Effects of habitat patchiness on American ... - Wiley Online Library

Ecology, 91(7), 2010, pp. 1993–2002 Ó 2010 by the Ecological Society of America

Effects of habitat patchiness on American lobster movement across a gradient of predation risk and shelter competition KEVIN A. HOVEL1,3

AND

RICHARD A. WAHLE2

1 Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, California 92182 USA Bigelow Laboratory for Ocean Sciences, P.O. Box 475, 180 McKown Point Road, West Boothbay Harbor, Maine 04575-0475 USA

2

Abstract. The influence of landscape structure on marine ecological processes is receiving increasing attention. However, few studies conducted in coastal marine habitats have evaluated whether the effects of landscape structure on species interactions and organismal behavior are consistent across the range of an organism, over which landscape context and the strength of species interactions typically vary. American lobster (Homarus americanus) juveniles seek refuge from predators within shallow rocky habitat but make short-distance movements to forage outside of shelter. We evaluated how the patchiness of cobble habitat influences juvenile lobster movement by conducting mark–recapture experiments on lobsters placed within patchy and contiguous cobble plots in three regions of New England among which risk of predation and intraspecific shelter competition vary (Rhode Island, mid-coast Maine, and eastern Maine, USA). We also evaluated whether habitat patchiness influenced lobster colonization of plots and whether lobster fidelity to individual shelters corresponds to variability in predator abundance and conspecific density among regions. Cobble patchiness reduced rates of lobster movement in all three regions in 2004 and in two of three regions in 2005, despite large differences in landscape context among regions. Region had much larger effects on lobster colonization than did patchiness, but patchy plots were colonized at higher rates than were contiguous plots where lobster densities were highest. Fidelity to shelter was higher in regions with low conspecific density (Rhode Island and eastern Maine) than in midcoast Maine where conspecific density is high and where unmarked lobsters often occupied shelters vacated by marked lobsters. Our results indicate that cobble patchiness influences juvenile lobster movement at small scales, but that the effects of patchiness on movement were consistent across much of the range of the American lobster despite strong regional variation in predator abundance and conspecific density. Key words: American lobster; cobble; competition; habitat fragmentation; Homarus americanus; movement; patchiness; predation; shelter.

INTRODUCTION Habitat fragmentation and degradation at the landscape scale pose severe threats to biodiversity in terrestrial and aquatic ecosystems. An emerging theme in landscape ecology is that the effects of fragmentation on ecological processes are largely inconsistent among taxa and through space and time, whether applied in terrestrial (Debinski and Holt 2000), freshwater (Gilliam and Fraser 1987), or marine (Bell et al. 2001) systems. In light of this, there has been increasing recognition that landscape context may dictate the strength and direction of landscape-scale effects on fauna and flora (Stephens et al. 2003). The amount of habitat cover (Donovan et al. 1997), surrounding habitat types (Selgrath et al. 2007), predator species and their behaviors (Tewskbury et al. 1998), and sources of fragmentation (Wiens 1995), among other factors, may affect how aspects of Manuscript received 7 April 2009; revised 19 August 2009; accepted 21 September 2009; final version received 20 October 2009. Corresponding Editor: J. F. Bruno. 3 E-mail: [email protected]

landscape structure, such as habitat edges and patchiness, dictate ecological processes. Differences among studies also arise from differences in experimental procedures and in the spatial and temporal scales addressed. Standardized, manipulative experiments across ecological gradients are required to determine whether the effects of habitat fragmentation are context dependent or consistent, but such studies are rare due to expense and logistical constraints (Debinski and Holt 2000). In marine habitats, landscape structure may strongly influence organismal settlement and recruitment (Eggleston et al. 1999), post-settlement survival (Irlandi et al. 1995, Hovel and Lipcius 2001), growth rates (Irlandi 1996), and movement (Micheli and Peterson 1999). Though small post larvae and newly settled juveniles may leave settlement patches rarely (Lawton and Lavalli 1995; but see Etherington and Eggleston 2000), these phases may be followed by increased movement of larger juveniles that forage within and outside of settlement habitat in order to select larger shelters (Caddy and Stamatopoulos 1990), to select alternative

1993

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KEVIN A. HOVEL AND RICHARD A. WAHLE

habitats or habitat patches (Edgar and Robertson 1992), to alleviate crowding (Moksnes 2002), or to forage (Lawton 1987). The patchy nature of many benthic habitats requires juveniles and adults to often move out of refuge and over unstructured seafloor where they may be vulnerable to predators, or to remain within patches if costs of leaving them, such as increased predation risk, outweigh costs of staying within patches, such as reduced feeding rates. In this study, we assess how patchiness of cobble nursery habitat influences movement rates of juvenile American lobsters, Homarus americanus, across strong gradients of predation risk and competition for shelter in the coastal waters of New England. From Atlantic Canada to Long Island Sound, USA, American lobster post larvae settle into relatively shallow (,30 m) shelterproviding habitats, primarily beds of gravel, cobbles, and boulders (hereafter ‘‘cobble’’; Wahle and Steneck 1991, Incze et al. 2000). Cobble nursery habitat generally is patchy along the New England coastline at scales of meters to tens of kilometers, even along the rocky coast of Maine where cobble comprises only 10–16% of the sea bed at depths ,20 m (Barnhardt et al. 1996). After settlement, lobsters remain cryptic and sedentary within cobble patches for one to two years, but then move from settlement patches to seek larger shelters and to forage. Lobsters remain vulnerable to fishes and other predators during their juvenile phases (Wahle and Steneck 1992). Several aspects of landscape context that may influence lobster movement behavior vary regionally throughout the range of the American lobster, notably the abundance and diversity of potential fish predators, densities of potential competitors for shelter, and sea surface temperature (Brown 2007). The diversity and abundance of fishes known to prey on lobsters is considerably higher in Rhode Island (RI) than in midcoast Maine (MC) and eastern Maine (EM; Collette and Klein-MacPhee 2002). Accordingly, in 2000, juvenile lobster relative mortality was about threefold higher in southern RI than in MC (Brown 2007). Many predatory fish populations, including cod (Gadus morhua) and flounder (Paralichthyes spp.), have collapsed in the Gulf of Maine, which may be linked to higher crustacean survival rates (Witman and Stebens 1992, Steneck and Carlton 2001) and increased lobster abundance and harvests in Maine over the past decade (Acheson and Steneck 1997). Additionally, in nearshore cobble nursery habitat, densities of newly settled and emergentphase H. americanus are four- to fivefold higher in MC than in RI or EM (Incze et al. 2006), a pattern also observed for larger lobsters in deeper (20– 40 m) nearshore waters (Selgrath 2006). This is in part due to consistent differences in larval supply and growth among regions, leading to a greater accumulation of year classes in MC than in warmer waters to the south (Wahle et al. 2004). Though in EM lobster abundance is limited by low settlement rates (Incze and Naimie 2000),

