Habitat restrictions in early benthic life" experiments on habitat

J. Exp. Mar. Biol. Ecol., 157 (1992)91-114 © 1992 Elsevier Science Publishers BV. All rights reserved 0022-0981/92/$05.00

91

JEMBE 01740

Habitat restrictions in early benthic life" experiments on habitat selection and in situ predation with the American lobster Richard A. Wa'&~e ~' ~::~1 R,-:~bei°t S. Steneck b "Department of Zoology and Darling Marine Center. University of Maine, Orono, Maine, USA; bDepartment of Oceanography and Darling Marine Center, UniversiO'of Maine, Orono, Maine, USA (Received 25 October 1990; revision received 30 October 1991; accepted 3 December 1991) .

.

Abstract: In shallow marine environments, many animals that eventually attain large body size and range widely are restricted to refugia early in life. A prime example is the American lobster Homarus americanus Milne Edwards. During the first few years of benthic life, lobsters are most strongly associated with shelter providing habitats (e.g., cobble) but this association is less frequent as they grow. The restricted distribution of such early benthicphase lobsters (5- ~ 40 mm carapace length, CL) may be reinforced by predation, but experiments to quantify predators and predation rates in situ have not been reported. This study confirms previous habitat selection studies in showing that shelter-seeking behavior is likely the proximate cause of the association, but that predation probably reinforces the association until lobsters outgrow their most vulnerable size. Field predation experiments and video observation show that tethered early benthic ptmse lobsters were attacked by demersal fishes and crabs significantly more often when unsheltered by cobble, and that this vulnerability declines dramatically with increasing body size. Moreover, many of the species of fish and crab predators observed by video were common at the five sites censused in mid-coast Maine, and occur throughout the range of the American lobster. There is strong evidence that lobsters and their macruran (large abdomened) allies in shallow marine and aquatic environments are similarly restricted to shelter-providing habitats early in their benthic life, possibly because of their inability to avoid predators by rapidly burying themselves in sediment.

Key words: Body size scaling: Bottleneck: Habitat shift' Homarus americamts; Predation risk; Substratum selection

INTRODUCTION

Associations of small animals with structurally complex habitats are common in nature, although the ecological processes that bring about these patterns are not always obvious. Populations may be restricted to habitats that create spatial refugia through differential mortality or through active habitat selection (Taylor, 1984; Sih, 1987). In shallow marine and aquatic environments, both differential predation (Woodin, 1978; Summerson & Peterson, 1984; Sih et al., 1985; Witman, 1985; Aronson, 1989), and Correspondence address: R.A. Wahle, Program in Ecology and Evolutionary Biology, Box G-W, Brown University, Providence, RI 02912, USA. Darling Marine Center Contribution 242.

92

R.A. WAHLE AND R.S. STENECK

habitat selection in response to predatiol~ (Coen et al., 1981; Leber, 1985; Main, 1987; Schlosser, 1987) have been shown to resuk in associations of small mobile animals with structural refugia. But, certain relatively large-bodied benthic and demersal animals with small juvenile forms can exhibit a relaxed association or an outright habitat shift as they grow (Stein & Magnuson, 1976; Werner & Gilliam, 1984; Kneib, 1987; Schlosser, 1987). Such habitat restrictions early in life can create a demographic bottleneck limiting the number of individuals surviving to adulthood (e.g., Werner & Gilliam, 1984; Reaka, 1987; Moran & Reaka, 1988; Quinn & Janssen, 1989). The American lobster Homarus americam~s Milne Edwards is the largest benthic decapod crustacean in the northwest Atlantic and spans approximately four orders of magnitude in body size from ~ d. 1 g at settlement to several kg as an adult. Despite its commercial importance, little was known until recently about the habitats of juvenile lobsters. Recent studies have documented a strong association of recently settled and relatively small lobsters 5 - ~ 40 mm carapace length (CL) with structurally complex habitats, especially cobbles, but also mussel and kelp beds (Hudon, 1987; Wahle, 1990; Wahle & Steneck, 1991), and subtidal salt marsh peat reefs (Able et al., 1988). Because thi~ group of smaller lobsters is demographically distinct, we refer to it as the earl), benthic phase (see Wahle, 1990, and Wahle & Steneck, 1991, for further explanation). These small lobsters are virtually absent from structurally simple habitats such as sediment or featureless bedrock (Hudon, 1987; Hudon & Lamarche, 1989; Wahle, 1990; Wahle & Stcneck, 1991) where larger lobsters are commonly found. Apparently, the association with shelter-providing habitats relaxes as lobsters grow (Hudon, 1987; Wahle, 1990; Wahle & Steneck, 1991) and become more mobile (Campbell & Stasko, 1985; 1986; Krouse, 1980; 1981). Observations consistent with this pattern are that predator avoidance behaviors decline with greater body size (Lang et al., 1977; Wahlc, 1990). Little information exists, however, on predation on lobsters in nature. This study examines the role of habitat selection and predation in explaining the restricted distribution of early benthic phase lobsters. Previous studies suggest that predation may play an important role in restricting the distribution of early benthic phase lobsters. Certain fishes have long been implicated by their stomach contents to prey on the American lobster (Herrick, 1909; Bige!ow & Schroeder, 1953; Ojeda, 1987). Experiments with enclosed predators have demonstrated lower rates of predation on juvenile lobsters in structurally complex habitats than in simple ones (Roach, 1983; Lavalli & Barshaw, !986; Richards & Cobb, 1986; Johns & Mann, 1987; Barshaw & Lavalli, 1988). It is tempting to speculate that predation makes shelter an essential resource for small lobsters. However, such laboratory and field enclosure studies cannot be extrapolated to indicate the occurrence of predators in nature. Although field studies of predation on spiny lobsters support such speculation (Herrnkind & Butler, 1986), there have been no quantitative studies of predation on clawed lobsters in the field. Shelter-use in the American lobster is well documented (Cooper & Uzmann, 1980) and ritualized agonistic interactions between lobsters for shelter (Scrivener, 1971)

