of sympatry between hermit crab species i and j, the following fates are possible for a new shell which becomes available in a hermit crab habitat. (1) A species i individual initially occupies and subsequently keeps the shell, or exchanges it with another i individual. (2) A species i individual initially occupies the shell, but loses it to a j individual in a shell tight. (3) A j individual occupies and keeps the shell. (4) A j individual occupies the shell, but loses it to species i. (5) The shell is destroyed or washed away before any individual occupies it. It is theoretically possible for multiple exchanges between i and j to occur. Given the results reported later in this article, however, this seems unlikely. Interspecific exploitative competition would be more important than interspecific shell fighting in determining shell supplies if alternatives (1) and (3) occur much more often than alternatives (2) and (4). Ideally, the relative importance of these pathways should be determined by frequent monitoring of the occupants of individually marked empty shells which were introduced into a hermit crab habitat. This has yet to be done. Laboratory experiments can provide suggestive evidence regarding the relative importance of the alternatives, however. If species i individuals occupying poor quality shells are seldom able to evict species j individuals occupying adequate or good quality shells (and vice versa), most crabs finding adequate or good shells will be able to keep them. Thus, shell fighting will have little impact on the level of competition determined by mutual exploitation of a common shell supply. The present study uses laboratory experiments to determine shell exchange frequencies for a number of hermit crab species pairs from several locations using a standardized experimental design. In addition to providing suggestive evidence regarding the relative importance of the different shell pathways explained above, the present study reveals a relationship between exchange frequencies and degree of dominance (defined on p. 105), as well as revealing common ecological characteristics of dominant and subordinate species.
METHODS
A similar design was used for determining shell exchange frequencies for all species pairs studied. Groups of 10 to 30 similarly sized individuals of each of two species were selected for an experiment. The exact number of hermit crabs used depended on the number of crabs available and the size of the experimental tanks available. An attempt
INTERSPECIFIC
SHELL
EXCHANGE
101
was made to keep experimental crab population densities within a factor of two of the estimated field densities. Density did not appear to have a significant effect on exchange frequencies in a separate study which used similar methods (Abrams, 1982). The species pairs studied are listed in Table I. Most of the experiments were parts of more general studies of resource partitioning and competition in several intertidal hermit crab communities (Abrams, 1980, and unpublished). Species pairs used in shell fight experiments were generally common species which had relatively high overlap in shell and habitat use. The shell size and species of the experimental animals were those for which there appeared to be the greatest overlap between species. The shells occupied by all experimental animals at a given location were similar in size, with a maximum difference between largest and smallest shells equal to 20% of the length of the largest. The shell quality of one of the two groups of crabs was decreased by breaking off part of the shell in which the crab was collected. This consisted of either breaking off the apex of the shell (removing enough of the apex so that the crab’s abdomen was exposed) or breaking away the outer lip of the shell to a point where at least some part of the crab’s limbs extended beyond the lip, even when the crab was withdrawn completely. Either of these treatments resulted in a shell of much poorer quality than those occupied in the field. For each species of crab studied here (except Pagurus hemphilli (Benedict), for which too few specimens were available), preliminary experiments were carried out to confirm that the modified shells were in fact of poorer quality than the intact shells occupied by the other group. A group of 10 or more individuals was offered a large array (100 or more) of modified shells. In no case did a crab leave its original shell during the 24-h trial period. The original (occupied) shells were then