Ecology, Vol. 91, No. 7

large-bodied crabs (primarily Cancer spp.) are abundant and may occupy potential lobster shelters. We predicted that nursery habitat patchiness would have little effect on the propensity of juvenile lobsters to move among shelters in MC and EM, because lower densities of predatory fishes may reduce the risk of predator-induced mortality outside of shelters, and because competition for shelters can ensue at high lobster or crab densities, increasing the odds of shelter and patch switching after foraging bouts (Wahle and Incze 1997, Steneck 2006). In contrast, we predicted that cobble patchiness would reduce the propensity for juvenile lobsters to move in RI, because high fish abundance may increase the risk of predator-induced mortality outside of shelters and because low lobster densities may lead to low competition for shelters. METHODS Study locations Our experiments on lobster movement and shelter fidelity were conducted in shallow nearshore waters of Rhode Island (RI; 41828 0 N, 71822 0 W), mid-coast Maine (MC; 43847 0 N, 69836 0 W), and adjacent to Mt. Desert Island in eastern Maine (EM; 44820 0 N, 68817 0 W; Appendix A). In RI, study sites were located near the mouth of Narragansett Bay, where sediment composition is largely cobble, sand, and bedrock, and mean monthly water temperatures range from 38C to 228C annually. In MC, we conducted experiments along the outer coast near the mouth of the Damariscotta River, where patches of cobble and boulder are interspersed with sand, mud, and granite bottom. Mean monthly water temperatures range from 28C to 188C. In EM, sediment composition is similar to that of MC, but water temperatures rarely exceed 128C. In each region, salinities at our study sites were between 30 and 33 psu (practical salinity units). Effects of cobble habitat patchiness on lobster movement among shelters To assess how patchiness of lobster nursery habitat influenced lobster movement among shelters, we monitored the movement of tagged emergent-phase and vagile-phase juvenile lobsters (15–40 mm carapace length [CL]) within constructed cobble plots in each location. Plots were constructed in August 2003 by placing trays of cobble on sandy sediment adjacent to naturally occurring rocky habitat in each region at depths of 4–8 m. Each 7.9-m2 plot consisted of twelve 1 3 0.66 m wire mesh trays filled with quarry cobble (;6– 15 cm diameter) to a depth of 0.15 m. We created two plot configurations: contiguous (four inner trays placed together with eight outer trays abutting them to form a rough rectangle) and patchy (four inner trays placed together with eight outer trays evenly spaced along a perimeter 1.5 m away). We chose a distance of 1.5 m because emergent-phase and vagile-phase lobsters are central place foragers that move relatively short

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AMERICAN LOBSTER MOVEMENT

distances from shelter (Lawton 1987). We constructed two replicate plots of each type at each of two sites within each region, with plots spaced no less than 25 m apart (N ¼ 24 plots). To standardize plot conditions among regions we scrubbed algae from all rocks and removed by hand all lobsters that had colonized plots over the winter. Lobsters used for tagging were captured in naturally occurring cobble habitat near each study site and held in running seawater flumes. Lobsters were tagged by placing a drop of colored superglue on the carapace. Only active lobsters with at least one claw were used in the experiment, and lobsters were never reused. For each trial, we placed 20 tagged juvenile lobsters (density ¼ 7.5/ m2) in the center of each plot (inner four trays) and then sampled plots 24 hours later to determine rates of movement to outer trays. Our starting density was equal to or less than typical densely populated cobble habitat in Maine (10–13 juvenile lobsters/m2; Wahle and Incze 1997). Pilot experiments indicated that 24 hours provided enough time for lobsters to move, but also allowed for reasonable rates of recapture. When introducing tagged lobsters to plots, we prevented them from fleeing the inner trays for one hour with a mesh screen. Likely because of faster growth rates at warmer temperatures, juvenile lobsters in RI nurseries tend to be slightly larger, are composed of fewer age classes, and become emergent at a younger age than those in Maine (Wahle et al. 2004). Therefore, the mean CL of our tagged lobsters was slightly greater in RI (33.7 6 0.69 mm [mean 6 SE]) than in MC (28.2 6 0.36 mm) and EM (29.8 6 1.8 mm). Differences in mean size likely did not influence results, however, as lobsters do not become wide ranging until adolescence (.40 mm CL; Lawton and Lavalli 1995), and they remain vulnerable to predators in shallow coastal habitats through adolescence (Wahle and Steneck 1992). After 24 hours, all trays within each plot again were cleared and all tagged lobsters, as well as untagged lobsters and crabs that had entered plots, were captured, measured for CL (or carapace width [CW] for crabs), and categorized as inhabiting inner trays or outer trays. Four trials of the experiment were conducted from July to September 2004 (Year 1) and two trials from June to September 2005 (Year 2; N ¼ 2880 lobsters total), with no less than 10 days between trials. Trials were identical between years, with the exception that in 2005 tagged and untagged lobsters were placed back into trays after the 24-hour check, rather than being removed. To assess movements over the long term we then checked plots for tagged and untagged lobsters and crabs after 7, 14, and 21 days, returning lobsters to the tray in which they were found on each occasion. To help prevent tag loss after 24 hours in Year 2, lobsters were tagged with individually numbered T-bar tags inserted into the dorsal musculature, which is retained through molting.

