Colonization of a shell resource by calyptraeid Gastropods: Tests of habitat selection and preemption models

J. Exp. Mar. Biol. Ecol., 1986, Vol. 99,

pp. 79-89

79

Elsevier

JEM 702

COLONIZATION OF A SHELL RESOURCE BY CALYPTRAEID GASTROPODS: TESTS OF HABITAT SELECTION AND PREEMPTION CODED

M. ANDREW SHENK and RONALD 11. KARLSON Ecology and Organismic Biology Program, School of Lif and Health Sciences. University of Delaware, Newark, DE 19716, U.S.A.

(Received 13 September 1985; revision received 13 March 1986; accepted 18 March 1986) Abstracti The influence of patch size, habitat selection, and preemption on the colonization of a patchy resource by three sympatric gastropod species (Cupola L.) was evaluated. These species are common epifaunal associates of hermit crabs. Althoqh adult populations exhibit strongly divergent resource utilization patterns, these patterns are not generally the result of divergent colonization processes. All three Crepidula species selectively colonize small shells rather than large shells, are strongly inhibited from colonizing shells dominated by the colonial hydroid Hydractinia echinata Fleming (but not by the colonial bryozoan Alcyonidiumpolyoum Hassall), and co-occur on individual shells in the absence of other epifauna. The field distribution patterns of Crepidula species are not wholly the result of divergent colonization patterns. These results suggest that significant post-colonization biological interactions also affect Crepidula distribution patterns. Key words: colonization; competition; habitat selection; patchy resources; preemption

INTRODUCTION

Ecologists study the distribution patterns of species in nature and seek to explain the patterns in terms of abiotic a$,bibiptip pr9Epsses (May, 1984). Distribution patterns generally result from at least three classes of biological events: (1) production of dispersal stages; (2) colonization of ~crohabitats by dispersal stages; and (3) postcolonization biological ~teractions. For many species, colonization is highly significant because it influences both the ability of individuals to produce future dispersal stages and the probability of interspecific encounters. Recent studies show that many invertebrate taxa are capable of sophisticated methods of habitat selection and that habitat preference &II play a major role in determining the distributions of species (Meadows & CampbLS, 1972; O’Connor et al., 1980; Grosberg, 1981; Sebens, 1981). In this paper we describe the microhabitat distributions of three marine gastropod species and examine the contribution of colonization events to their ~s~bution patterns. These three species are members of the genus Crepidtiu, members of a predictable epifaunal assemblage on hermit crab-occupied gastropod shells. These three species 0022~0981/86/$03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)

80

M. ANDREW

SHENK AND RONALD

have broadly overlapping

geographic

ranges (Hoagland,

overlap

distributions.

C. convexa

occupied & Franz,

in microhabitat

H. KARLSON

1975, 1977, 1979), but limited

Say is common

by the hermit crab Pagunrs Zongicalpus Say (Franz 1971; Karlson

& Cariolou,

& Hendler,

on small

shells

1970; Hendler

1982). Crepidulu fomicatu is common

on large

shells occupied by the hermit crab Pugurus pollicarik (Hoagland, 1977; Karlson & Shenk, 1983) and Crepidulaplana Say is common on the inner surface of shells occupied by Pugurus poZZicaris(Hoagland, 1977, 1979). In this paper, we describe two field experiments, a habitat selection experiment and a preemption experiment, which were designed to assess the contribution of colonization events to microhabitat distribution patterns. We define Crepidula colonists as juvenile and adult individuals which colonized experimentally introduced shells and Crepidtda residents as individuals living on shells in field samples. Our habitat selection experiment was designed to test two null hypotheses: (1) that the microhabitat distribution pattern of Crepidufa colonists is not different from the distribution pattern of Crepidula residents of each species; and (2) that the microhabitat distribution of colonists does not differ among Crepidula species. The first hypothesis addresses the general question: are the microhabitat distribution patterns of Crepidula residents the result of microhabitat selection by Crepidula colonists? The second hypothesis, a subset of the first, addresses the question: are the distribution patterns of colonists different from each other? Many benthic assemblages are characterized by strong negative interactions between resident individuals and newly arrived colonists (Jackson, 1977; Sutherland & Karlson, 1977; Karlson, 1978). The preemption experiment was designed to test the null hypothesis that the microhabitat distribution patterns of Crepidulu colonists are not affected by the presence of colonial epifauna on experimental shells. The hermit crab epifaunal assemblage is made up of several species in addition to the Crepidula species (Karlson & Cariolou, 1982; Karlson & Shenk, 1983). Two common epifaunal species, the hydroid Hydractinia echinata Fleming and the bryozoan Alcyonidium polyoum (Hassall), were used to test for the effects of preemption of space on shells on the distribution patterns of the Crepidula species. These two experiments allow us to test for the effect of colonization events on the microhabitat distributions of the CrepiduZu species. It has been suggested that the Crepidula species have developed microhabitat preferences which reduce the microhabitat overlap between species (Hoagland, 1979). Our results show that for one species, C. convexa Say, habitat selection does have a significant effect on distribution. The other two species show significant effects of both habitat selection and preemption on colonization, but these effects are not sufficient to explain the field distribution patterns. We use our findings to predict significant post-colonization interactions which also influence Crepidula distribution patterns.

