the development of shell preferences by the hermit ... - Science Direct

Anim . Behav ., 1979, 27, 940-946

THE DEVELOPMENT OF SHELL PREFERENCES BY THE HERMIT CRAB PAGUR US BERNHARD US By ROBERT W . ELWOOD, ANNE McCLEAN & LINDA WEBB Department of Zoology, The Queen's University of Befast, Belfast, Northern Ireland

Abstract. The occurrence of empty gastropod shells and those occupied by the hermit crab, Pagurus bernhardus, was examined on the shore . This survey suggested that small crabs prefer L . littoralis shells to those of Gibbula species and this was confirmed by preference tests in the laboratory . Crabs removed from these small shells show an initial preference for Nucella shells to those of L . littorea . However, medium sized crabs collected in either Nucella or L . littorea prefer the species in which they were collected . This preference is still apparent when the size of the test shells is varied . These data provide the first clear evidence for a modification of shell preferences after experience of particular shell species. Markham (1968) thought that crabs selected a specific volume to weight ratio and Hazlett (1970b) found that the possession of shells which were either too heavy or had too little internal volume would induce shell fighting . Species preferences have also been the subject of several studies. Jackson (1913) concluded that full grown P. bernhardus preferred shells of Buccinum undatum and Fuscus antiquus (Neptuna antiqua) while Pike and Williamson (1959) reported that Littorina littorea, Nucella (Thais) lapillus, L . littoralis and Nassarius reticulatus shells were preferred in that order. Both reports of `preferences', however, were interpreted from the results of sublittoral samples and reflected the occurrence of the shells rather than preference per se. In controlled experiments, Orians & King (1964) demonstrated a preference by P . hirsutiusculus for Nucella (Thais) emarginata shells to either Calliostoma or Tegula shells . Reese (1962) found that P . sammuelis preferred Tegula shells at low weight indexes (shell weight = crab weight) but preferred Acanthina shells at high weight indexes . Other species of crabs also showed changes in preferences as the weight indexes of the test shells were varied . Grant (1963) offered the crab's original shell along with a shell of a different species . The majority of crabs chose their original shell but, as the shells were not matched for either weight or volume, no reliable conclusions concerning species preferences can be drawn . Many of these studies on shell selection were complicated by the wide range of crab sizes and the variety of shell species which they inhabit . The present study is an attempt to assess the development of shell preferences of P . bernhardus . At different stages of development

Hermit crabs have a soft asymmetrical abdomen which they protect by living in empty gastropod shells . This use of shells has intrigued biologists over the years (Reese 1962 for historical review) . More recently this interest in hermit crabs and their shells has come from two overlapping biological disciplines, those of ecology and ethology . Ecologists have investigated interspecific and intraspecific competition for shells which appeared to be a limited resource in population growth (Spight 1977) . Experimental addition of empty shells to a reef was found to increase the hermit crab population (Vance 1972a) and crab populations have been related to natural fluctuations in shell availability (Spight 1977) . The possession of a suitable shell has been found to enhance growth (Markham 1968), reproduction (Childress 1972), success in agonistic interactions (Childress 1972) and protection against predators (Vance 1972b) . Possession of an unsuitable shell by Clibanarius vittatus increased aggression towards conspecifics (Hazlett 1970a) but did not increase aggression in Pagurus hirsutiusculus (Vance 1972b), although in the latter case the probability of effecting a transfer of shells by shell fighting was increased. Ethologists have been interested in the effects of the shell upon interactions with other individuals (Hazlett 1970a, b) and the development of the shell selection behaviour after the larval stage (Reese 1962), and particularly in the stimulus control of shell selection (Reese 1962, 1963) . This last author has concluded that the weight of the shell and the internal configuration are the most important factors in shell selection, while Grant (1963) considered a high internal volume to weight ratio to be important . 940

ELWOOD ET AL . : SHELL PREFERENCES OF PAGURUS BERNHARDUS

crabs were offered choices of shells appropriate to those particular stages . Experiments were also designed to test for any individual preferences which may develop after particular experiences . However, the first stage of the study was a shore survey carried out in order to assess the range of crab sizes and the shell species available. Shore Survey The collecting area was the North Down coast, Northern Ireland ; specifically, between the towns of Millisle and Donaghadee . The shore in this area is a mixture of sand and rock with many pools remaining at low tide . Collections were made in January and February 1977 and 1978 . The lower shore was searched and all gastropod shells which were found were examined . Those still containing the snail were discarded . The remaining shells were grouped into shell species and whether or not they contained a crab . The hermit crabs, all Pagurus bernhardus, are found to occupy seven main shell species. The smallest crabs (0 . 03 to 0 . 60 g) are found in Littorina littoralis, L . saxatilis, Gibbula cineraria and G. umbilicalis shells . The two Gibbula species are characterized by differences in shell markings but, since worn shells of these species are often difficult to segregate, they were grouped together in the analyses as Gibbula shells . Medium sized crabs (0 .3 to 1 . 8 g) are found in L. littorea or Nucella lapillus, while the largest crabs (1 .4 to 7 .6 g) are found in Buccinum undatum shells. The weight distributions of crabs occupying the most abundant shell species (Table I) : L. littoralis, Gibbula spp ., Nucella and L. littorea, are shown in Fig . 1 . The majority of crabs in L. littoralis (98-7%) and Gibbula (91-5%) shells are less than 0 . 5 g; however, the majority of crabs in Nucella (80 .3 %) and L. littorea (79 . 8 %) shells are between 0 . 5 and 1 . 5 g. Crabs between 0.3 and 0 . 6 g appear to have a choice of all