1995

We used separate three-way, nested analyses of variance (ANOVAs; one for each year) to test for the effects of region, configuration, and site (nested within region) on the proportion of recaptured lobsters moving to outer cobble trays after 24 hours. Separate analyses were performed for each year due to unequal sample sizes between years and because a larger analysis would lack statistical power to detect differences, especially for high-order interactions. Too few tagged lobsters remained in plots at the 7 d, 14 d, and 21 d checks in 2005 to conduct analyses on tagged lobsters beyond 24 hours. We also used three-way, nested ANOVAs to test for effects of region, configuration, and site on the proportion of lobsters recovered alive within plots (inner plus outer trays) after 24 hours. We examined the total proportion of lobsters recovered alive to help us determine whether potentially lower recapture rates in outer trays of patchy cobble plots vs. contiguous plots were due to lower rates of interception by outer trays (i.e., lobsters might not contact trays if on a random walk) or due to lower propensity to leave inner trays (i.e., a behavioral effect of the treatments). Similar total recapture rates between contiguous and patchy plots, but lower recapture rates in outer trays in patchy vs. contiguous plots, would signify that lobsters were less willing to move from inner trays in patchy plots. We also tested for differences in the mean CL of lobsters that moved from inner to outer trays between plot configurations using separate t tests (one for each region). We used data on the abundance of untagged lobsters and crabs found in plots to conduct two additional tests. First, to assess whether movement rates of tagged lobsters to outer trays were inversely correlated with the density of potential shelter competitors in outer trays (i.e., untagged lobsters and crabs .30 mm CW) we used separate linear regressions with the proportion of recaptured lobsters moving to outer trays as the dependent variable and untagged lobster density, crab density, or the total density of other organisms (lobsters plus crabs) within outer trays as the independent variable. Second, we tested for the effects of region, configuration, and site on the density of untagged lobsters entering plots within 24 hours using three-way nested ANOVAs. Here, we were interested in whether the density of untagged lobsters in our recently cleared plots varied regionally and with plot configuration. Specifically, higher rates of immigration to plots where naturally occurring lobster densities are highest would suggest that movement among shelters (and hence competition for shelters) is more frequent in regions with high lobster density, and the greater perimeter to area ratio of patchy plots vs. contiguous plots may result in greater interception rates of untagged lobsters moving from naturally occurring cobble habitat. In 2005, the density of lobsters entering plots generally did not stabilize after 14 days (see Results), and therefore we conducted the same analysis on the density of lobsters entering plots after 21 days.

1996


For all ANOVAs, we used Cochran’s test to test for homogeneity of variances, and normal probability plots to examine data for normality, and transformed data when necessary to meet the assumptions of ANOVA (Underwood 1997). To increase power to detect treatment effects, we pooled data across the nested term (site) and re-ran ANOVAs when Psite 0.25, following the protocol in Underwood (1997). Post hoc tests for differences in means were conducted using either lowerlevel ANOVAs or Student-Newman-Keuls (SNK) tests where appropriate. We also used techniques described in Graham and Edwards (2001) to calculate the proportion of the total variance (¼ magnitude of effect, x2) accounted for by each factor and by the error term when P , 0.1. Rather than using an arbitrary alpha value of P , 0.05 to determine which trends were significant, we used resulting P values, effect sizes, x2 terms, and error bars to suggest which tests provided strong vs. weak evidence for treatment effects on movement. Potential shelter competition We conducted an additional tagging experiment in naturally occurring cobble habitat to assess regional differences in potential shelter competition among lobsters and crabs. Between July and October 2005, we captured lobsters by turning over rocks within a 30 3 6 m belt transect (;3–5 m depth) laid parallel to the shoreline at each of four sites in RI and three sites each in MC and EM (Appendix A). All lobsters were measured (CL) and a subset of no less than 30 lobsters at each site was tagged by wrapping individually numbered plastic bands around the carpus. We then returned lobsters to shelters in which they were found and marked each shelter used by tagged lobsters with an individually numbered flag. Flagged shelters were observed for several minutes to ensure that lobsters did not immediately crawl away. We returned to sites 48 hours later and recorded whether flagged shelters contained (1) the original lobster, (2) a different (tagged or untagged) lobster, or (3) another organism (primarily the crabs Cancer irroratus or Cancer borealis). We also thoroughly surveyed the entire transect for tagged lobsters that may have moved from their original shelters. We used a multiple logistic regression, with region and lobster CL as independent variables, and lobster presence in shelter into which they had been placed 48 hours earlier (dependent variable: present or not) to compare propensity to remain in shelter among regions and lobster sizes. We only considered recaptured lobsters in this analysis to eliminate missing lobsters that might have been eaten by predators or that may have moved from the transects. We also used a G test of independence to test for differences among regions in the frequency of occupancy of flagged shelters from which lobsters had moved (i.e., whether vacated shelters contained another organism) and used a one-way