SHELL ~LONIZATION

BY C~P~~U~~

SPP.

81

METHODS

The field sampling and experiments were conducted in the Thimble Islands in Long Island Sound near Stony Creek, Connecticut. In this study area, hermit crab-occupied gastropod shells are the principal substrata for Crepidula. In other portions of their geographic ranges, the Crepidula species commonly occur on shell debris, rocks, eelgrass, and rn~-made structures (Franz & Hendler, 1970; Hoagland, 1977, 1979). Field samples of Pagurus lmgicarpus Say and P. pollicaris Say were collected, using SCUBA, at depths of 3-4 m near Baine’s Island, Smith Island, and Wayland Island, at lo-20 day intervals from June to September 1982. Each sample consisted of all crabs encountered during 1 h of searching. Crabs with vagile epifauna were bagged individually in sea water within 1 h of collection. All of the shells occupied by P. Iongicalpus were censused within 2 h of collection using a steromicroscope. The shells occupied by P. ~llica~ were preserved in 4% formalin in sea water. Shell length and width were measured to the nearest mm using vernier calipers. Density estimates for the Crepidula species were based on counts of the total number of individuals of each species on the outer and inner surface of shells. In both field experiments, we used tethered Busycon carica (Gmelin) shells as substrata (Rittschof, 1980; Karlson 8c Cariolou, 1982). Each shell was attached to a transect line using 0.5 m of monostrand stainless steel wire. Shells were spaced along the transect lines at l-m intervals. The transect lines were anchored along the bottom in an array running east-west at a site just north of Baine’s Island. At each census we recorded the number of each Crep~la species on the outer surface of the shells. In order to avoid evicting the hermit crabs from experimental shells, we did not census the inner surface of shells. The habitat selection experiment was designed to test for the effect of differential colonization of shells on the microhabitat distribution of Crepidula species. We provided a broad size range of shells for colonization and compared the distribution of colonists on experimental shells to the distribution of residents in field samples. Forty Busycon carka shells were divided into four size classes (O-100 cm2, 101-200 cm’, 201-300 cm2, 301-400 cm2) based on the estimated surface area of each shell. The shells ranged in size from 16 to 400 cm2. Surface areas were estimated by covering 20 shells with aluminum foil, weighing the foil, and comparing the weights to standards of known area. Linear regression models, using estimated areas and a shell parameter (i.e., width, height, aperture), were constructed. The best predictor of shell area was shell width (log area = 1.9618 x log width + 0.6249; R2 = 0.99). The 40 shells were assigned randomly to four transect lines. The experiment began on 5 August 1982 and the shells were censused for Crepidula colonization at 12-24 day intervals. The experiment was terminated on 19 October 1982. The preemption experiment was designed to test the hypothesis that colonial species influence the shell colonization pattern of the three Crepidula species. The null hypothesis of the experiment was that the density of Crepidula colonists did not differ between

TABLE

I

(26) 0.03%, o.o-0.13% 0.27x,

(126) 0.332, 0.21-0.46% (5) 0.07%, 0.02-0.13%

Hydractinia spp.

Membranipora tenuis

Podocoryne carnea

Bare space

Balanus spp.

(23) 19.08%, 11.03-28.71%

0.18x, 0.12-0.24% 55.05%, 51.40-58X5% (330)

(14)

35.88%,

(93) 5.53%,4.11-7.05%

0.49x, 0.22-0.85x 13.08%, 9.14-17.592 (6)

(2)

0.06-0.95 %

25.16-46.69%

2.387* 8.089**

1.550 NS

2.172*

4.116**

7.934**

3.247*

4.40 1** 24.896**

0.0786 no.’ + 0.0260 0.7424 no. + 0.1584

Student’s t-test

0.0053 no. kO.0059

0.0754 no. + 0.0145 0.0034 no. * 0.0019 0.0116 no. + 0.0070 6.53x, 5.14-8.07x

Shell size range: 10.11-299.79 cm*

Shell size range: 0.74-37.09 cm2

Crepidula convexa Crepidula fornicata Crepidula plana Alcyonidium polyoum

P. pollicaris n = 111

P. longicarpus n = 945

Crab species

Epifaunal abundance patterns on hermit crab shells from Long Island Sound: data are presented as mean percent cover (%) or mean number per cm2 (no.), and 95% confidence limits; number of shells with > 90% of a species is given in parentheses; Crepidulu plana was found only on the inner surfaces of shells; percent cover data were transformed using the arc-sine transformation (Sokal & Rohlf, 1981); NS = P > 0.05; *P < 0.05; ** P < 0.001.