HABITAT RESTRICTIONS IN EARLY BENTHIC LIFE

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suggest shelter limitation has been an important part of the evolutionary history of lobsters. This is, in part, the basis for proposals that some lobster populations experience a recruitment bottleneck imposed by the availability of suitable habitat (Caddy, i 986; Fogarty & Idoine, 1986). However, what exactly constitutes suitable habitat for early benthic phase lobsters has been a question of some debate. The debate partly stems from the behavioral plasticity of postlarval arid early benthic phase lobsters with respect to habitat selection. For example, postlarval lobsters can delay settlement for some time until they find a habitat with pre-existing shelter, but they can also successfully settle in featureless sediment (Cobb, 1968; Barshaw, 1988). Early benthic phase lobsters appear to prefer to occupy shelter-providing habitats (Pottle & Elner, 1982), but they are also known to be adept burrowers, able to construct U-shaped tubes in featureless sediment (Berrill & Stewart, 1973; Botero & Atema, 1982) which have been observed in nature, albeit rarely (McKay, 1926). The rarity with which small lobsters are observed in open habitats in nature raises questions as to the consequences of occupying such habitats. If the negative consequences on fitness are minimal then there is little support for the existence of a demographic bottleneck. Here we address the roles of habitat selection and predation under three major objectives. First, we built on previous habitat selection studies to determine whether early benthic phase American lobsters prefer to occupy the substratum where they are most abundant in nature. Second, we identify predators from direct video observation of tethered lobsters and determined their distribution and abundance in our study area. Third, we did field experiments to determine whether predation rates on tethered lobsters are significantly lower in the preferred habitat and examined how predation risk varies with body size. MATERIALS, METHODS AND STUDY SITES HABITAT SELECTION EXPERIMENTS

In this study, laboratory experiments on substratum selectivity expand on the previous work of Pottle & Elner (1982) by placing tighter controls on the sizes of available shelters. These short-term experiments were designed to: (1)establish whether early benthic phase lobsters exhibit a substratum preference given a choice of mud, sand, gravel, or cobble; and (2)examine the tendency of a lobster to accept or reject a substratum depending on available shelter sizes. All experimental animals were collected in the wild and were in captivity for ~< 10 wk before use. Animals were maintained at 10-12 °C in the flowing seawater facility at the University of Maine's Darling Marine Center, Walpole, Maine. All experiments were conducted in a flow-through system at the same temperature with overhead fluorescent lighting. Consistent with the methods of Pottle & Elner (1982), a lobster was recor6ed as having selected a shelter site when it was either partly or entirely concealed by the substratum and apparently immobile.

94

R.A. W~HLE AND R.S. STENECK

Substratum preference experiment Substratum preference experiments were conducted in a rectangular (76 x 61 x 20 cm) fiberglass tank divided into four equal quadrants with sieved size grades of mud ( ~ 0 . l - m m diameter), sand (1-2 mm), and gravel (10-20mm), and haod-selected cobble (80-110 mm). Substrata were contained in four 38 x 30.5 x 10-cm deep plastic basins that snugly fit together to completely fill the bottom of the tank. The basins were filled to capacity with substratum to permit lobsters unrestricted movement between them. Seawater entered at the center underneath the basins and exited at one corner of the tank. Each lobster was given a 5-min trial after a 5-min acclimation period confined by a cylindrical barrier [a 10-cm section of 4-in (10.2 cm)diameter PVC pipe] to a circular PVC starting platform at the center of the tank. When the barrier was removed the lobster could move freely from the platform with equal access to each substratum. The time spent on each substratum and the lobster's location at the end of the trial ("final choice") were recorded for 39 lobsters ranging in size from 6 to 35 rnm CL. Preliminary trials demonstrated that the choice of substratum was independent of the configuration of the four substrata ( Z 2 = 0.017, 0.71 < p < 0.90, n = 9 trials in each of two configurations) ruling out artifacts introduced by the experimental design. All trials were done in a single day. We used a X2 test (with ~ = 0.5) against the null hypothesis that lobsters would only occupy cobble in proportion to its availability (i.e., the ratio of lobsters occupying cobble to those on the other three substrata combined would be 1:3). Lobsters, however, were not expected to sample all substrata before making a choice, and therefore cannot be said to have rejected substrata not sampled. Because it is possible that the choice can depend on the sequence in which the substrata were encountered, it was necessary to do a second experiment which narrowed the choices.

Substratum size prt,/erem'e e.weriment This experiment examined the possible relationship between lobster body size and substratum size preference, and in so doing resolved the "sequence-of-encounter" problem stated above. In this experiment only half the experimental tank was used (a 38 x 31-cm area) accommodating two substratum basins, one with 30-mm and the other with 100-ram maximum diameter' rocks. Rocks were selected such that the length to width ratio was < 2. Thus, more or less spherical rocks were selected, placing limits on the size and shape of interstitial spaces. 30 lobsters were used in this experiment, ranging in size from 7 to 34 mm CL. Each lobster experienced two trials, one starting in the 30-ram substratum ("pebble") and the other starting in the 100-mm ("cobble"). In each trial a lobster had the option of staying on the substratum where it started or moving to the other. As in the previous experiment, acclimation and trial times were 5 rain and time spent on a substratum and "final choice" were recorded. These trials were completed over 2 consecutive days. To normalize the data, we arcsine-squareroottransformed proportions of time on a substratum before testing the significance (~ - 0.05) of linear regressions on body size.


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PREDATOR ABUNDANCE

Predator groups The video-monitored predation experiments described below identified a set of predators which we report from previous field censuses. The predators include two species of crab, Carcinus maenas (Linnaeus) and Cancer irroratus Say, and a diverse assemblage of benthic and demersal fishes. The crabs ranged in size up to ~ 10 cm in carapace width. Because some of the fishes are difficult to identify in the field, we placed them in four functional groupings indicated as follows along with the approximate body length range we observed: (1) cunner Tautogolabrus adspersus (Waldbaum), ~ 8-15 cm; (2) sculpins, i.e., short horn sculpin (Myoxocephalus scorpius (Linnaeus) and grubby M. aeneus (Mitchell), ~ 6 - 1 6 cm, and sea raven Hemitripterus americanus (Gmelin), 12- 25 cm; (3) flounder, winter flounder Pseudopleuronectes american,,is (Waldbaum), ~ 8 - 1 0 cm; and (4)"blenny-like" fishes, a l~ame used by Bigelow & Schroeder (1953) to apply to gunnels Pholis gunnellus (Linnaeus) and shannies Ulvaria subbifurcata (Storer), and Stichaeus spp., which are indistinguishable in our videos, ~, 10-15 cm.