ANOVA to test whether total lobster density varied among regions. RESULTS Effects of cobble patchiness on lobster movement Tagged lobsters within plots.—In 2004, cobble habitat patchiness moderately reduced rates of lobster movement from the inner to outer trays of cobble plots in all regions. The proportion of lobsters moving to outer trays was ;10–15% higher in contiguous plots than in patchy plots, and configuration accounted for 10.7% of the variability in lobster movement. There was little evidence of an effect of region or site on lobster movement and no interaction of configuration and region (Table 1, Fig. 1). We found no evidence that lobster CL in outer trays varied between plot configurations in any region (all P values . 0.35; Appendix B). In 2005, there was an interactive effect of configuration and region on the proportion of lobsters moving to outer trays after one day (Table 1, Fig. 1). The effects of patchiness on movement were stronger than in 2004: the proportion of lobsters moving to outer trays was 20– 30% higher in contiguous plots than in patchy plots in Rhode Island (RI) and in mid-coast Maine (MC), but not in eastern Maine (EM). As in 2004, we found no evidence that lobster CL in outer trays varied between contiguous and fragmented patches in any region in 2005 (all P values . 0.15; Appendix B) The proportion of lobsters recovered alive did not differ between contiguous and patchy plots, suggesting that lower numbers of lobsters found in outer trays of patchy plots vs. contiguous plots were due to a reduced propensity to move in patchy plots, rather than to lobsters missing patchy cobble trays on a random walk from shelter. We recaptured an average of 32% of tagged lobsters in the patchy treatment and 32% of tagged lobsters in the contiguous treatment after one day in 2004 (totals include all trays within patches). The proportion of tagged lobsters recaptured was higher in MC than in RI and EM, but there was no difference in recapture rates between contiguous and patchy treatments and no interactive effect of region and configuration (Appendix C). In 2005, after one day we recaptured an average of 38% of tagged lobsters in the patchy treatment and 40% of tagged lobsters in the contiguous treatment. In 2005, the proportion of lobsters recaptured was higher in RI than in MC and EM, but as in 2004 there was no effect of configuration on recapture rates and no interactive effect of region and configuration after one day (Appendix C). Region accounted for 38% and 35% of the variance in recapture rates in 2004 and 2005, respectively. Lobster movement to outer trays was inversely correlated with crab density in outer trays (linear regression: F ¼ 4.07, df ¼ 1, 123, P ¼ 0.04), though crab density explained only 5% of the variability in lobster movement among sites. Lobster movement rates were not correlated with the density of untagged lobsters

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1997

TABLE 1. Results of three-way nested ANOVAs on the proportion of recaptured tagged American lobsters (Homarus americanus) that moved to outer trays within cobble plots after one day in (a) 2004 and (b) 2005, and on the density of untagged lobsters moving to plots after one day in (c) 2004 and (d) 2005. Source

df

MS

F

P

x2 (%)

a) Tagged, 2004 Configuration (C) Region (R) C3R Site(region) C 3 site(region) Residual

1 2 2 3 3 81

0.178 0.055 0.094 0.009 0.041 0.056

3.09 0.96 1.65 0.16 0.69

0.08 0.33 0.19 0.92 0.56

10.7

b) Tagged, 2005 Configuration (C) Region (R) C3R Site(region) C 3 site(region) Residual

1 2 2 3 3 20

0.120 0.043 0.119 0.072 0.061 0.045

2.73 0.60 2.71 1.60 1.35

0.11 0.60 0.08 0.23 0.28

c) Untagged, 2004 Configuration (C) Region (R) C3R Site(region) C 3 site(region) Residual

1 2 2 3 3 20

3.024 35.18 3.038 3.639 0.275 1.215

11.0 9.66 11.0 3.00 0.23

0.04 0.05 0.04 0.08 0.87

d) Untagged, 2005 Configuration (C) Region (R) C3R Site(region) C 3 site(region) Residual

1 2 2 3 3 20

0.089 32.84 1.265 8.731 0.635 0.919

0.14 3.76 1.99 9.49 0.69

0.73 0.15 0.28 ,0.001 0.57

9.7

1.6 36.4 3.1 5.6

57.3 22.8

Notes: F ratios for region (R) used the nested term site(region) in the denominator. F ratios for configuration (C) and configuration 3 region used the nested term configuration 3 site(region) in the denominator. Data were pooled over nested terms when Pnstd 0.25. Factors providing strong evidence of an effect on lobster movement (see Methods) are shown in boldface type. The precentage of the total variance accounted for by each factor when P , 0.1.

entering patches over 24 hours from the surrounding area (linear regression: F ¼ 0.23, df ¼ 1, 123, P ¼ 0.63), nor with the total density of organisms inhabiting outer trays (linear regression: F ¼ 1.07, df ¼ 1, 123, P ¼ 0.30). Untagged lobster movement to plots.—In 2004, we found an interactive effect of region and configuration, as well as an effect of site (nested within region), on the density of lobsters moving to plots from surrounding habitat over 24 hours (Table 1, Fig. 2). Movement to plots was higher in patchy than in contiguous plots in MC but not in RI or EM. The density of lobsters moving to plots was two- to fourfold higher in MC (21.6 6 2.5 lobsters per plot [mean 6 SE]) where untagged lobsters in plots outnumbered tagged lobsters, than in RI (10.4 6 0.09) and EM (5.5 6 0.88). In 2005, we found only an effect of region on lobster movement to plots after one day (Table 1, Fig. 2). The density of lobsters moving to plots was two- to threefold higher in MC (19.5 6 1.8 lobsters per plot) than in RI (8.7 6 0.66) or EM (5.9 6 0.72). Lobster densities increased throughout the 21-day period in MC and RI, but not in EM. Though the density of lobsters moving to plots after 21 days was four- to fivefold higher in MC and RI than in