941

four of these species, but crabs smaller or larger than this appear to have a more restricted choice of shells . The numbers of occupied and empty shells found during the shore survey are given in Table I, which shows that some species are considerably more common than are others . Furthermore, different proportions of the different species are occupied by crabs . L. littoralis are occupied significantly more than are the Gibbula shells (91 % against 59%, x2 153 P < 0 .001) . However, Nucella and L. littorea are both occupied to the same extent (94 %) . The high percentage of shells occupied by P . bernhardus (87 % overall) suggests that shell availability may be a limiting factor for the crab population . That shell availability is a limiting factor for certain crab populations has been demonstrated previously (Vance 1972b ; Spight 1977) . The highest levels of occupancy appeared, from Table I, to be for the larger shell species . This suggests that competition for shells may increase as the crabs develop . The significant difference between the levels of occupancy of L. littoralis and Gibbula shells suggests the possibility that the former species is preferred by the crabs and that those crabs unable to locate a suitable L . littoralis shell will be forced to take a Gibbula shell, other species being rare . There is, however, an alternative hypothesis which relies, not on selection by crabs, but on selection by physical forces . L . littoralis shells of a given weight tend to have a larger internal volume than do Gibbula shells of that weight (Fig . 2) . Thus, the former may be more liable to movement by wave action and would be removed from the lower shore more readily than would Gibbula shells . This would result in a high proportion of unoccupied Gibbula shells . The first hypothesis is examined in the following experiment. The second hypothesis was not within the scope of this study .

Table I . Results of the Shore Survey

L . littoralis Gibbula L. saxatilis and others

small crabs

Nucella L . littorea

medium crabs

Buccinum undatum

large crabs

Vacant

Occupied

Total

102 97 7

989 137 20

1091 234 27

91 59 74

10 5

152 78

162 83

94 94

0

6

6

100

% Occupied



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ANIMAL BEHAVIOUR, 27,

Experiment 1 : Selection between L . littoralis and Gibbula Shells Crabs were collected and maintained overnight in large plastic containers with about 4 cm of well aerated sea water at 10 C . The crabs were grouped according to the species of shell in which they were found . The following morning 30 crabs in Gibbula shells were placed in each of two large containers in which were 45 empty L . littoralis shells . Thirty crabs in L . littoralis shells were also placed in each of two containers in which were 45 Gibbula shells . A wide range of shell sizes were used in each case. The experiment was monitored, initially after 3 h, and then four times daily for four days, and the number of crabs housed in each shell species was recorded on each occasion . As the numbers of crabs in each species of shell varied over the four days the median number in each species was calculated . Thirty-eight crabs out of the 60 originally in Gibbula shells changed to L . littoralis shells, 30L.litforalis 20-

10-

Gibbula spp.

3

while only eight of those originally in L . littoralis changed to Gibbula shells (x 2 7 . 5, P < 0 .01) . Thus, on average, 25 % of the crabs were in Gibbula shells, and 75 % in L . littoralis shells. Even allowing for a possible measure of differential selection by wave action against L . littoralis shells these data clearly demonstrate a strong preference by small crabs for these shells which may account for the observed levels of occupancy . There are several possible reasons for the preference for L . littoralis shells. Crabs of a given size occupy heavier shells when in Gibbula than when in L . littoralis (personal observation) . It has also been determined that the latter species has a greater internal volume to weight ratio (Fig . 2) . Therefore crabs which select L . littoralis of suitable volume obtain shells which weigh less than do Gibbula shells of the same volume . It appears from these data that crabs select shells with a high internal vol ./wt ratio ; this is in agreement with conclusions of Grant (1963) concerning P. acadianus. However, other factors such as the internal shape of the shell (Fig . 1), or the angle of the columellar to the substrate, may also be influencing the choice (Reese 1962) . It can be seen from Fig. 1 that the great majority of crabs weighing less than 0 . 5 g are found in either Gibbula or L . littoralis shells, and that above this weight they tend to be found in L. littorea or Nucella shells. The shore survey revealed that 94 % of shells of these last two species are occupied and that no preference for a 25-

0 N .lapil lus 20-

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L littorea

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- 1 111"7 1 6 8 10 12 Weight of the crabs (g )

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