David B. Eggleston

The Identification, Conservation, and Management of Estuarine and Marine Nurseries for Fish and Invertebrates

Michael W. Beck, Kenneth L. Heck, Jr., Kenneth W. Able, Daniel L. Childers, David B. Eggleston, Bronwyn M. Gillanders, Benjamin Halpern, Cynthia G. Hays, Kaho Hoshino, Thomas J. Minello, Robert J. Orth, Peter F. Sheridan and Michael P. Weinstein

Ecological processes underlying ontogenetic habitat shifts in a coral reef fish

Distribution of mobile animals may reflect decisions on how to balance conflicting demands associated with foraging and avoiding predators. A simple optimality model predicts that mobile animals should respond to changes in mortality risk (μ) and growth rate (g) by shifting habitats in a way that maximizes net benefits. In this study, field caging and tethering experiments quantified habitat-specific growth rates and mortality risk, respectively, for three different sizes of a coral reef fish, Nassau grouper (Epinephelus striatus), during its juvenile tenure in off-reef nursery habitats. These sizes bracketed the size at which this species undergoes an ontogenetic habitat shift from the interstices of macroalgal clumps (“algal habitat”) to areas outside, or adjacent to, macroalgae and other physically complex microhabitats (“postalgal habitats”). Experimental results were used in a cost–benefit analysis to test the following alternative (but not mutually exclusive) hypotheses: (1) juvenile grouper shift habitats in a way that maximizes growth rates (g); (2) juveniles shift habitats in a way that minimizes mortality (predation) risk (μ); and (3) if trade-offs exist between maximizing growth rate and minimizing mortality risk, juveniles shift habitats in a way that minimizes the ratio of mortality risk to growth rate (μ/g). Results suggested that small fish face a trade-off between living in the relatively safe algal habitat and achieving high growth rates in postalgal habitats. The value of μ/g was significantly lower in the algal than postalgal habitats for small fish, which typically reside in the algal habitat, and significantly lower in postalgal habitats for medium and large fish, which typically reside in postalgal habitats. Thus, habitat use by juvenile Nassau grouper was consistent with the “minimize μ/g hypothesis.” These results highlight how behavioral responses to ecological processes, such as changing predation risk with body size, determine distribution patterns of mobile animals.

DENSITY-DEPENDENT PREDATION, HABITAT VARIATION, AND THE PERSISTENCE OF MARINE BIVALVE PREY

The persistence of prey encountering intense predation varies by species, prey density, and habitat type; however, the collective impact of these factors has rarely been tested experimentally in natural marine systems. Using the thin-shelled clams Mya arenaria and Macoma balthica as prey, and the main epibenthic predator of whole adult clams, the blue crab Callinectes sapidus, we conducted a series of experiments in Chesapeake Bay tributaries that (1) links field abundance and distribution of bivalve prey species with habitat-specific mortality patterns; (2) represents the first comprehensive field test of species-specific, habitat-specific, and density-dependent mortality for subtidal, soft-bottom, deep-burrowing prey; and (3) thereby enables development of a conceptual model to be used as a heuristic tool linking predator–prey dynamics, habitat type, and evolutionary defense tactics for marine benthos. In 15 years of field monitoring, Mya was more common in sand than mud habitats, and Macoma was widely distributed and at higher densities than Mya in mud and sand. In field experiments, mortality of both Mya and Macoma was density dependent in those habitats where the clams are common. The blue crab population in the field exhibited a type III “guild functional response” on Mya in sand, and on Macoma in both mud and sand. Mortality was lower in sand than mud for Mya, and similar in mud and sand for Macoma, correlating with the high abundances of Mya in sand and Macoma in sand and mud. The persistence of large juvenile and adult bivalves when confronted with intense predation derived substantially from a low-density refuge from predation that varied in a species-specific manner with habitat type, demonstrating the species-specific importance of density and habitat to clam survival. We developed a conceptual model detailing the relative importance of behavior, morphology, habitat features, and the basic components of predator–prey interactions to the survival of bivalve molluscs. At one extreme are bivalve molluscs, such as oysters, that emphasize morphological refuges that increase the predators handling time. At the other extreme are bivalves, such as Mya and Macoma, that reduce predator encounter rates. The model is intended to be used as a heuristic tool to develop testable hypotheses.