Census sites and technique has ~'o'~" The abundance of preuators ..... J " u. . . . . ;nf,~rr~d . . . . . . . . . .from . . . fishes and crabs co-occurring within 0.25-m 2 quadrats that had been censused primarily for early benthic phase lobsters (reported in Wahle, 1990; Wahle & Steneck, 1991). We emphasize, however, that while they provide a reasonable index of abundance for slow-swimming benthic fishes, stronger swimmers (e.g., cunners) were simply noted as to their presence or absence at the collection sites during the census (not necessarily within a quadrat). The population densities we report are probably underestimates, but, because most of the species are quite cryptic, they are probably higher than would be obtained by a nondestructive visual census alone. In presenting these data we wish to demonstrate the widespread occurrence of these predators among the habitats censused. We censused five sites separated by at least 2 km along an estuarine to outer coast gradient in the Pemaquid area ofmid-coast Maine (a total distance of 13 km; see Wahle, 1990; Wahle & Steneck, 1991). These sites span a range of subtidal coastal habitats common to the central Gulf of Maine. Early benthic phase lobsters are known to be concentrated in shelter-providing cobble habitats at all these sites (Wahle, 1990; W ahle & Steneck, 1991). Pemaquid Harbor (PH; 43°53'90"N,69°31'25"W) is a shallow ( < 7 m depth) protected estuary with patches of mud-sand, eelgrass, and cobble adjacent to each other. Rutherford Island (RI; 43°50'20"N, 69°33'40"W) is a semiprotected site having sand-mud, cobble, and ledge substrata to 20 m depth. Unlike the other four locations, rock surfaces at RI are covered with a dense kelp (Laminaria spp.) canopy extending below 10m depth. Pemaquid Point (PP; 43°50'10"N, 69 ° 31 '00" W), Ocean Point (OP; 43 ° 48'80" N, 69 ° 36'80" W), and Damariscove Island (DI; 43 °46'20"N: 69 ° 36' 60"W) are exposed sites with extensive bedrock slopes and

96


patches of cobble and sand ranging from a few to > 100 m in breadth. Rock surfaces below ~ 2-3 m at these last three sites have been denuded of macroalgae by the sea urchin Strongylocentrotus droebachiensis (Lamarck). At most sites we were able to census two depths (5 and 10 m below mean low water) and three categories of primary substratum: sediment (mud or sand), ledge (bedrock), and cobble (a heterogeneous mixture of pebbles, cobbles, and boulders as defined in Shepherd, 1964). These substrata constitute the vast majority of primary substrata available subtidally. We were forced to deviate from this sampling scheme where the desired depth or substratum was not available. Thus, at Pemaquid Harbor we collected no samples from 10 m or from bedrock, and at Ocean Point there was no sediment at 10 m. Although sites were variously vegetated we did not attempt to further stratify our sampling by the type of vegetative cover except at Pemaquid Harbor where we sampled sediment substratum inside and outside eelgrass beds. First we censused quadrats visually and then sampled them with an airlift suction sampler. Only bare bedrock (so called "urchin barrens") and sandy substrata could be censused adequately without using the suction sampler. Quadrats were haphazardly tossed with at least 2 m between them and we censused no less than 18 quadrats per depth-substratum combination at a site. Animals sampled with the airlift were captured in mesh bags which could be changed underwater for each quadrat. The bags were then brought to the surface to be sorted. Further details of the airlift census technique are provided in Wahle & Steneck (1991). PREDATION EXPERIMENTS

We designed predation experiments to examine how lobster body size and substratum influence the risk of attack. Relative rates of predation were measured using tethered lobsters. Preliminary video observations in 1987 were followed by experimentation in 1988. We used a combination of video-monitored and unmonitored experiments to address these questions. Video observation served to identify predators, determine the times of attacks, and assess the tethering technique. Experiments that were not videomonitored were free of the time and space constraints imposed by light and the camera's field of view, respectively, and so they ran longer (24 h) and tethered individuals could be more widely spaced.

Study sites Preliminary observations influenced the design and placement of subsequent experiments. Pemaquid Harbor was the site of preliminary video observations in 1987. In 1988, ~xperiments were conducted at a second site, Crow Island, in part, to gain spatial replication, and because tidal currents in the estuary at Pemaquid Harbor presented some difficulty for the tethering and video techniques. Crow Island is a semiprotected coastal location ~ 200 m across a channel from the Rutherford Island site. Unlike Rutherford Island, the bottom at Crow Island is composed of' open rock and cobble

HABITAT RESTRICTIONS IN EARLYBENTHIC LIFE

97

surfaces denuded by sea urchins with intervening patches of sediment. At these sites underwater visibility was ~ 5-8 m, always sufficient to make video observations.

Tedwring technique The tethering technique we used depended on lobster body size. Lobsters < ~ 20 mm CL were tethered by gluing the end of fine nylon thread (for the smallest lobsters) or braided nylon fishing line (20 lb test, for the larger lobsters of this group) to the dorsal side of the carapace with a very small drop ofcyanoacrylate glue (Super Glue). Lobsters > ,~ 20 mm CL were tethered by encircling the thorax between the first and second walking legs with a loop of braided nylon. It would have been inappropriate to use the same thread for all body sizes because the fine nylon thread was far too weak for the larger lobsters and the braided nylo:~ was too stiff and bulky for the smaller ones. For tethers that were glued directly to the carapace we achieved the best tether retention by drying the dorsal surface of the carapace at the tethering point with a gentle stream of air blown through a Pasteur pipette before applying the glue. Depending on the experiment, we attached lobsters to a stake or wire loop on a tethering platform with a plastic cable-tie through a loop in the free end of the tether. Lobsters were tethered at a depth of 4-5 m below MLW. Very few instances of tether breakage occurred and we attribute the success of our technique to a few precautions taken before tethering lobsters in the field. Lobsters were held overnight in captivity after applying the tethers. The next day we selected only vigorous lobsters and tested their tethers by lifting them out of the water by the tether and gently bouncing them a few times. Tethers withstanding this test almost never let-go under the forces applied by lobsters in the field. Video monitoring the tethering experiments (detailed below) permitted us to distinguish escapes from actual predation. In experiments that were not video monitored we used caged control treatments to detect tethering artifacts. Lobsters did not appear to suffer ill effects from the glue; we often held them for several days with the tether intact and they remained active during the period.

Video technique In 1987 we used a color video camera (Panasonic, Newvision Omnipro) and in 1988 an ultra low light, high resolution video camera (Osprey Electronics, Model OE 1323 with silicon intensifier target pickup tube, and a 5.5-mm, f l.5 wide angle lens) to improve observations under low light conditions. The camera was suspended by buoys from three anchor blocks on the bottom and was powered externally with a generator on an anchored vessel above. Experiments were monitored and recorded on board the vessel. Video recording was done with ambient daylight and no artificial lights.