EM, there was only an effect of site in the ANOVA for untagged lobster density within plots (Appendix D). Lobster shelter fidelity Of lobsters tagged with numbered claw bands in naturally occurring cobble habitat, we recovered 22%, 25%, and 11% of lobsters after 48 hours in RI, MC, and EM, respectively. We found strong evidence for greater lobster shelter fidelity in RI and EM than in MC (logistic regression: P ¼ 0.002 and 0.04 for RI vs. MC and EM vs. MC, respectively; Fig. 3). The odds that lobsters would remain in shelter were more than twofold higher in RI and EM than in MC. Additionally, the odds that vacated shelters would be occupied by another organism were higher in MC than in RI, and higher in RI than in EM (G test of independence: G ¼ 40.2, df ¼ 2, P , 0.001; Fig. 3). In all regions, the majority of organisms occupying vacated flagged shelters were other lobsters (96%, 91%, and 83% in RI, MC, and EM, respectively) with crabs (primarily Cancer irroratus and Cancer borealis) making up the remainder. The total number of lobsters found in transects was approximately twofold higher in MC (80.0 6 10 lobsters [mean 6

1998



regions, but lobster movement was deterred by patchiness similarly between regions with contrasting landscape context. Lobster behavioral responses to habitat patchiness may be similar between regions with very different conspecific densities and predation risk (e.g., RI and MC) if there has been strong selection for avoidance of unstructured sediment due to historically high predation rates throughout New England. However, lobsters alter shelter selection and movement behavior in response to cues from predators as well as conspecifics (Spanier et al. 1998), and visitation rates by fish predators to tethered lobsters and to fixed video monitoring stations deployed near our plots were far higher in RI than in MC (Brown 2007). Similar behavioral responses to patchiness among regions also could result if predation risk deters movement among patches in RI, and high densities of conspecifics deter movement among patches in MC. This is unlikely, however, because at high lobster densities such as those in MC, lobsters are subject to a lottery process whereby shelter switching is common, and larger juvenile lobsters may evict smaller juveniles from shelter (Steneck 2006). Our shelter fidelity experiment indicated that tagged lobsters were far more likely

FIG. 1. Percentage (mean þ SE) of tagged American lobsters (Homarus americanus) recaptured alive that emigrated to outer plots after one day within contiguous or patchy cobble plots in 2004 and 2005. Different letters and asterisks above bars denote means that differed significantly (P , 0.05) in SNK post hoc comparisons. RI is Rhode Island, MC is mid-coast Maine, and EM is eastern Maine.

SE]) than in RI (39.8 6 4.4) and EM (46.6 6 4.7; oneway ANOVA, F ¼ 11.4, df ¼ 2, 8, P ¼ 0.004). DISCUSSION Few studies have tested for regional consistency in the influence of habitat fragmentation on faunal survival or movement in marine systems. We found that juvenile American lobsters inhabiting cobble habitat in coastal New England were more likely to move within contiguous habitat than within patchy habitat, with the exception of eastern Maine (EM) in 2005 where movement rates were similar between contiguous and patchy plots. Though we found an interactive effect of region and patchiness in 2005, it did not match our prediction that patchiness would deter lobster movement in Rhode Island (RI), where predator densities are high and competition for shelters is low, but not deter movement in mid-coast Maine (MC) and EM, where predator densities are low and competition for shelters is high. Instead, lobster movement was deterred by patchiness even in MC, where lobster densities and competition for shelters are highest and where many untagged lobsters quickly immigrated to plots. Thus, effects of patchiness were not entirely consistent across

FIG. 2. Density of untagged lobsters (mean þ SE) moving to contiguous or patchy cobble plots after one day in 2004 and 2005. Abbreviations for regions are as in Fig. 1; study site codes are explained in Appendix A.

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to have switched shelters, and those shelters were more likely to be occupied by another lobster, in MC than in RI or EM. Lobsters are not the only large-bodied inhabitant of cobble habitat in New England; rock crabs (C. borealis and C. irroratus), and to a lesser extent green crabs (Carcinus maenus), were frequent inhabitants of our cobble plots. Differences in crab abundance among regions may help explain trends in lobster behavioral responses to patchiness, as crabs are predators of juvenile lobsters and may deter lobster movement from shelter (Wahle and Steneck 1992, Rossong et al. 2006). We sampled multiple sites in RI, MC, and EM in 2003 and found that the collective abundance of Cancer spp. and Carcinus maenus was four- to fivefold higher in MC than in RI, and twofold higher in EM than in MC (Appendix E), which matches recent sharp increases in the abundance of these crabs in Maine observed in cobble sampling time series (R. A. Wahle, unpublished data). As a result, increased predation by crabs (or at least perceived predation risk by lobsters) may compensate for reduced predation by fishes in Maine, creating similar responses to patchiness among regions. For instance, relative juvenile lobster mortality, measured by tethering, was threefold higher in RI than in MC in 2000 but did not differ among RI, MC, and EM in 2004 and 2005, due primarily to increased lobster relative mortality in Maine (Brown 2007). Although we do not know what proportion of tagged lobsters in the present study were lost to predation vs. movement beyond plot borders, from 2004 to 2005 the proportion of tagged juvenile lobsters recovered decreased in MC and increased in RI. Additionally, we found an inverse relationship between lobster movement from inner to outer trays and crab density in outer trays, although this explained a relatively small amount of the variability in lobster movement among sites. High crab abundance in EM also may help explain the lack of a difference in movement from inner to outer trays between contiguous and patchy plots in EM in 2005, which appeared to be primarily due to unexpectedly low movement from inner to outer trays in contiguous plots at one site. Crabs colonization rates after one day were highest in contiguous cobble plots in EM (Appendix D), and we found five times as many crabs in the outer trays than in the inner trays of contiguous cobble plots in EM (as opposed to, for example, approximately twice as many in outer than in inner trays in MC). We therefore suspect that higher than normal crab use of outer trays within contiguous cobble plots led to reduced movement of lobsters among trays within these plots. Our findings suggest that the effects of landscape structure on ecological processes do not always vary among locations, even if locations differ greatly in landscape context. This generally contrasts the collective results of many other studies on the effects of landscape structure on ecological processes (reviewed by Debinski