modified, and the crabs were presented with a large array of the more commonly utilized species of intact shells. In every case, all of the crabs abandoned the modified for the intact shells. Because all of the shell species used in the shell fight experiment were represented in these preliminary selection experiments, modified shells would seem to be inferior to all intact shells of these species (provided that they were of an acceptable size). Other selection experiments (Abrams, 1982) on one of the species studied here, Clibanarius virescens (Krauss), showed that crabs would abandon modified shells for intact shells which were 20% smaller (in length) than the average shell size occupied by that sized crab in the field. A comparison of results obtained using the two different shell modification techniques did not reveal any significant differences in shell exchange frequencies for that species. Using 10 or more crabs of each of the two species meant that each defender (each crab in a good quality shell) had a large number of potential attackers (initiators). This was always true at the beginning of the experiment, and was true throughout the experiment unless there was a very high proportion of exchanges. In almost all of the experiments reported below, fewer than half of the attackers were successful in forcing defenders out of their shells, so there were always a number of potential attackers for each defender. Experiments were generally run for 48 h. Over 80% of the exchanges occurred in the first 24 h. Crabs in unmodified shells occupied the shells in which they
102
PETER A. ABRAMS TABLE I
Species pairs studied, locations, and shell species occupied by experimental animals. Crab species pair
Shells occupied
Location studied
Cal&us laevimanus Randall Clibanarius humilis (Dana)
Cerithium and Rhinoclaws sp., Morula grantdata (Duclos)
Pago Bay, Guam
Pagurus traversi (Filhol) Pagurus novaezelandiae (Dana)
Turbo smaragda, Lepsiella scobina, Cominella virgata (see Powell, 1979, for
Goat Island Bay, New Zealand
Calcinus tibicen (Herbst) Clibanarius tricolor (Gibbes)
Nerita sp., Cerithium litteratum Born
CARMABI, Curacao and West Indies Lab., St. Croix, U.S. Virgin Islands
Calcinus elegans
Cantharus undosus (Linnaeus), Drupa morum (Roding), Strombus sp.
Enewetak Island Marshall Islands
Rhinoclavus sp.
Enewetak
Morula granulata (Duclos)
Enewetak
taxonomic authorities)
(H. Milne Edwards) Calcinus latens Randall Calcinus laevimanus Randall Clibanarius coralhnus
H. Milne Edwards Calcinus seurati Forest Clibanarius corallinus
H. Mime Edwards Calcinus latens Randall Clibanarius corallinus
Rhinoclavus sp.
H. Milne Edwards Clibanarius virescens (Krauss) Calcinus latens Randall
Planaxis sulcatus Born
One Tree Island, Great Barrier Reef, Australia
Calcinus laevimanus Randall Clibanartus virescens (Krauss)
Turbo sp.
One Tree Island
Clibanarius virescens (Krauss) Clibanatius corallinus
Planaxis sulcatus Born
One Tree Island
Cerithium stercumuscarum
Valenciennes, Planaxis planicostatus Sowerby
Venado Beach, Punta Paitilla, Flamenco Island (all in Bay of Panama)
Cerithium stercumuscarum
Venado Beach, Bay of Panama
H. Milne Edwards Calcinus obscurus Stimpson Clibanarius albidigitus Nobili Paguristes sp. (Abrams, 1980) Clibanarius albidigitus Nobili
Valenciennes
Calcinus obscurus Stimpson Pagurtstes sp.
Valenciennes
Cerithium stercumuscarum
Venado Beach, Bay of Panama
Pagurus granosimanus (Stimpson) Pagurus hirsutiusculus (Dana)
Tegula finebralis (A. Adams) Littorina sitkana Phillipi Olivella biplicata (Sowerby)
Bamfield, Vancouver Island, B.C. Friday Harbor, Washington Santa Barbara, California
Pagurus hemphilli (Benedict) Pagurus granosimanus (Stimpson)
Tegula funebralis (A. Adams)
Bamfield, Vancouver Island
Pagurus hemphilli (Benedict) Pagurus hirsutiusculus (Dana)
Tegula fiatebralis (A. Adams)
Barnfield, Vancouver Island
Pagurus granosimanus (Stimpson) Pugurus samuelis (Stimpson)
Tegula jiinebralis (A. Adams)
Pacific Grove, California
INTERSPECIFIC
103
SHELL EXCHANGE
were collected (“field” shells). Although these may have been smaller than the preferred size for their occupants, the selection experiments described above showed that they were preferred over the modified shells occupied by the other group of crabs. Thus, any exchanges which occurred in the shell fight experiments were competitive rather than mutualistic. For each species pair studied, at least two experiments were run concurrently, each with a different crab species occupying the modified shells.