98


PrelimOlaryfieM observations of tethered lobsters In 1987 we made preliminary video observations in the field to assess the efficacy of the tethering and video techniques. We established two sites that were representative of cobble and mud habitats ~ 300 m apart in Pemaquid Harbor. Observations were made of lobsters tethered to the natural substratum as well as to featureless patio blocks (38 x 19 x 5 cm). On the cobble substratum, several cobbles (~, 100-mm diameter) were placed a few cm apart and lobsters were tethered in a position to enable them to hide under the rocks. The animals and the entrance to their shelters were visible to the video camera. In each observation period 10 lobsters (5-7 mm CL) were tethered with a ~ 7-cm lead and were placed so they could come no closer than 5 cm to each other. We found a few limitations to the tethering technique as have Barshaw & Able (1990). Our preliminary observations showed that when lobsters were tethered to sediment substratum the lobsters would make small depressions, but were apparently inhibited from constructing deeper burrows as they do in the laboratory (Berrill & Stewart, 1973; Botero & Atema, 1982). Lengthening the tether did not improve the ability to burrow. In addition, tidal currents in Pemaquid Harbor occasionally caused debris to become snagged either on the tethering block, occluding our view, or on the tethers, interfering with the movement of the lobster and access of the predator. With direct videomonitoring we could identify such cases and either restart the trial or remove an affected lobster from the analysis. By the end of the preliminary studies we excluded one such lobster and had to restart one trial because of snagged debris. The following year we conducted experiments at Crow Island where there was less current. A potential methodological difficulty is that the initial disturbance created by the diver at the beginning of a tethering experiment may attract or deter predators and artificially change the rates of predation. However, we do not believe this would affect our conclusions regarding the dependence of predation rates on body size and shelter.

Si'.e-speci,fk, predation exper#nents In 1988 we conducted size-specific and substratum-specific predation experiments at Crow Island. Two types of size-specific experiments were deployed. The first involved 24-h trials that assessed size-specific survival without video-monitoring. In this experiment a total of 90 lobsters were tethered comprising three size classes of equal numbers (5-7, 15-20, and 30-40 mm CL). On each of 3 consecutive days (starting 10 July) l0 lobsters from each size class were equally divided into experimental and caged control groups. The experimental group was tethered to featureless cement patio blocks and the control group was tethered to identical blocks enclosed with plastic mesh (Vexar, 6-mm mesh size). A 1-mm mesh screen was used for the smallest lobsters in the control group. Patio blocks served to standardize substratum effects on vulnerability. The tether was long enough (4 cm for the smallest to 7 cm for the largest) to permit the lobster to go into a defensive display and move no closer than ~ 2 cm from the edge of the block. The 30 blocks were spread out in a 6 x 5 array on the bottom separated by 1.5 m and


99

treatments were randomly assigned. Three identical trials were deployed and censused 24 h later at mid-day. The results of the three trials were pooled, and the frequencies of losses were analysed with a log-linear model to test the significance of a two-factor interaction between body size and cage/no cage treatment (~ = 0.05). Subsequent repeated video observations of additional tethered lobsters were helpful in further examining size-specific predation. Because the larger lobsters in the 24-h experiment experienced almost no mortality, we focused our attention in this experiment on lobsters at the lower end of the range (5-25 mm CL). Video trials were conducted on 7 days between the dates of 28 July and 17 August. On each date between four and 11 lobsters spanning the size range were placed on patio block tethering platforms. Trials ran slightly < 6.5 h. The identity of the predators and the times of attack were determined from video recordings. To determine whether the number of lobsters attacked significantly depended on body size we used a G test of independence (~ = 0.05)on two arbitrarily chosen size classes of lobsters (5-9, 10-25 mm CL). We chose to pool all trials prior to statistical analysis because the number of lobsters tethered in any given trial was small and variable, and there was no apparent temporal trend in the data.

Substratum-specific predation experiments To examine substratum-related differences in predation rate we constructed three tethering platforms, each with a different substratum, and placed them in the same location. The platforms were 40.5 x 40.5-cm squares ef 0.25-in gray PVC sheet with 3 cm high walls, and five tethering points: one at the c :r,tcr 9nd one ~ 10 cm in from each of the corners. Cobble, mud, and featureless hard substrata were represented. The mud substratum was contained by the walls of the platform and was flush with them, but the opposite side of the platform was used for the other two substrata. The featureless platform was left blank and the cobble platform had one layer of 80-110 mm diameter cobbles attached with underwater epoxy (Koppers Company, splash zone compound). Certain cobbles were not attached to provide access to the tethering points. The latter two platforms were roughened with sand paper to provide lobsters some traction. Tethers were ~ 4 cm long. An experimental tri~l constituted five lobsters (5-7 mm CL) tethered to each substratum platform for 24 h. We did eight trials between 16 September and 14 October 1988, each beginning in mid-morning. Five of the trials included a caged control treatment to assess escapes from the tether. A control trial comprised five lobsters, each tethered in the center of a l-ram mesh cage that was 10 cm in diameter and 5 cm high. The experimental platforms were video-monitored for ~ 6 h during the first five trials to identify predators and record attack times. To fit all the platforms into the camera's field of view with equal exposure to predators, the platforms were placed on the bottom corner-to-corner enclosing a triangle. Because it was not necessary to observe the control treatment, the cages were placed outside the field of view within a meter of the

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platforms. To minimize spatial pseudoreplication (Hurlbert, 1984)we placed each trial in a different place along a ,~ 100 m workable length of the 5-m depth contour at Crow Island. This distance seemed sufficient since it is unlikely that the small fishes observed would be attracted from a distance greater than a few meters. For each substratum we calculated the mean number of lobsters remaining over the eight trials. Because we had 100% tether retention in the five caged-control trials, this treatment was excluded from the subsequent statistical analysis which examined differences in survival among the three substrata. Because the variances were heterogeneous among the three substrata (Bartlett's test, Sokal & Rohlf, 1981), we used a one-way ANOVA for samples with unequal variance (Rice & Gaines, 1989) to test the equality of means. Since this analysis indicated significant differences, we used a FlignerPolicello nonparametric test for planned comparisons (Day & Quinn, 1989) to examine differences between pairs of treatments. RESULTS HABITAT SELECTION EXPERIMENTS

Substratum preJbrence experiment In the habitat selection experiments lobsters tended to quickly traverse featureless sediment, and spent most of the time in larger substrata probing the interstices between rocks with one or both claws until they found a crevice large enough to occupy. This very stereotyped investigative behavior suggested that lobsters were actively testing the suitability of interstitial spaces for shelter. Table I indicates a preference for cobble, in TAal.l.: ! Results of 39 substratum preference trials with individual lobsters. (a) Number of lobsters found in designated substratum at end of individual rain trials ("final choice"). Null hypothesis was rejected because lobsters did not disperse according to hypothesized ! : 3 ratio of lobsters occupying cobble to those on all three of other substrata (7,a = 101.8, d f = I, p < 0.001), (b) Average percent of time lobsters spent in designated substrata. Substratum Mud (a) "Final choice" Number of lobsters (n = 39) (b) Percent of time .~ si-

S and

2

0

6 2.1

5 1.1

Gravel

0 10 2.6

Cobble

37 79 3.7

terms of both the time spent on the substratum and the final substratum choice. With 37 of 39 lobsters occupying cobble, the null hypothesis was rejected. In all cases where cobble was chosen, lobsters found shelter in the interstitial spaces among the rocks.