1999

FIG. 3. Results of the lobster tagging experiment within naturally occurring cobble habitat in the three regions. (A) Proportion of tagged lobsters remaining in cobble shelters after 48 hours. (B) Proportion of shelters vacated by tagged lobsters that subsequently contained another organism. Region abbreviations are as in Fig. 1.

and Holt 2000), in which substantial variability among studies or locations may be caused by differences in factors such as the underlying causes of habitat fragmentation and loss, predator species, and the density of conspecifics. For instance, the degree to which proximity to edges influenced predation on artificial bird nests varied with the overall amount of fragmentation within the landscape in hardwood forests in the midwestern USA (Donovan et al. 1997), and the effects of forest fragmentation on nest predation in Montana was opposite that found in many studies conducted in eastern U.S. forests, due in large part to differences in predator species and their behaviors between regions (Tewksbury et al. 1998). In experimentally fragmented arenas of grassland habitat, movement rates of deer mice and prairie voles (Diffendorfer et al. 1995) and gray-tailed vole (Microtus canicaudus; Wolff et al. 1997) were reduced as distance between patches increased and patch sizes decreased. However, Norway root vole (Microtus oeconomus) interpatch movement increased as grassland habitat became more fragmented, most likely because habitat fragments became smaller than that required by individual voles, thereby promoting movement to alternative patches (Andreassen et al. 1998). Microtus pennsylvanicus dispersal from grassland habitat patches was influenced by patch shape when

2000


conspecific densities were low, but not when they were high (Harper et al. 1993), and in contrast to expectations, killifish (Rivulus hartii ) movement among refuge patches increased in the presence of a piscivore (Hoplias malabaricus) compared to non-piscivore areas, because killifish were forced to be more selective when predators were present (Gilliam and Fraser 1987). As expected, we found that region and site accounted for most of the variability in untagged lobster movement to cobble patches, due to the inherent differences in lobster densities among regions. Similar to the results of the tagging experiment in naturally occurring cobble habitat, this suggests that high lobster densities promote movement of lobsters and potentially frequent shelter switching. Though the interactive effect of cobble patchiness and region accounted for much less of the variance in lobster movement to patches than did region, lobster colonization rates were higher in patchy than in contiguous patches in MC, but not in RI or EM. Due to high perimeter to area ratios (P:A), patchy habitats may intercept moving organisms more frequently than may contiguous habitats. Colonization rates for juvenile American lobsters were higher in small artificial kelp patches (high P:A) than in larger patches (low P:A; Bologna and Steneck 1993), and the same was true for grass shrimp (Palaemonidae sp.), isopods, and amphipods in artificial seagrass patches (Eggleston et al. 1999). In our study, patchy cobble plots contained an additional 16 m of perimeter relative to contiguous patches. For lobsters, this may have resulted in higher movement rates to patchy than to contiguous patches in MC in 2004, where overall colonization rates were highest and where more lobsters may have been searching for alternative shelter. Though high P:A ratio may increase rates of patch interception by mobile organisms, it also results in a reduction of interior habitat that is necessary for the survival of many organisms, and an increase in edge habitat that may increase predator-induced mortality rates. For instance, relative mortality of tethered juvenile American lobsters was highest at patch edges and decreased going into cobble patches in Rhode Island (Selgrath et al. 2007), likely because predatory fishes often forage along cobble patch edges (Robbins 2004). In Florida seagrass beds, adult bay scallop (Argopectin irradians) survival was lower at habitat edges than in patch interiors (Bologna and Heck 1999), and in Nebraska the probability of occurrence for several grassland breeding birds decreased with P:A ratio, as patches with high P:A ratio contained little interior habitat that promoted offspring survival (Helzer and Jelinski 1999). It is important to study the effects of cobble habitat patchiness on American lobster ecology for several reasons. Cobble habitat is by far the most valuable nursery habitat for American lobsters in New England waters (Wahle and Steneck 1991). Though humaninduced disturbances to submerged cobble habitat are relatively infrequent and natural changes to cobble