RESULTS
Table II gives the average proportion of exchanges forced by each member of each species pair. When the same species pair was studied at several locations, average exchange frequencies are listed separately. There is clearly considerable variation in the ability of one species to evict another via shell fights, with exchange frequencies ranging from 0 to 0.65. For the majority of species pairs, very few shell exchanges occurred. 31 of the 42 average exchange frequencies given in Table II are < 10%. For 9 of the 2 1 pairs, neither species was able to evict > 10% of the individuals of the other species. For 15 of the 21, neither species evicted > 25% of the other. High frequencies of exchanges did occur between some species pairs, however. There does not seem to be any simple explanation for the variation in shell exchange frequencies observed. The cases of high shell exchange frequencies include both temperate and tropical species, as well as species from both major families of marine hermit crabs (Paguridae and Diogenidae). The cases in which a single species pair was studied at several locations reveal that shell fighting relationships may have pronounced TABLE
II
Shell exchange frequencies: *, f 1 SD; number of experiments in parentheses; **, r-test on arcsine transformed proportions with Bartlett’s correction for 0 and 1, 0.05 level; *** , for those species pairs without replicates, it was assumed that variances would have been similar to other species pairs.
Species pair _._____ A. Cal&us laevimanus B. Clibanarius humilis
Average exchange frequency when species A in modified shells*
Average exchange frequency when species B in modified shells (7)
Are exchange frequencies significantly different?**
0.078 f 0.106
(9)
A. Pagurus traversi B. Pagurus novaezelandiae
0.45
+ 0.071
(2)
0 (2)
yes
A. Calcinus tibicen B. Clibanarius tricolor
0.65
k 0.071
(2)
0 (2)
yes
A. Calcinus latens B. Cal&us elegans
0.05
+ 0.071
(2)
0 (2)
no
A. Calcinus laevimanus
0.017 k 0.024
(2)
0 (2)
no
B. Clibanarius corallinus
0.037
+ 0.064
no
PETER A. ABRAMS
104
TABLEII (continued) Are exchange frequencies significantly different?**
Average exchange frequency when species A in modified shells*
Average exchange frequency when species B in modified shells
A. Calcinus seurati B. Clibanarius corallinus
0 (2)
0 (2)
IlO
A. Cal&us latens B. Clibanarius corallinus
0 (2)
0 (2)
no
A. Clibanarius virescens B. Calcinus Iatens
0.058 f 0.043 (4)
0.005 * 0.011 (5)
no
A. Clibanarius virescens B. Clibanarius corallinus
0 (1)
0 (1)
no
0 (1)
yes***
Species pair
A. Calcinus laevimanus B. Clibanarius virescens A. Calcinus obscurus
0.6
(1)
0.25 kO.132
(3)
0.0167 + 0.0288 (3)
yes
A. Calcinus obscurus B. Clibanarius albidigilus (Venado)
0.075 f 0.05
(4)
0.025 rtr0.0353 (2)
no
A. Calcinus obscurus B. Clibanarius albidigitus (Paitilla)
0.480 f 0.057 (5)
0.0125 k 0.025 (4)
no
B . Clibanarius albidigilus
(Flamenco)
A. Paguristes sp. B. Clibanarius albidigitus
0.05
(1)
0 (1)