!


101

Moreover, of 10 lobsters that encountered cobble first, nine never left, and of the remaining 29 that encounter another substratum first, 27 ended up in cobble. Two lobsters ended up in the mud substratum and both were backed against the corner of the tank in excavated depressions. Since only nine (23.1~o) lobsters sampled all four substrata, the following experiment was a more definitive test of the attributes of substratum that determine its suitability.

Substratum size preference experiment Lobsters appeared to move to the alternative substratum only if they could not find shelter where they started. Thus, all lobsters that started in cobble spent the entire trial period there, regardless of body size (Fig. 1). In contrast, lobsters starting in pebble tended to spend less time there with increasing body size and moved over to take shelter in cobble (see Fig. 1 for statistical analysis).

1.0

~

:-.~¢

COBBLE 0.8

E

~

0.6

"

°

PEBBLE

o

°

5

15

a

,°°°

25

35

BODY SIZE (mm CL)

Fig. 1. Relationshipbetween lobster body size and substratum occupancy. Lobsters released in cobble did not move from it, regardless of body size. When same lobsters were released in smaller pebbles tendency to stay there declined significantlywith body size. Regression equation using untransformed proportions of time spent on pebble (as above):y = 1.14 - 0.03x, n = 30 lobsters. Proportions were arcsine-squareroottransformed (Sokal & Rohlf, 1981) before testing significanceof the regression (r 2 = 0.58, p -- 0.0001).

P R E D A T O R S AND P R E D A T I O N EXPERIMENTS

Distribution and abundance of predators At least a subset of the predator species observed to attack lobsters in the predation experiments (below) were found in each habitat censused (Table II). Overall, the predator density in the cobble substratum was more than twice as high as on ledge or

102

R.A, WAHLE

AND R.S. STENECK

sediment substrata. The greatest diversity of predators was also found on cobble. Blenny-like fishes were the most abundant fish group but rarely attacked lobsters in the tethering experiments (see below). Sculpins were |bund in lower population densities, TABLE II P o p u l a t i o n d e n s i t y (n. m - 2 .[. 1 SE) o r o c c u r r e n c e ( + ) o f p r e d a t o r s o b s e r v e d t o a t t a c k l o b s t e r s ( T a b l e I) in c e n s u s e s o f t h r e e different s u b s t r a t a at sites w i t h i n d i c a t e d v e g a t i o n a l s t a t e s , n, n u m b e r o f 0.25-m 2 q u a d r a t s c e n s u s e d at e a c h site. S e e t e x t for site a b b r e v i a t i o n s a n d p r e d a t o r s p e c i e s d e s c r i p t i o n s . Lain,

Laminaria; Zos, Zostera. Veg.

Depth (m)

u

Crabs

Fishes

All predators

state

Care#ms Ledge D! -

Cancer

0

0

0

0.4 + 0.2 0.1 + 0.1 0

0 0

OP -

10

24

0

0

0

0

0

5 10

20 19

0 0 0

2.6 + 0.9 4.4 + I.I i.! + 0.4

1.8 -+ 0.5 I.I + 0,4 0.6 -+ 0.2

0.4 _+ 0.3 0.2 -+ 0.2 0.2 + 0.1

0 0 0

23 23 31

0.2+0.8 0 0.5+0.2

-

10

23

0

3.0_+0.9 0.7 ±. 0.3 1.5+0.8 0.5 _+ 0.4

1.6_+0.4 2.! _ 0.4 0,3+0.2 0,3 _+ 0.4

0.7+0.3 0.3 + 0.3 0 0.3 + 0.4

0

-

5 10 5

-

5

20

0

1.4 ± 0.5

1.4 +_ 0.5

0.2 -+ 0.2

0.2 -+ 0.2

-

10

23

0

!.4 + 0.4

5 10

18 21) 19

0 0 7.2± 1.4 0,9 .+ 0.3

0.7 (1.5 i.4 (1.7

!,2 ± 0.4 0.4 + 0.3 11.4 ± 0.3 2.5±(1.5 i.I ± 0.4

0.2 -+ 0,2 0.2 _+ 0.2 0.2 + 0.2

0

Lttm Lain

0.7±0.5

0

0.3 ± 0.2

0

0 ± 0.2 + 0.3 +_ 0.3 + 0.7

0 0 0.1 _+ 0.1 0 0.2 + 0.2

0.2+0.2 !.7 -+ 0.4 0.3 _+ 0.2 0.3 _+ 0.2 0.6 _+ 0.4 0.2 + 0.2 0 0.7 + 0.5 0.5 _+ 0.3

0.2+ 0.2 0.3 -+ 0.2 0 0.1 -+ 0.1 0 0.4 -+ 0.3 0.2-+ 0.2 0 0.2 + 0.1

-

RI

Lain Lain Overall Cobble DI -

PP OP

RI

PH Overall Sediment DI -

5

2,4 ± 1.2 ± 4.0± 1.8 ±

+ 0.2 + 0.3 -+ 0.2 + 0.3 0

0.2 -+ 0.2

0 0 0 0 0

-

0.3 0.3 0.3 0.6

Flounder

24 24 30 31 24

PP

+ 0.3 + 0.3 + 0.2 _+ 0.1 0

Sculpin

5 10 5 i0 5

-

0.7 0.3 0.3 0.1

"B~enny"

-

5 10 5

24 24 30

0 0 0

-

10

-~1

0

-

5

19

0

0.3 0.5 0.6 1.9

-

i0

20

0

i.4 + 0.8

0

PH -

5 5

23 20

0.8+0.3 !.0 + 0.4 0.2 _+ 0.1

0 0.7 + 0.4 0.7 + 0.3

0 0.2 -+ 0.2 0.1 _+ 0.1

-

PP R!