landscapes are slight over ecological time scales, cobble habitat generally exists in discrete patches throughout the range of the American lobster (Wahle and Steneck 1991, Selgrath 2006). A variety of studies have focused on the effects of cobble shelter on lobster survival and abundance at small (i.e., within-patch) scales (e.g., Lawton 1987, Wahle and Steneck 1992, Steneck 2006); however, the effects of cobble landscape structure on lobster movement and survival are largely unexplored. Second, American lobsters may be particularly susceptible to post-settlement demographic bottlenecks that limit population size, because they must leave shelters to forage at a size at which they are vulnerable to predators and are subject to potential shelter competition (Wahle and Steneck 1991). It is unknown, however, how recent rapid changes in lobster density (e.g., Wahle et al. 2009) and in the abundance and diversity of predators (e.g., recent decreases in the abundance of predatory fishes in the Gulf of Maine; Worm and Meyers 2003) interact with habitat patchiness to influence lobster population dynamics. To predict how future changes in landscape context may influence post-settlement processes, more experiments conducted at the landscape scale, particularly among regions, are needed. Third, the vast majority of studies that have addressed the effects of landscape structure on organismal survival, abundance, and movement have been conducted in vegetated habitats that are subject to potentially rapid changes over short or long time scales, often via anthropogenic disturbances (e.g., forests, grasslands, and seagrass beds). The ecological value and patchy nature of cobble habitat create an opportunity to determine whether the effects of landscape structure on ecological processes are similar among disparate habitat types. Biogeographical comparisons of the effects of habitat fragmentation and loss on ecological pattern and process, particularly using standardized experimental habitat, are rare. Future studies on how landscape structure influences the survival, movement, and density of organisms should be conducted across biogeographical gradients whenever possible to best determine whether organism responses to patchiness and fragmentation are predictable and what courses of action may minimize the effects of human-induced landscape change. ACKNOWLEDGMENTS We thank J. Mercer, A. Frantz, J. Bowie, T. Langley, C. Luderer, A. Bellantuano, C. Brown, G. Sharrard, and R. Kushner for assisting with field work; S. Cobb, K. Castro, and M. Gufstason for their valuable advice; and two anonymous reviewers for their comments on an earlier draft of this paper. This research was supported by National Science Foundation and National Undersea Research Program grants to R. A. Wahle and K. A. Hovel LITERATURE CITED Acheson, J., and R. S. Steneck. 1997. Bust and then boom in the Maine lobster industry: perspectives of fishers and biologists. North American Journal of Fisheries Management 17:826–847.

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Andreassen, H., P. Hertzberg, and R. Ims. 1998. Space-use response to habitat fragmentation and connectivity in the root vole Microtus oeconomus. Ecology 79:1223–1235. Barnhardt, W. A., J. T. Kelley, D. F. Belknap, S. M. Dickson, and A. R. Kelley. 1996. Surficial geology of the inner continental shelf of the northwestern Gulf of Maine: Piscataqua River to Canada. Maine Geological Survey Open File Report 96-6, 7 Maps at 1:100000. Bell, S. S., R. A. Brooks, B. D. Robbins, M. S. Fonseca, and M. O. Hall. 2001. Faunal response to habitat fragmentation in seagrass habitats: implications for seagrass conservation. Biological Conservation 100:115–123. Bologna, P. A. X., and K. L. Heck, Jr. 1999. Differential predation and growth rates of bay scallops within a seagrass habitat. Journal of Experimental Marine Biology and Ecology 239:299–314. Bologna, P. A. X., and R. S. Steneck. 1993. Kelp beds as habitat for American lobster Homarus americanus. Marine Ecology Progress Series 100:127–134. Brown, C. 2007. Spatial and temporal patterns of predation on the American lobster, Homarus americanus, across New England’s biogeographic transition zone. Thesis. University of Maine, Orono, Maine, USA. Caddy, J. F., and C. Stamatopoulos. 1990. Mapping growth and mortality rates of crevice-dwelling organisms onto a perforated surface: the relevance of ‘‘cover’’ to the carrying capacity of natural and artificial habitats. Estuarine, Coastal and Shelf Science 31:87–106. Collette, B. B., and G. Klein-MacPhee, editors. 2002. Bigelow and Schroeder’s Fishes of the Gulf of Maine. Third edition. Smithsonian Institution Press, Washington, D.C., USA. Debinksi, D. M., and R. D. Holt. 2000. A survey and overview of habitat fragmentation experiments. Conservation Biology 14:342–355. Diffendorfer, J. E., M. S. Gaines, and R. D. Holt. 1995. Habitat fragmentation and movements of three small mammals (Sigmodon, Microtus, and Peromyscus). Ecology 76:827–839. Donovan, T. M., P. W. Jones, E. M. Annand, and F. R. Thompson III. 1997. Variation in local-scale edge effects: mechanisms and landscape context. Ecology 78:2064–2075. Edgar, G. J., and A. I. Robertson. 1992. The influence of seagrass structure on the distribution and abundance of mobile epifauna: pattern and process in a western Australian Amphibolis bed. Journal of Experimental Marine Biology and Ecology 160:13–31. Eggleston, D. B., W. E. Elis, L. L. Etherington, P. Dahlgren, and M. H. Posey. 1999. Organism responses to habitat fragmentation and diversity: habitat colonization by estuarine macrofauna. Journal of Experimental Marine Biology and Ecology 236:107–132. Etherington, L. L., and D. B. Eggleston. 2000. Large-scale blue crab recruitment: linking postlarval transport, post-settlement planktonic dispersal, and multiple nursery habitats. Marine Ecology Progress Series 204:179–198. Gilliam, J. F., and D. F. Fraser. 1987. Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856–1862. Graham, M. H., and M. S. Edwards. 2001. Statistical significance versus fit: estimating the importance of individual factors in ecological analysis of variance. Oikos 93:505– 513. Harper, S., E. Bollinger, and G. Barrett. 1993. Effects of habitat patch shape on population dynamics of meadow voles (Microtus pennsylvanicus). Journal of Mammology 74:1045– 1055. Helzer, C. J., and D. E. Jelinski. 1999. The relative importance of patch area and perimeter–area ratio to grassland breeding birds. Ecological Applications 9:1448–1458. Hovel, K. A., and R. N. Lipcius. 2001. Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82:1814–1829.