no***
A. Calcinus obscurus B. Paguristes sp.
0.3
(1)
0 (1)
yes***
0 (2)
yes
A. Pagurus granosimanus B. Pagurus hirsutiusculus Santa Barbara)
0.40 & 0
A. Pagurus hirsutiusculus B. Pagurus granosimanus (Friday Harbor)
0.224 f 0.107 (2)
0.020 + 0.028 (2)
yes
A. Pagurus granosimanus B. Pagurus hirsutiusculus (Bamtield)
0.205 k 0.004 (3)
0 (3)
yes
(2)
A. Pagurus granosimanus B. Pagurus hemphilli
0.074 (I)
0.057 (1)
no***
A. Pagurus hemphilli B. Pagurus hirsutiusculus
0.138 (1)
0 (1)
yes***
A. Pagurus granosimanus B. Pagurus samuelis
0.15 kO.0578 (4)
0.075 ?; 0.05
(4)
no
INTERSPECIFIC
SHELL
EXCHANGE
105
geographical variation. The Venado and Paitilla sites in Panama were separated by a distance of < 15 km, and crabs studied at the two sites were of similar sizes and occupied the same shell species. Nevertheless, shell exchange frequencies were very different. The dominance relationship between Pagurus grunosimanus (Stimpson) and P. hirsutiusculus (Dana) is reversed in comparing Bamfield, British Columbia and Friday Harbor, Washington locations. This particular case may be explained by the fact that P. hirsutiusculus in Littorina sitkuna Phillipi shells at Friday Harbor are significantly larger than the Pagurus granosimanus occupying that shell species. At Bamlield, P. hirsutiusculus and P. granosimanus occupying similarly sized Tegula funebralis (A. Adams) shells do not differ significantly in size. Shell tighting is probably more important in some hermit crab communities than in others. Very low exchange frequencies were obtained for all species studied in the northern tropical Indo-Pacific at Guam and Enewetak. The results presented in Table II do show a correlation between the presence of a high frequency of exchange and a high degree of dominance. The two exchange frequencies associated with a species pair can be averaged to give a total exchange frequency. The degree of dominance may be measured by the following index, (higher exchange frequency - lower exchange frequency) higher exchange frequency This index varies from 0 (no dominance) to 1 (when only one species is successful in forcing exchanges). The index is very sensitive to sampling variation when both exchange frequencies are low, but it should be replicable when at least one of the frequencies is large. Of the 10 species pairs which have the highest total exchange frequency (of 21), 9 have a dominance index of 0.9 or greater. There was no case in which each member of a species pair evicted > 10% of the individuals of the other member of the pair. A closer examination of those species pairs in which one member was clearly dominant reveals that certain ecological characteristics are shared by most dominant species. This can be seen from Table III. Although there are some exceptions, dominants tend to attain larger sizes, be found lower in the intertidal habitat, and be less abundant than subordinate species. Pugurus hirsutiusculus at Friday Harbor is an exception in all three categories. As noted above, P. hirsutiusculus inhabiting Littorina sitkuna shells at Friday Harbor are significantly larger than Pagurus grunosimanus in similar shells. This is not the case at other locations, nor is there such a clear size difference for any of the other species pairs listed in Table I.
PETER A. ABRAMS
106
TABLE III
Ecological correlates of dominance: *, relative abundance measured in those areas in which the two species co-occur; **, refers to maximum size. Relative position of dominant in intertidal
Relative size of dominant**
Dominant species
Subordinate species
Relative abundance of dominant*
Pagurus Waversi Calcinus tibicen Cal&us laevimanus Calcinus obscurus Calcinus obscurus Pagurus hirsutiusculus
Pagurus novaezelandiae Clibanarius tricolor Clibanarius virescens Clibanarius albidigitus Paguristes sp. Pagurus granosimanus
less less less less less more
lower lower lo.wer lower lower higher
smaller larger larger larger larger smaller
more
lower
larger
less
lower
larger
less
lower
(Friday Harbor) Pagurus granosimanus
Pagurus hirsutiusculus
(Bamtield) Pagurus granosimanus
Pagurus hirsutiusculus
(Santa Barbara) Pagurus hemphilli
Pagurus hirsutiusculus
DISCUSSION