Zos Overall

0

0

0.1_+ O.I 0

0 0

Cunner

+ + + + +

+

!.2 0.7 0.9 0.9

_+ 0.5 + 0.4 -+ 0.3 -+ 0.3 0 0 4.8 + !.0 5.7_+ i.1 !.8 + 0.4 5.4+ 1.1 3.1 + 0 . 6 2.5 + 1.0 i.2 + 0.5 3.2 + 0.9 2.8 + 0.7

2.8 1.8 13.9 4.1

+ 0.9 _ 0.6 -+ 2.1 _+0.9

0.3 + 0.2 2.3 + 0.4 0.9 + 0.4 !.0 + 0.3 2.7 + 0.8 2.0 _+ I.i 2.6 + 0.6 !.0 + 0.4 1.6 + 0.5

but were more widespread among habitats. Flounder, were largely restricted to sediment substrata, but were occasionally seen in cobble habitats without kelp cover. Cunner, in contrast, were only seen at sites (except Pemaquid Harbor) with ledge overhangs, boulders, or large macroalgae where they retreated in the presence of divers.

Tethering surface

n

n attacked

Size range t

Tethered lobsters

Hours/number of sessions observed

25 18 73 = 201

1 11

5 8 1 4

* Includes subsequent attacks on lobster if it survived first one. See text for further explanation. ** Crangon septemspinosa attack at Pemaquid Harbor; lobster and hermit crab attacks at Crow Island. * Size range in mm CL. ** In this experiment, third experimental substratum, cobble, is not shown because attacks could not be directly observed.

0 0 3 Total attacks

0 3

0 0 1 2 6

0 0 0 0

Sculpin

Flounder

Fishes

Predator attacks*

"Blenny"

1 0 2 0

Cancer

Crabs Carcinus

Preliminary observations: Pemaquid Harbor (28 September to 5 October 1987) Sand/mud Sand 10 10 5-7 0 Block 9 9 5-7 7.92/2 0 Rocky Cobble l0 l0 5-7 3.08/1 7 Block 10 10 5-7 3.i3/1 8 Size-specific predation experiments: Crow Island (28 July to 17 August 1988) Rocky Block 21 21 5-7 45.02/7 0 Block 27 16 8-25 0 Substratum-specific predation experiments** Crow Island (16-29 September 1988) Rocky PVC 25 16 5-7 26.12/5 0 Mud platform 25 13 5-7 0 Totals 137 105 85.27/16 15

Habitat

Summary of predator attacks on tethered lobsters observed by video at Pemaquid Harbor and Crow Island, Maine.

TABLE n l

0 0 97

58 39

0 0 0 0

Cunner

Other**

;>

,...e

¢3 t" '-el

N

m Z

t..
18 mm CL was tethered under video camera but it was never attacked. Predator groups as in Table III. Median time of first attack All lobsters By: All predators* All fishes** Cunner Sculpins All crabs***

18 16 21 14 36

(105) (86) (30) (51) (17)

5-7 mm CL

15 14 13 14 36

(89) (71) (20) (47) (17)

8-18 mm CL

45 45 45 17

(16) (15) (10) (4) -

* Includes all crabs, fishes, and "other" predator categories from Table III. ** Includes cunner, sculpins, flounder, and "blenny-like" fishes. Separate medians are not shown for latter two categories beceuse of their small numbers. *** Carc#tus m a e n a s and Cancer irroratus.


105

The first attack on a lobster was considered to be the most biologically meaningful because without a tether the first bout would most likely determine the fate of the lobster. Therefore, whereas Table Ill details all predator attacks, Table IV and Fig. 2 present 30

Median = 15 min.

>-

20

O

Z ILl O ILl nI.I. 10

0

20

40

60

80

100 120 140 160 180 200 2 2 0 2 4 0 260 280 300

T I M E OF F I R S T A T T A C K

(min.)

Fig. 2. Frequenc2v distribution of times of first attack on lobsters 5-7 mm CL pooled from all videomonitored experiments (see Table Ill). n = 89 lobsters attacked of 110 tethered. These data represent 16 separate recording sessions at Pemaquid Harbor and Cr6w Island, Maine. Session duration was > 240 min unless all lobsters were consumed before that time.

data on time to the first attack. The median time-of-first-attack on the smallest lobsters (5-7 mm CL) occurred within the first 15 min of being tethered on the bottom (Fig. 2, Table IV). The median attack time on larger lobsters was about three times greater (Table IV). Fishes tended to attack substantially more frequently (Table III) and sooner (Table IV) than crabs. Sculpins and cunners were the quickest of the fishes to respond to tethered prey (Table IV). Sculpins were most consistently present whenever and wherever lobsters were placed on the bottom, but cunners were responsible for more attacks than any other predator (Table III). Cunners were an ephemeral element of the predictor assemblage and were only seen to attack during experiments conducted in mid-summer (July and August, Table I). Attacks by flounder were only seen when lobsters were tethered directly on sediment substrata (Table III). The three attacks by blenny-like fishes only occurred when lobsters were tethered in rocky surroundings (Table III). Crabs, in general, took about twice as long as fish to attack and only attacked the smallest lobsters offered (Table IV). Attacks by crabs were generally infrequent except in the rocky area of Pemaquid Harbor where Carcim~s maenas was responsible for most

106


attacks (Table Ill). In spite of the abundance of Cancer irroratus throughout the study area (Table II), attacks by this predator were disproportionately uncommon (Table III). Size-specific predc ~.ion In the 24-h size specific experiment (not video monitored), survival appeared to be significantly related to body size only in the uncaged lobsters (Table V). Log-linear TABI.E V Results of 24-h size-specific predation experiment (not video-monitored). Log-linear analysis of total frequencies of lobsters remaining tethered (sum of three trials) indicates a significant interactions between body size and cage/no-cage treatment (7.2 = 65.5, df = 6, p < 0.001). Separate X2 tests on control and experimental groups indicate that survival depended on body size only in the uncaged experimental group (experimental: 7,-"= 33.7, df = 2, p < 0.001; control: Z-" = 2.9, df = 2, p = 0233). All lobsters remaining tethered at end of a trial were alive as well as those that broke their tethers inside cages. Size class (ram CL)

Trial

Experimental (uncaged)

Control (caged)

Tethered (it)

Remaining (n)

Tethered (n)

Remaining (n)

5-7

I 2 3 Total

5 5 5 15

0 0 0 0

5 5 5 15

5 5 4 14

15-20

1 2 3 Total

5 5 5 !5

2 0 0 2

5 5 5 15

4 5 4 13

30-40

! 2 3 Total

5 5 5 15

5 4 4 13

5 5 5 15

5 5 5 15

analysis indicated a strong two-way interaction between body size and cage/no cage treatment (see Table V for statistical details). While survival increased dramatically with greater body size in the uncaged experimental treatment, survival was high in all size classes in the caged control treatment and losses from the tether were minimal. ;(2 analysis of experimental and control groups separately indicated a significant dependence of survival on body size only in the experimental group (statistical details in Table V). Moreover, the frequency of predator attacks observed by video paralleled the pattern of losses observed in the unmonitored experiment. Pooling the results of the seven 6.5-h video trials reveals that small lobsters were attacked significantly more frequently than larger ones (see Fig. 3a for statistical analysis). In addition, a scatterplot of "attack rates" (the inverse of the time-to-first attack, Fig. 3b) as a function of body size suggests that small lobsters tended to be attacked sooner than larger ones.