PRE- AND POST-SETTLEMENT DETERMINANTS OF ESTUARINE DUNGENESS CRAB RECRUITMENT'

Abundance of early juvenile Dungeness crab (Cancer magister) is dramat- ically higher in intertidal shell habitats compared to mud habitats in several coastal estuaries of the Pacific Northwest. To define the mechanisms underlying this habitat-specific pattern in abundance, we concurrently examined four components of recruitment to intertidal shell and mud habitats at two locations within the Grays Harbor estuary (Washington, USA): (1) water column supply of crab megalopae (postlarvae); (2) settlement patterns of crab megalopae 48 h after settlement substrates were deployed; (3) density of first benthic juvenile instars (J1) 48 h after deployment of such substrates; and (4) density of early juvenile crab in shell and mud habitats over a 4-mo period. We also describe the physical processes likely to be influencing postlarval supply within Grays Harbor, and take advantage of natural variation in postlarval supply between two locations, in combination with a predator exclusion experiment, to define the relative importance of postlarval supply vs. post-settlement survival in regulating population size of juvenile crab in certain intertidal habitats. Water column postlarval supply (measured with plankton and neuston nets, and artificial settlement substrates) in terms of both megalopal density (number per cubic metre) and flux (number per hour) was significantly higher in the southern part of the estuary vs. the northern part during a week-long settlement pulse. Our field observations and measurements suggest that spatial variation in postlarval supply was due to local differences in wind- driven surface currents, since tidal current speeds in the two locations were similar. More- over, there was no correlation between current speed and flux of megalopae over the bottom. There was generally no difference in postlarval supply between shell and mud habitats. Our experimental results further indicate that: (1) the abundance of recently settled crab megalopae in 0.25 m2 settlement trays was significantly higher in shell than in mud habitats, irrespective of whether the trays were placed in 3-5 ha of shell vs. mud; (2) there was a positive and significant correlation between postlarval supply and density of megalopae in shell and mud habitats; and (3) there was a positive and significant correlation between postlarval supply and density of J1 instars only in habitats where specific predators were excluded. Once the number of J1 instars at both geographic locations was reduced to similar levels, equivalent but steadily decreasing densities persisted throughout the summer growing season. The decoupling of settlement patterns and density of J1 instars took place within our 48-h sampling interval. Thus, future attempts to examine the correspondence between larval supply and post-settlement abundance of marine benthic species with planktonic larvae should do so at extremely small temporal scales or a critical life history phase may be overlooked. The results from this study demonstrate that substrate selection can affect distribution of juvenile crab, and that predation (including cannibalism) is a key factor regulating local population size of early juvenile crabs in intertidal habitats where postlarval supply is relatively high.

Organism response to habitat patchiness: species and habitat-dependent recruitment of decapod crustaceans

Abstract Habitat fragmentation from natural or anthropogenic causes is a common phenomenon in shallow water marine habitats such as seagrass beds and oyster reefs throughout the world. Thus, habitat- and scale-dependent information on how organisms perceive and respond to changes in the landscape is critical to efforts aimed at predicting the effects of habitat change on population abundance. In estuarine systems, seagrass is considered one of the predominant nursery habitats for numerous ecologically and commercially important species; however, recent information suggests that alternative habitats such as oyster reefs may also be important sites for settlement and refuge. We used artificial seagrass- and shell-filled plastic trays placed on unstructured seafloor in Back Sound, North Carolina, USA to examine the interactive effects of Experiment, Patch size and Habitat type upon recruitment success of four species of decapod crustaceans: the grass shrimps, Palaemonetes intermedius Holthuis, P. pugio Holthuis and P. vulgaris (Say), and the blue crab, Callinectes sapidus Rathbun. Regardless of habitat type, all species of grass shrimp and J1 blue crab responded to habitat patchiness at scales as small as 0.25 to 4 m −2 , whereas larger J2–J4 blue crab did not. Mean densities of all three species of grass shrimp responded in a similar manner to patch size, with significantly higher densities in the smallest patch size (0.25 m −2 ) compared to larger patches (0.5 to 4 m −2 ). Conversely, mean densities of J1 blue crabs were significantly higher in the largest patch size (4 m −2 ) compared to smaller patches (0.25 to 1 m −2 ). There was a negative and significant relationship between the density of grass shrimp predators and density of J1 prey, and no relationship between potential fish predators and J1–J4 prey. Thus, patterns observed for J1 may be dependent upon predators and not habitat patch size. Both species demonstrated different responses to habitat type depending upon relative densities and body size. Mean densities of P. intermedius and P. vulgaris were higher in seagrass than oyster shell during Experiment 1 (May) when shrimp were relatively abundant, but did not differ between habitat types during Experiment 2 (October), when densities were reduced 10-fold. Conversely, densities of P. pugio did not differ between seagrass and oyster shell. Mean densities of J1 blue crab were similar between seagrass and oyster shell, but higher in seagrass than oyster shell for later juvenile stages (J2–J4). Thus, blue crabs may rely equally on seagrass and oyster reefs as an initial settlement and refuge habitat for early juveniles. Our study demonstrates that an organisms response to habitat patchiness is species-specific, and that for a given species, the response is further modified by animal density and body size. The patterns observed in this study further highlight the importance of scale-dependent responses by mobile organisms to complex benthic habitats.