2001

Incze, L. S., and C. E. Naimie. 2000. Modelling the transport of lobster (Homarus americanus) larvae and postlarvae in the Gulf of Maine. Fisheries Oceanography 9:99–113. Incze, L. S., R. A. Wahle, and A. T. Palma. 2000. Advection and settlement rates in a benthic invertebrate: recruitment to first benthic stage in Homarus americanus. ICES Journal of Marine Science 57:430–437. Incze, L. S., R. A. Wahle, N. Wolff, C. Wilson, R. S. Steneck, E. Annis, P. Lawton, H. Xue, and Y. Chen. 2006. Early life history and a modeling framework for lobster (Homarus americanus) populations in the Gulf of Maine. Journal of Crustacean Biology 26:555–564. Irlandi, E. A. 1996. The effects of seagrass patch size and energy regime on growth of a suspension-feeding bivalve. Journal of Marine Research 54:161–185. Irlandi, E. A., W. G. Ambrose, Jr., and B. A. Orlando. 1995. Landscape ecology and the marine environment: how spatial configuration of seagrass habitat influences growth and survival of the bay scallop. Oikos 72:307–313. Lawton, P. 1987. Diel activity and foraging behavior of juvenile American lobsters, Homarus americanus. Canadian Journal of Fishery and Aquatic Science 44:1195–1205. Lawton, P., and K. L. Lavalli. 1995. Postlarval, juvenile, adolescent, and adult ecology. Pages 47–88 in J. Factor, editor. Biology of the lobster Homarus americanus. Academic Press, New York, New York, USA. Micheli, F., and C. H. Peterson. 1999. Estuarine vegetated habitats as corridors for predator movements. Conservation Biology 13:869–881. Moksnes, P. O. 2002. The relative importance of habitatspecific settlement, predation and juvenile dispersal for distribution and abundance of young juvenile shore crabs Carcinus maenas L. Journal of Experimental Marine Biology and Ecology 271:41–73. Robbins, S. H. 2004. The biology and behavior of black sea bass (Centropristis striata) on Rhode Island artificial reefs. Thesis. University of Rhode Island, Kingston, Rhode Island, USA. Rossong, M. A., P. J. Williams, M. Comeau, S. C. Mitchell, and J. Apaloo. 2006. Agonistic interactions between the invasive green crab, Carcinus maenus (Linnaeus), and juvenile American lobster, Homarus americanus (Milne Edwards). Journal of Experimental Marine Biology and Ecology 329:281–288. Selgrath, J. C. 2006. Linking American lobsters (Homarus americanus) and benthic habitat configuration in the coastal waters of New England. Thesis. San Diego State University, San Diego, California, USA. Selgrath, J. C., K. A. Hovel, and R. A. Wahle. 2007. Effects of habitat edges on American lobster abundance and survival. Journal of Experimental Marine Biology and Ecology 353: 253–264. Spanier, E., T. P. McKenzie, J. S. Cobb, and M. Clancy. 1998. Behavior of juvenile American lobsters, Homarus americanus, under predation risk. Marine Biology 130:397–406. Steneck, R. S. 2006. Possible demographic consequences of intraspecific shelter competition among American lobsters. Journal of Crustacean Biology 26:628–638. Steneck, R. S., and J. T. Carlton. 2001. Human alterations of marine communities: students beware! Pages 445–468 in M. D. Bertness, S. D. Gaines, and M. E. Hay, editors. Marine community ecology. Sinauer Associates, Sunderland, Massachusetts, USA. Stephens, S. E., D. N. Koons, J. J. Rotella, and D. W. Willey. 2003. Effects of habitat fragmentation on avian nesting success: a review of the evidence at multiple spatial scales. Biological Conservation 115:101–110. Tewksbury, J. J., S. J. Heil, and T. E. Martin. 1998. Breeding productivity does not decline with increasing fragmentation in a western landscape. Ecology 79:2890–2903.

2002


Underwood, A. J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, UK. Wahle, R. A., M. Gibson, and M. J. Fogarty. 2009. Distinguishing disease impacts from larval supply effects in a lobster fishery collapse. Marine Ecology Progress Series 376:185–192. Wahle, R. A., and L. S. Incze. 1997. Pre- and post-settlement processes in recruitment of the American lobster. Journal of Experimental Marine Biology and Ecology 217:179–207. Wahle, R., L. S. Incze, and M. J. Fogarty. 2004. First projections of American lobster fishery recruitment using a settlement index and variable growth. Bulletin of Marine Science 74:101–114. Wahle, R. A., and R. S. Steneck. 1991. Recruitment habitats and nursery grounds of the American lobster Homarus


americanus: a demographic bottleneck? Marine Ecology Progress Series 69:231–243. Wahle, R. A., and R. S. Steneck. 1992. Habitat restrictions in early benthic life: Experiments on habitat selection and in situ predation with the American Lobster. Journal of Experimental Marine Biology and Ecology 157:91–114. Wiens, J. 1995. Habitat fragmentation: island v landscape perspectives on bird conservation. Ibis 137:S97–S104. Witman, J. D., and K. P. Sebens. 1992. Regional variation in fish predation intensity: a historical perspective in the Gulf of Maine. Oecologia 90:305–315. Wolff, J., E. Schauber, and W. Edge. 1997. Effects of habitat loss and fragmentation on the behavior and demography of gray-tailed voles. Conservation Biology 11:945–956. Worm, B., and R. A. Myers. 2003. Meta-analysis of cod– shrimp interactions reveals top-down control in oceanic food webs. Ecology 84:162–173.

APPENDIX A Location of study sites within the three regions in New England (Ecological Archives E091-136-A1).

APPENDIX B Results of t tests on the mean carapace length of tagged lobsters recaptured in outer cobble trays after one day in 2004 and in 2005 (Ecological Archives E091-136-A2).

APPENDIX C Results of a three-way nested ANOVA on the proportion of tagged lobsters recovered within contiguous and patchy constructed cobble plots after one day in 2004 and in 2005 (Ecological Archives E091-136-A3).

APPENDIX D Three-way nested ANOVA results and bar graph for untagged lobster movement into contiguous and patchy constructed cobble plots after 21 days in 2005 (Ecological Archives E091-136-A4).

APPENDIX E One-way ANOVA results and bar graph for crab densities in naturally occurring cobble patches in each region (Ecological Archives E091-136-A5).