107

(a) 100--

,9 Ill

5014,11-iiiN = 21 ii! 5-7

8-25

BODY SIZE (ram CL)

(b)

7060

re :3 O

50

re

40

•

•

w Q.

30 0

,¢I:

20

10

•

O

•

4

O0

!

8

"

"

I

12

'

"

I

16

'

!

20

'

'

I

"

24

BODY SIZE (rnrn CL) Fig. 3. Video observations ofsize-specific predation on tethered lobsters. (a) Frequency of lobsters attacked significantly depends on body size (G = I 1.87, df = 1, p < 0.01, n = lobsters tethered in each size category). (b) Scatter plot of predator "attack rate" (inverse of tim,; to first attack) against lobster body size. n -- 37 lobsters attacked of 48 tethered. Not all points are visible beca.use of overlap. These data represent a total of seven separate recording sessions, each slightly < 6.5 h in duration, totalling 45.02 h of observation (see Table III for predators; text for details).

Substratum-.wec(fic predation In these 24-h trials, lobster survival was significantly higher in the cobble than on bare PVC or mud substrata while survival on the latter two was similar (statistical details in Table VI). On the basis of video observations and 100% tether retention in the caged trials, we conclude that losses in the experimental treatments were unlikely to be due

108


to escape from the tether. While it is clear that small lobsters tethered without shelter are extremely vulnerable, it is possible that those tethered on sediment may not have been able to take full advantage of the substratum, thereby potentially biasing the results. We address this issue below along with other implications of the results. TABLE VI

Results of substratum-specific predation experiment with tethered lobsters (5-7 mm CL). In each 24-h field trial five lobsters were tethered per substratum. Tabulated is outcome of each trial, as well as their ~ and SE values. Survival on cobble was significantly higher than on other two substrata (one-way ANOVA for groups with unequal variances; Rice & Gaines, 1989; F = 10.33, df = 2,p < 0.01) which are equal (p > 0.1, Fligner-Policello nonparametric test for planned comparisons; Day & Quinn, 1989). There was 100~ tether retention in five control trials (not shown; see text for details). Remaining after 24 h (n)

Trial

1 2 3 4 5 6 7 8 st-

Bare PVC

Mud

Cobble

0 5 4 0 3 3 0 2 2.1 0.7

1 4 4 1 5 2 0 0 2.1 0.7

4 5 5 4 4 5 4 4 4.4 0.2

DISCUSSION PROCESSES RESTRICTING BENTHIC RECRUITMENT IN AMERICAN LOBSTER

The early benthic phase is the most habitat-restricted segment of the American lobster's life history (Hudon, 1987; Wahle, 1990; Wahle & Steneck, 1991). The present study reaffirms the role of habitat selection and predation as two processes that may explain the association of the early benthic phase with shelter-providing habitats. We have provided direct evidence of predation through video monitoring and report the widespread occurrence of the predators among shallow subtidal habitats in Maine. While it is clear that habitat selection is the proximate cause of the association, predation may be the evolutionary process reinforcing this behavior (see Howard & Nunny, 1983, and Johns & Mann, 1987, for alternative explanations). Homams prefers to occupy shelter-providing habitats as soon as it settles (Cobb, 1968; Howard & Bennett, 1979; Cobb et al., 1983). During its benthic life, it exhibits stereotyped shelter-seeking and construction behaviors (Cobb, 1971; Pottle & Elner, 1982; Wahle, 1990). The habitat selection experiments in this study suggest that body


109

size-substratum scaling considerations are important in habitat selection (Fig. 1; and see Wahle (1990) for more experiments on substratum-body size scaling). The predators observed to attack tethered lobsters are widespread and abundant in our study area (Table II), and are common over much of the range of the American lobster (Bigelow & Schroeder, 1953; Williams, 1984). Our estimates of predatory fish density could probably be improved by taking separate approaches appropriate to each functional grouping (e.g., McCormick & Choat, 1987; Hankin & Reeves, 1988; Collins. 1989). In addition, stomach contents and laboratory predation experiments have implicated other fish and decapod crustacean predators not seen in this study, e.g., cod Gaddus callarius (Herrick, 1909), tautog Tautoga onitus (Richards & Cobb, 1986), and mud crabs Neopanope texana (Lavalli & Barshaw, 1986; Barshaw & Lavalli, 1988). As predators, fish were clearly superior to crabs in terms of their response to and handling of prey (Table IV, Fig. 2) in these day-time observations of predation. Nonetheless, crabs may be more effective nocturnal predators. Fish attacked sooner and more frequently than crabs. Indeed, the time and frequency of attacks seemed to be more a reflection of the mobility than the abundance of the predators. Our observations of predation are consistent with the observations of Roach (1983) who also saw small fishes quickly detect and attack small lobsters in field enclosures. Thus, fish predators could have a gre~_ter per-capita impact than crabs on lobster numbers. Fishes located prey visually, whereas crabs appeared to be more dependent on tactile stimuli in their handling of prey. Crabs were somewhat clumsy at capturing tethered lobsters and we suspect that, had the lobsters not been tethered, most would have escaped the attack. Unlike fish however, crabs have the advantage of being able to manipulate and excavate the substratum to reach infaunal prey (Lavalli & Barshaw, 1986; Barshaw & Lavalli, 1988). As visual predators, fishes are known to be most active during the day, whereas decapod crustacean predators are more active at night (Choat, 1982; Witman, 1985). Thus, we may have underestimated crab predation potential in this study. Vulnerability appears to diminish rather quickly with small increments in body size (e.g., Table V, Fig. 3). This may be due to the rarity of large vertebrate predators in coastal waters. In fact, our current studies (Steneck & Wahle, unpubl, data) indicate that lobsters are virtually immune to predation in coastal sites once they attain a size of ~ 60 mm CL. Offshore, where larger predators are more abundant, we have observed tethered lobsters up to 110 mm CL being attacked. While it is clear that exposed settlement-size lobsters are more vulnerable than sheltered ones, we could not thoroughly test the vaiue of sediment habitat in the field since tethered lobsters could not construct complete burrows (also see Barshaw & Able, 1990). Nonetheless, laboratory studies of untethered lobsters indicate that they remain vulnerable to excavating predators like crabs even inside the burrow (Lavalli & Barshaw, 1986; Barshaw & Lavalli, 1988). Moreover, small lobsters may be attacked before they even have time to construct a burrow. Behavioral studies of lobsters on sediment substrata in the laborc~'~ory indicate that settled post-larvae spend at least several hours constructing a burrow (Berrill & Stewart, 1973; Atema et al., 1982; Botero