Shelter Selection by Spiny Lobster Under Variable Predation Risk, Social Conditions, and Shelter Size

Shelter use patterns of den—dwelling Caribbean spiny lobster, Panulirus argus, appear to be regulated by predation risk. The risk of predation may be modified by (1) social structure, which alters the effectiveness of communal defense, and (2) the scaling between lobster size and shelter size, which enhances the protective capacity of the den. These hypotheses were tested with field enclosure experiments using artificial lobster shelters, which examined the effects of predation risk (i.e., presence or absence of a major predator, the nurse shark Ginglyostoma cirratum), spiny lobster size, social condition (i.e., presence or absence of conspecifics), and shelter size upon den choice by juvenile and adult P. argus. To corroborate the findings of the enclosure experiments we also quantified seasonal, size—specific abundance patterns of P. argus in the field by deploying artificial lobster shelters (casitas) of different sizes in two habitats that differed primarily in the potential for gregarious interactions: an inner—bay, sand seagrass flat with high lobster densities, and an outer—bay, seagrass bed adjacent to coral reefs with sparsely distributed lobsters. The experimental and observational field results were strikingly similar–social condition and the scaling of lobster size to shelter size jointly regulated den choice patterns of adult and juvenile Panulirus argus, particularly under high predation risk. When conspecific density and predation risk were low, lobsters resided primarily in shelters whose dimensions were scaled to their own; when conspecific density was high and predation risk was low, lobsters resided predominantly in large shelters offering the highest potential for gregariousness; when conspecific density and predation risk were high, lobsters shifted to gregarious habitation in smaller, scaled shelters; and, when predation risk was high and conspecific density was low, lobsters occupied smaller shelters. The frequency of gregariousness in the field was much higher at the inner—bay site, where lobsters were dense, than at the outer—bay site, where lobsters were sparse, even accounting for the difference in lobster density between sites. This study indicates that the density of conspecifics in a given habitat can enhance gregariousness in spiny lobsters, which in turn influences the relative impact of lobster size, shelter size, and predation risk upon den choice. In defining the critical determinants of den choice for P. argus, we also provide an empirical and conceptual framework for identifying how variation in the availability of resources, such as conspecifics and appropriately scaled refuges, influence the distribution and abundance of social, shelter—dwelling species.

Organism responses to habitat fragmentation and diversity: Habitat colonization by estuarine macrofauna

Abstract Ecologists increasingly recognize that their choice of spatial scales may influence greatly their interpretation of ecological systems, and that small changes in the patchiness of habitat resources can produce abrupt, sometimes dramatic shifts in distribution and abundance patterns of a species. Moreover, identification of scale- and habitat-dependent ecological patterns are central to management efforts aimed at predicting the response of organisms to the increasing threat of habitat fragmentation. We used habitat plots containing artificial seagrass, oyster shell, and a mixture of seagrass and shell, placed on unstructured seafloor for 14 days in Back Sound, North Carolina, USA to examine the interactive effects of patch size, habitat diversity and experimental site on colonization by assemblages of estuarine macrofauna. We tested three a priori predictions of the general hypothesis that macrofaunal colonization is scale- and habitat-dependent: (1) colonization (per unit area) will be higher in small patches than in large ones; (2) small macrofauna will show a stronger response to habitat patchiness at a given scale than large macrofauna; and (3) colonization by estuarine macrofauna will be higher in habitat plots containing a mixture of seagrass and oyster shell compared to monotypic plots. Macrofauna responded to habitat patchiness in a complex manner that varied according to habitat type, experimental site, species, taxon, functional group, and animal body size (small: 500 μm–2 mm; large: >2 mm). Of the five out of seven response variables where we observed a significant patch size effect, grass shrimp ( Palaemonidae sp.) and small, mobile crustaceans (i.e., amphipods and isopods) were the only taxonomic or functional groups whose densities were higher in small (0.25 m 2 ) than large (1 m 2 ) patches, as predicted. Moreover, there was a disproportionate reduction in macrofaunal abundance and diversity in small patches of oyster shell compared to seagrass and mixed habitat treatments; this pattern was significant for both the total density and numbers of small species but not for large macrofauna. The total density and number of macrofaunal species was not higher in the mixed habitat treatment compared to seagrass or oyster shell. Our study demonstrates that an organisms response to habitat patchiness is dependent upon species, taxa, functional group, and animal body size, and that an organisms response is further modified by habitat type. The patterns observed in this study highlight the importance of scale- and habitat-dependent responses by mobile organisms to complex benthic habitats, and, because of the disproportionate reduction in faunal density and diversity in small versus large patches of oyster shell, heightens concern over the negative impacts to biodiversity through large-scale fragmentation of subtidal oyster reefs in certain regions.