SHELL COLONIZATION

BY CREPIDULA SPP.

83

epifauna-free shells and those covered by one of the two most common colonial species in this assemblage, Alcyonidium and Hydructiniu. One hundred and twenty Busycon carica shells were allocated to Alcyonidium, Hydructinia,, and epifauna-free (control) treatments with 40 shells per treatment. To control for ‘the potential effects of shell surface area, all of the shells in this experiment were within the 101-200 cm2 size class. The Alcyonidium and Hydructiniu shells had > 90% cover of the appropriate colonial species. The epifauna-free, control shells were brushed to remove all epifauna. The shells were assigned randomly to 10 transect lines and introduced to the habitat on 15 June 1983. The shells were censused at 13-21 day intervals for Crepidulu colonization. The experiment was terminated on 28 September 1983.

RESULTS

Analysis of field shell samples reveals that most,epifaunal species were signiticantly more abundant on shells occupied by Pagurus pollichnk than on those occupied by P. longicarpus (Table I). Only Crepidulu convexa Say, with over an order of magnitude higher density, was significantly more abundant on shells occupied by Pugurw longicarpus (Table I). Density estimates for the three Crepidulu species were also calculated for each of three shell-size classes among shells occupied by Paguruspollicaris (Fig. 1). Only Crepiduh fomicuta (L.) exhibited a significant shell-size effect (Table II) with densities increasing with shell size (Fig. 1). C. plunu Say was found only on the inside of these shells. These data clearly establish the ditferent distribution patterns of Crepidula residents. TABLE II ANOVA summary for field densities of Crepidulu species across three shell size classes: data were transformed using the log transformation, constant = 1.0 x 10e6 individuals per cm’; NS = P> 0.05, * P < 0.05. C. convexa

C. fomicata

C. plana

Source of variation

d.f.

MS

F

MS

F

MS

F

Shell size Error Total

2 108 110

3.259 8.170

0.399 NS

228.59 29.29

7x04*

17.38 8.499

2.045 NS

In the habitat selection experiment, the three Crepidulu species colonized the outer shell surfaces of shells in all four shell-size classes (Fig. 2). Each species exhibited signiticant shell size effects (Table III) with densities decreasing with increasing shell size (Fig. 2). When we compar&:the microhabitat distribution of colonists in the habitat-selection experiment with the-distribution of residents of each species in field samples, we found significant differences for both C. fomicatu and C. plana. Com-

84

M. ANDREW

SHENK

AND RONALD

H. KARLSON

C. convexa

0.05 no./cm2 0.0 L

12

3

C. plana

Gfornicata

0.30

I .o

0.25 0.20 0.15 no/cm2

0.50 no./cm*

0.10

123 Shell Size Class

Shell Size Class

Fig. 1. Mean field density k 95% confidence limits for three Crepiduh species in three shell size classes: all shells were occupied by Puguruspollicuris; size class 1 = O-100 cm2 (n = 75); 2 = 101-200 cm2 (n = 24); 3 = 201-300 cm2 (n = 12).

TABLE III ANOVA summary for densities data were transformed using

of Crepidulu colonists across four shell size classes in the experiment: the log transformation, constant = 1.0 x 10e6 individuals per cmZ; * P < 0.05. C. convexa

C. fornicutu

C. pluna

Source of variation

d.f.

MS

F

MS

F

MS

F

Shell size Error Total

3 36 39

14.93 3.549

4.207*

10.02 3.409

2.939*

10.28 3.412

3.013*

parison of cumulative relative frequency distributions (Fig. 3) indicates that a significantly higher frequency of C. fornicata colonists were found on small shells than among the C. fornicata residents in field samples (Kolmogorov-Smimov test, D = 36.4%, P < O.Ol), and a significantly lower frequency of C. plana colonists were found on small shells than were C. pfana residents (Kolmogorov-Smimov test, D = 9.2%, P < 0.01).

SHELL COLONIZATION

BY CREPHKJLA

SPP.