For most of the species pairs studied, crabs which occupied adequate or good quality shells initially were able to retain those shells. If this is also true in the field, it would suggest (by the argument in the introduction) that mutual exploitation of a common shell supply was more important than shell fighting in determining the impact of one species on another’s shell supply. It must be noted, however, that laboratory results may not always reflect interactions in the field. It is possible that the proportion of subordinates evicted in field situations is greater than indicated by these experiments, because of the larger number of dominant individuals which may encounter any given subordinate. However, dominants are generally less abundant than subordinates. In addition, most dominant individuals in the field would not have as high a motivation to exchange shells, because field quality shells are significantly preferred over the modified shells used in these experiments. Other work (Abrams, 1982) showed much lower exchange frequencies in the laboratory when both groups of crabs occupied unmodified shells. It should also be noted that experiments on intraspecific lighting in one species (Abrams, 1982) have suggested that crabs in newly occupied shells are more susceptible to eviction than those in field quality shells. If this is true in general, the significance of shell lighting in interspecific competition may be greater than indicated here. On the other hand, it is possible that this phenomenon is of little significance in the field because crabs of a subordinate species may be capable of moving to areas where they are unlikely to encounter any dominant individuals. Field experiments on shell exchanges between CIibnnnriusalbidigitus and Crrlcinusnbscunrs (Abrams, 198 1)
INTERSPECIFIC
SHELL EXCHANGE
107
and on intraspecific exchange in Clibff~~riMsvirescens (Abrams, 1982) resulted in exchange frequencies comparable to those determined in the laboratory using the methods described here. The experiments reported here were carried out over the course of several years in connection with more extensive studies of resource partitioning in a number of different hermit crab species assemblages. Availability of specimens and time available for experiments varied between locations. The latter was often too short to perform as many experiments as would have been desirable. It should be noted, however, that frequency of exchange showed very little variability at a given location for all species pairs for which there was extensive replication. I have therefore reported several cases in which the experiment was not replicated. It should be remember~~hat each potential initiator in an experiment had 10 to 30 defenders with which exchanges could have occurred, and each experiment involved 10 to 30 potential initiators. Based on observed rates of encounter, every individual in an experimental tank should have encountered every other individual many times during the normal 48-h course of the experiment. Observed frequencies of exchange in a single experiment are the result of many potential exchanges (if each encounter between a crab in a modified shell and a crab in a good shell represented a potential exchange). It is therefore not surprising that frequencies should not vary much between experiments. It was noted earlier that molt condition, sex, and crab size could influence the probabi~ty of an exchange occurring. These attributes were not controlled in the experiments. The shell sizes occupied by the two groups before shell modi~cation were similar, because shell sizes were matched (by eye) when selecting the individuals for the experiment. A relatively narrow range of shell sizes was present in both modified and field quality groups. Shell size was matched (rather than crab size) because competition (if it occurs) will occur between crabs which use similarly sized shells, regardless of whether the crabs themselves are of the same size. Sex was not controlled, so the sex ratio of each species in an experiment should have been approximately that present in the field. The length of an experiment was sufficiently short that there was very little chance of more than one field quality individual molting during the experiment. Different shell exchange frequencies might have been obtained if larger individuals of one species had been selected for the expe~m~t, or if only one sex had been used. However, sex and size are not controlled in the field, and the method used here seemed most appropriate for estimating average shell exchange frequencies. It is only possible to speculate about the reason for the correlation between high exchange frequencies and a high degree of dominance. It may ,be that a crab will not leave a desirable shell when attacked unless there is a significant chance of injury. Injury by the other individual may be unlikely between two morphologically similar crabs of similar size. Hazlett (1980) noted a case in which a Pag~rus impressus was killed by a Clibunarius vittatus in a shell fight, but does not report any injuries in tights between the more closely related P~~~spo~li~a~~ and P. impressus. In the present study, the cases with the highest exchange frequencies involve a dominant species with a very large