Importance of Metapopulation Connectivity to Restocking and Restoration of Marine Species

We examine the impact of spatial processes on the efficacy of restocking in species with varying forms of population or metapopulation structure. Metapopulations are classified based on spatial complexity and the degree of connectedness between populations. Designation of effective restocking sites requires careful attention to metapopulation dynamics; populations in the metapopulation can differ dramatically in demography and connectivity, and the sites they occupy can vary in habitat quality. Source populations, which are optimal for restocking, can be distinct geographically and may be a small percentage of the metapopulation. Sink areas, where restocking is almost certain to be fruitless, can nonetheless serve as productive locations for habitat restoration since larvae from source reefs are likely to recruit to these areas. Effective restocking of metapopulations is most likely to be attained by selection of optimal source populations; inattention to metapopulation dynamics can doom restoration efforts with marine species.

Marine reserves for Caribbean spiny lobster: empirical evaluation and theoretical metapopulation recruitment dynamics

Field data on spiny-lobster abundance , habitat quality , and hydrodynamic transport patterns for a reserve ( ECLSP ) and three exploited sites ( CI , EI , LSI ) were used to assess reserve success in reducing fishing mortality and increasing theoretical metapopulation recruitment . Fishing mortality was estimated empirically by quantification of lobster density at ECLSP and the three exploited sites before and after the start of the fishing season in two years . Fishing mortality was estimated to be 47-98% lower at the reserve . Using a circulation model , we theoretically assessed effectiveness of ECLSP and nominal reserves at the exploited sites in augmenting recruitment through redistribution of larvae to all sites . Larvae discharged from ECLSP and EI recruited throughout Exuma Sound, whereas those from LSI and CI recruited only to CI and LSI. Hence, only reserves at EI and ECLSP would be suitable for metapopulation recruitment. In selecting an optimal reserve for metapopulation recruitment, use of information on habitat quality or adult density did not yield a higher probability of success than did determining the reserve location by chance. The only successful strategy was one that used information on transport processes. Designation of effective marine reserves therefore requires careful attention to metapopulation dynamics and recruitment processes.

The Chesapeake Bay Blue Crab (Callinectes sapidus): A Multidisciplinary Approach to Responsible Stock Replenishment

The Chesapeake Bay has traditionally been one of North Americas most productive fishing grounds, supporting the worlds largest blue crab fishery. During the last several decades, fishing mortality and environmental degradation led to ∼ 70% drop in the bays blue crab abundance, 84% decline in its spawning stock, and historically low levels of juvenile recruitment as well as nursery habitats being below carrying capacity. This situation makes the Chesapeake Bay blue crab an appropriate candidate for responsible stock enhancement. A multidisciplinary, multi-institutional program was developed to study the basic biology and life cycle of the blue crab, develop hatchery and nursery technologies for mass production of blue crab juveniles, and assess the potential of using cultured juveniles to enhance blue crab breeding stocks and, in turn, bay-wide abundance and harvests. Basic biology and culture studies enabled closing the life cycle of the blue crab in captivity. Juvenile crabs have been produced year round, with excellent survival. During 2002–2006, over 290,000 cultured crabs were tagged and experimentally released into the bays nursery habitats. Cultured crabs survived as well as their wild counterparts, increased local populations at release sites by 50–250%, grew quickly to sexual maturity, mated, and migrated from the release sites to spawning grounds, contributing to the breeding stock as soon as 5 to 6 months post-release. Findings reported in this text and other articles in this volume are indicative of the feasibility of our approach of using hatchery juveniles to replenish the blue crab breeding stocks in the Chesapeake Bay.