85

C. plana 0.25

T

T

0.05 no./cm* 0.0

I234

0.10 no./cm* 0.05 0.0

no

&.fornicata

l-li_AL I234 Shell Size Class

Shell Size Class

Fig. 2. Mean density of colonists +_95% confidence limits for three Crepidula species in four shell size classes: size class 1 = O-100 cm2 (n = 10); 2 = 101-200cm’ (n = 10); 3 = 201-300cm2 (n = 10); 4 = 301-400 cm2 (n = 10).

There was no significant frequency difference between the distributions of C. convex0 colonists and residents (Kohnogorov-Smirnov test, D = 24.5%, x2 = 3.01, P > 0.20). The second null hypothesis for the habitat selection experiment was that there is no difference in the distribution of colonists between the three species. Between species comparisons of the cumulative relative frequency of colonists show that the frequency of Crepidula convexa > the frequency of C. fomicata > the frequency of C. plana on small shells (Fig. 3). The difference between C. convexa and C. jbmicata is significant (Kohnogorov-Smirnov test, D = 28.8 %, P < 0.025) as is that between C. fomicata and C. plana (Komogorov-Smirnov test, D = 19.1x, P < 0.005). These data suggest differential colonization ability among Crepidula species on the basis of shell size. In the preemption experiment, we compared the density of each Crepidula species on epifauna-free shells and shells dominated by Alcyonidium or Hydracti~ia. Hydractinia clearly inhibited colonization by all three Crepidzda species. After 15 wk, the total numbers of colonists on Hydractinia-dominated shells were 0,4, and 0 for C. convexa, C. fimicata, and C. plana, respectively. Comparisons of mean colonist densities at the terminal census (28 September 1983) alI indicate highly significant differences among treatments (Fig. 4). These data indicate strong preemption by Hydvactinia, but there is no evidence for different responses among CrepiduZa species. DISCUSSION

Our data strongly indicate that postcolonization processes modify the frequency distribution of C. plana and C. fomicata whereas they do not alter that of C. convexa

M. ANDREW SHENK AND RONALD H. KARLSON loo

C. convexa

80 1

r

60-

:

-

%

:.

;...:

:‘.-.

:“’ ”

,..:

c :

0

,

50

ioo-

100

150

ZOO

250

300

250

xx)

C. Diana

80. 60. %

. 40.

0

50

loo

Shell

150

Size

(mm)

Fig. 3. Cumulative relative frequency of Crepidda colonists and residents as a function of shell size: sample sizes for colonists (c) and residents (r) were 41 and 18 for C. convexa, 119 and 1046 for C. fhicatu, and 638 and 6949 for C. plano.

SHELL COLONIZATION

0.05-

BY CREPZDULA SPP.

87

C. convexa

no./cm2

6/15 6/28

7/12

727

8/11 8/24

917

9/28

DATE Fig. 4. Mean density of colonists 4 95 % confidence limits (n = 40) for three Crepidulu species in three shell treatments: a, epifauna-free, control, A, ~-90% cover of Alcyonidium, and D = >90% cover of Hydructinia; Kruskal-Wallis three sample tests for data from 28 September; C. convexa, H = 19.01, P < 0.001; C. jiimicata, H =-47.57, P < 0.001; C. plana, H = 55.79, P < 0.001.

(Fig. 3). This is especially true for C. plana whose distribution is normally restricted to the inner surface of shells (Table I). The densities of C. plana colonists on the outer surfaces of experimental shells were the hieest among the three Crepidula species (Figs. 2 and 4). The influence of habitat selection on the microhabitat distributions of Creptiula residents would appear to be greatest for C. convexa, least for C. phna, and only marginally important for C. jbrnicata (given the large divergence in cumulative relative frequencies between colonists and residents in Fig. 3). Our data do not support the hypothesis that preemption by either Hydractinia or Alcymidium results in divergent colonization patterns among Crepiduh species. All three Crepidula species rarely colonized shells covered by Hydracfinia and showed no divergent response on Alcyonidium-dominated shells. Although Hydractinia is more common on large shells than small shells (Karlson & Cariolou, 1982; Karlson & Shenk, 1983 ; Table I) and it strongly inhibits Crepidula colonization, we found that colonization of large shells was low even in the absence of this colonial species (Fig. 2). We therefore