108
PETER A. ABRAMS
major cheliped and a subordinate with two small chelipeds (i.e. Calcinus tibicenClibanarius tricolor; Calcinus obscurus-Clibanarius albidigitus; Calcinus laevimanusClibanarius virescens). This morphological difference may result in asymmetries in
abilities to attack or defend. If a dominant and a subordinate species had extensive habitat overlap, and if the subordinate was readily evictable by the dominant, it would seem likely that the dominant would competitively exclude the subordinate. This result could be avoided if there were relatively little habitat overlap between the two species, if the subordinate had a refuge in shell or habitat use, or if the dominant’s population density were regulated by intraspecific competition. The fact that the dominant species are found lower in the intertidal suggests that the subordinate often does have a refuge in the upper intertidal. Dominant species tend to attain larger sizes, and large dominant individuals only experience intraspecific competition. This, together with the fact that the dominant species tend to be less abundant, suggests that there is no “problem of coexistence” created by the dominant’s superior shell fighting abilities. Hazlett (1978) has suggested that many shell tights are mutualistic. The experiments described above were designed to determine maximum shell exchange rates in a competitive situation. They are consistent with the actual effect of most shell tights being mutualistic. In general, the difference in shell qualities between interacting individuals in the field is likely to be smaller than the difference between the modified and the unmodified shells used in the experiments here. In fact, one might expect shell selection behaviors to evolve in such a way that crabs could make use of shell exchange to obtain a better shell. Thus, a small crab may be willing to move into a too-large shell if it can expect to exchange shells with an individual in a more suitably sized shell in the near future. ACKNOWLEDGEMENTS
Field work was made possible by the hospitality of a number of marine laboratories: Hopkins Marine Station, Bamtield Marine Station, Friday Harbor Laboratories, The Marine Science Institute of the University of California, Santa Barbara, University of Auckland Marine Laboratory, University of Guam Marine Laboratory, Caribbean Marine Biological Intitute, West Indies Laboratory, the Smithsonian Marine Laboratory at Naos Island, and the Mid-Pacific Marine Laboratory. Support was provided by a Canada Council Killam postdoctoral fellowship, a NATO postdoctoral fellowship, and a grant from the Graduate School of the University of Minnesota. REFERENCES ABRAMS, P.A., 1980. Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia (Berlin), Vol. 46, pp. 365-319. ABRAMS, P.A., 1981. Shell fighting and competition between two Panamanian hermit crabs. Oecologia (Berlin), Vol. 51, pp. 84-90.
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SHELL EXCHANGE
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ABRAMS,P.A., 1982. Intraspecific shell exchange in the hermit crab Clibanarius virescens (Krauss). J. Exp. Mar. Biol. Ecol., Vol. 59, pp. 89-101. BACH,C. B., B. HAZLETT& D. RITTSCHOF,1976. Effects of interspecific competition on the fitness of the hermit crab Clibanarius tricolor. Ecology, Vol. 57, pp. 579-586. BERTNESS,M.D., 1981. Interference, exploitation, and sexual components of competition in a tropical hermit crab assemblage. J. Exp. Mar. Biol. Ecol., Vol. 49, pp. 189-202. HAZLE~, B.A., 1966. Social behavior of the Paguridae and Diogenidae of Curacao. Stud. Fauna Curacao, Vol. 23, pp. 1-143. HAZLEJT, B.A., 1967. Interspecific shell fighting between Pagurus bernhardus and Pagurus cuanensb. Sarsiu, Vol. 29, pp. 215-220. HAZLETT,B.A., 1968. Size relationships and aggressive behavior in the hermit crab Clibanarius vittatus.Z. Tierpsychol., Vol. 25, pp. 608-614. HAZLETT, B.A., 1970. Tactile stimuli in the social behavior of Pagurus bernhardus. Behaviour, Vol. 36, pp. 20118. HAZLETT,B.A., 1972. Shell fighting and sexual behavior in the hermit crab genera Pagwistes and Cal&us, with comments on Pugurus. Bull. Mar. Sci., Vol. 22, pp. 806-823. HAZLE~, B.A., 1978. Shell exchange in hermit crabs: aggression, negotiation, or both? Anim. Behav., Vol. 26, pp. 1278-1279. HAZLETT, B.A., 1980. Communication and mutual resource exchange in North Florida hermit crabs. Behav. Ecol. Sociobiol., Vol. 6, pp. 177-184. POWELL,A. W. B., 1979. New Zealand Mollusca. Collins, Auckland. VANCE,R.R., 1972. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology, Vol. 53, pp. 1075-1083.