II0


& Atema, 1982). In our field experiments half of the attacks on the smallest lobsters (5-7 mm CL) occurred within 15 min. It appears that, where predators are present, time is at a premium during settlement, and many lobsters are likely to succumb if pre-existing shelters are not found. Our benthic censuses of predators suggest that newly settled lobsters are likely to encounter predators in almost any benthic habitat they occupy. Where predators may be locally absent, however, only the intrinsic preference for, pre-existing shelter would prevent lobsters from immediately occupying featureless sediment. PREDATION AND DEMOGRAPHIC RESTRICTIONS OF LOBSTERS AND THEIR ALLIES

The American lobster is not alone among decapods in being restricted to shelter providing habitats early in life. Indeed, the distributions of juvenile freshwater crayfish (Stein & Magnuson, 1976) and spiny lobsters (Herrnkind & Butler, 1986; Howard, 1988; Yoshimura & Yamakawa, 1988) are similarly restricted. Caddy (1986) suggested that many shelter-dependent crustaceans may experience a recruitment bottleneck after settlement if the availability of suitable shelter-providing habitat is limited. While Caddy's hypothesis remains to be tested, strong evidence exists that predation plays an important part in restricting the early benthic phase of representatives of a wide range of modern-day reptant macruran (large-abdomened) decapod crustaceans, including clawed lobsters and freshwater crayfish (Infraordo Astacidea), spiny lobsters (Infraordo Palinura), ghost shrimp (Infraordo Thalassinidea), and hermit crabs (lnfraordo Anomala; classifications after Schram, 1986). Direct field evidence of predation as a process structuring the distribution and abundance of these crustaceans is difficult to obtain. Nonetheless, experimental evidence exists for at least one genus of each infraorder: in addition to the present study of Homarus, field experiments have demonstrated that fish and/or crab predation restrict distributions of young freshwater crayfish Orconectes propinquis (Stein & Magnuson, 1976; Quinn & Jansson, 1989) and spiny lobsters, Panulirus argus (Herrnkind & Butler, 1986) and P. cygnus (Howard, 1988), to shelter-providing habitats. Hermit crabs, e.g., Pagurus spp. (Vance, 1972; Bertness, 1982), are an example of extreme specialization where the consequences of being without shelter are most dire. Where recruitment to featureless sediment does occur in macrurans, e.g., ghost shrimp Callianassa (Posey, 1986), they appear to be at least locally restricted to intertidal flats where predation pressure is reduced. Understandably lacking are similar studies of the less accessible deep water species, although several predators have been identified from stomach analyses (Phillips et al., 1980). In this respect, it is interesting that larval settlement in Nephrops norvegicus occurs on featureless sediment in relatively deep water, largely below the photic zone (Chapman, 1980), where visual predators may be at a disadvantage. In shallow water environments, successful recruitment to featureless sediment appears to require effective mechanisms to escape predators. Homarus americamls


I!!

specifically was shown in mesocosm experiments to suffer greater mortality to fish predation than the crab Cancer irroratus, which can bury itself rapidly (Richards & Cobb, 1986). Indeed, many of the most active sediment-dwelling brachyuran crabs (e.g., Cailinectes, Ovalipes) and crab-like anomalans (e.g., mole crabs, Hippidae) have this ability. Lobsters, ghost shrimp, and hermit crabs share the attributes of having large abdomens and, in general, being unable to bury themselves in sediment. We believe that recruitment by many of the reptantians with large abdomens cited above may be constrained by their inability to rapidly bury themselves in sediment. Clearly, more studies are needed to compare the attributes of the brachyuran and macruran body form with respect to habitat use and predation. It is well known that mobile predators in open sediment habitats of shallow marine and aquatic environments limit the distribution and abundance of a spectrum of benthic invertebrates (Virnstein, 1977; Reiss, 1978; Nelson, 1979; 1981; Heck & Thoman, 1981; Choat, 1982; Quammen, 1984; Summerson & Peterson, 1984; Wilson et al., 1987; Matilla & Bonsdorff, 1989; Aronson, 1989; but see Raffaelli et al., 1989 for an opposing view). Structurally complex habitats, the intertidal zone, and perhaps even deep water below the photic zone may represent spatial refugia where predation pressure is reduced. Behavioral preferences for such refugia are a predictable outcome of strong selection against occupying open habitats. Our field studies have shown predation to be potentially important in enforcing the preference of early benthic phase American lobsters for shelter-providing habitats. While these habitats may be an essential resource early in life, the association relaxes, perhaps as lobsters outgrow the risk of predatioo. It will be important for future studies to assess the extent to which the availability of these habitats may place fundamental limits on lobster recruitment. ACKNOWLEDGMENTS

This study was made possible by contributions from a spectrum of sources. Primary support came from Maine Sea Grant NA 86 AA-D-SG 047. Specific contributions were made by several groups at the University of Maine: the Association for Graduate Students, the Center for Marine Studies, and the Migratory Fish Research Institute. Additional outside support was given by the Lerner-Grey Foundation for Marine Research and the Society of Sigma Xi. Thanks go to the staff of the Darling Marine Center, the summer interns of 1987 and 1988, and K. Moody, S. Hacker, J. Gross, D. Packer, D. Low, and H. Whittenburg for their help in the field. We appreciate the help of P. Humphreys with lab experiments and diving. S. Gaines kindly gave statistical advice. J.S. Cobb, J. Dearborn, W. Glanz, K. Heck and two anonymous reviewers gave valuable comments on previous versions of this paper.

il2

R.A. WAHLE AND R.S. STENECK REFERENCES

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