88

M. ANDREWSHENKANDRONALDH.KARLSON

reject preemption as an important factor influencing the microhabitat distribution patterns of Crepidula species. The results of these colonization experiments allow us to make some predictions about postcolonization events which may contribute to CrepiduZa distribution patterns. First, we found significant between-species differences in the relative frequency distributions of colonists as a function of shell size. This finding allows us to hypothesize that interspecific competition between Crepidula species during shell colonization produces the field distribution patterns of the species. The high colonization rates of C. convexa onto small shells may reflect negative interactions with congeners on large shells. Similar interactions between C. fomicata and C. plana are also compatible with our results. Secondly, differential survivorship of the Crepidula species in different microhabitats may produce the distribution patterns of the species. We note that C. plana, which has a thin shell and lacks a strong muscular attachment between the body parts and the shell (Hoaghtnd, 1977), colonized the outer surface of experimental shells in large numbers. This species may suffer high mortality on the outside of shells and have a significant refuge inside shells. The effects of interspecific competition and predation on the microhabitat distribution patterns of Crepidula within this assemblage are currently being experimentally evaluated.

ACKNOWLEDGEMENTS

We wish to thank L. W. Buss and the Yale Peabody Museum Field Station for providing us with laboratory space and boat use. M. Carriker, T. Hughes, L. Hurd, D. Levitan, R. Osman, and an anonymous reviewer provided thoughful comments on earlier versions of the manuscript. Funds were provided by the School of Life and Health Sciences, University of Delaware; the Explorer’s Club of America; the LemerGray Fund for Marine Research; and NSF grant No. OCE 82-14827.

REFERENCES FRANZ, D.R. & G. HENDLER,1970. Substrate diversity and the taxonomy of Crepiduh convexu (Say) (Gastropoda : Prosobranchia). Corm. Occur. Pap. Biol. Sci. Ser., Vol. 1, pp. 281-289. GROSBERG,R.K., 1981. Competitive ability influences habitat choice in marine invertebrates. Nature (London), Vol. 290, pp. 700-702. HENDLER,G. & D.R. FRANZ, 1971. Population dynamics and life history of Crepiduh convexu Say (Gastropoda : Prosobranchia) in Delaware Bay. Biol. BUN. (Woods Hole, Muss.), Vol. 141, pp. 514-526. HOAGLAND,K. E., 1975. Patterns ofevolution and niche partitioning in North American Crepidtdu (Gastropoda : Calyptraeidae). BUN. Am. Malacol. Un., 1975, pp. 52-53. HOAGLAND,K.E., 1977. Systematic review of fossil and recent Crepidula and discussion of evolution of the Calyptraeidae. Muhcologiu, Vol. 16, pp. 353-420. HOAGLAND, K. E., 1979. The behavior ofthree sympatric species of Crepiduu (Gastropoda : Prosobranchia) from the Atlantic, with implications for evolutionary ecology. Nuurilus,Vol. 94, pp. 143-149. JACKSON,J. B. C., 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am. Nut., Vol.111, pp.743-767. KARLSON,R. H., 1978. Predation and space utilization patterns in a marine epifaunai community. J. Exp. Mar. Biol. Ecol., Vol. 31, pp. 225-239.

SHELL COLONIZATION

BY CREPIDULA SPP.

a9

KARLSON,R. H. & M. A. CARIOLOU,1982. Hermit crab shell colonization by Crepidula convexa Say. 1. Exp. Mar. Biol. Ecol., Vol. 65, pp. l-10. KARLSON,R. H. & M. A. SHENK, 1983. Epifaunal abundance, association, and overgrowth patterns on large hermit crab shells. J. Exp. Mar. Biol. Ecol., Vol. 70, pp. 55-64. MAY, R.M., 1984. An overview: real and apparent patterns in community structure. In, Ecologicul communifies, edited by D. R. Strong et al., Princeton University Press, Princeton, New Jersey, pp. 3-16. MEADOWS,P. J. & J. I. CAMPBELL,1972. Habitat selection by aquatic invertebrates. Adv. Mar. Biol., Vol. 10, pp. 271-382. O’CONNOR,R. J., R. SEED St P. J. S. BOADEN,1980. Resource space partitioning by the Bryozoa of a FUCUS serrutus L. community. J. Exp. Mar. Biol. Ecol., Vol. 45, pp. 117-137. RIT~SCHOF,D., 1980. Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. J. Gem. Ecol., Vol. 6, pp. 103-l 18. SEBENS, K. P., 1981. Recruitment in a sea anemone population: juvenile substrate becomes adult prey. Science, Vol. 213, pp. 785-787. SOKAL, R.R. & F.J. ROHLF, 1981. Biometry. W.H. Freeman & Co., San Francisco, Calif., 2nd edition, 859 pp. SUTHERLAND,J.P. & R.H. KARLSON, 1977. Development and stability of the fouling community at Beaufort, North Carolina. Ecol. Monogr., Vol. 47, pp. 425-446.