Romuald N. Lipcius

HABITAT FRAGMENTATION IN A SEAGRASS LANDSCAPE: PATCH SIZE AND COMPLEXITY CONTROL BLUE CRAB SURVIVAL

Habitat fragmentation is increasingly common on land and in the sea, leading to small, isolated habitat patches in which ecological processes may differ substantially from those in larger, continuous habitats. Seagrass is a productive but fragmented subtidal habitat that serves as a refuge from predation for many animals because its structural complexity limits the detection and capture of resident prey. The singular influence of seagrass habitat fragmentation (e.g., patch size) on faunal survival is largely unknown and has been difficult to quantify because seagrass habitat complexity (e.g., shoot density) and patch size are often confounded and vary seasonally. In early summer 1998 we quantified the effect of seagrass habitat fragmentation on juvenile blue crab (Callinectes sapidus) survival in the absence of covarying complexity by exposing tethered crabs to predators in density-controlled, artificial eelgrass (Zostera marina) plots embedded within natural seagrass patches of four broad size classes ( 30 000 M2). We repeated this experiment in late summer 1998 with three different shoot densities, after predictable environmental events (defoliation and bioturbation) had increased seagrass habitat frag- mentation and decreased shoot density. In early summer; crab survival was inversely cor- related with seagrass patch area; survival of juvenile blue crabs increased as patch size decreased, in contrast to patterns typically observed in terrestrial and marine systems. This pattern appears to have been due to low abundance of adult blue crabs, the chief predator of juvenile conspecifics, in small patches. In late summer; blue crab survival was greater than in early summer, and survival increased with artificial seagrass shoot density but did not vary with patch size. The breakdown of the relationship between crab survival and patch size in late summer may have resulted from influx of cownose rays, which fragmented large, continuous patches of seagrass into smaller patches in midsummer, potentially equal- izing fragmentation across the seagrass meadow. These results show that (1) fragmented seagrass landscapes hold significant refuge value for juvenile blue crabs, (2) fragmentation and crab survival vary temporally, and (3) crab survival increases with habitat complexity (shoot density) regardless of patch size. The findings indicate that habitat patch size and complexity jointly drive organismal survival, and that their influence differs temporally in this dynamic landscape. Thus, ecological processes are sensitive to landscape structure, and studies of habitat structure should incorporate multiple scales of space and time, as well as potentially confounding structural variables.

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. n nIn 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. n nWe 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.

Unprecedented Restoration of a Native Oyster Metapopulation

Restoring Oysters Populations and wild fisheries of native oyster species have collapsed worldwide because of overfishing and habitat destruction, resulting in severe ecosystem alteration and degradation. Expensive restoration efforts have met with little success, leading to the introduction of non-native oyster species in an attempt to recover lost economic and ecological benefits. In the Chesapeake Bay on the U.S. East Coast, eastern oyster landings and population abundance have plummeted to approximately 1% of historical levels, despite considerable expensive attempts to restore the fishery. Schulte et al. (p. 1124, published online 30 July) present field evidence of a successful restoration of a large metapopulation of native oysters in the Great Wicomico River, a tributary on the western shore of the Chesapeake Bay. The metapopulation is composed of a network of reef complexes spanning 35 hectares and comprises an estimated 185 million live native oysters of 1-year-old juveniles and 2- and 3-year-old adults. The height of oyster reefs above the river bed promotes their restoration in the Chesapeake Bay, USA. Native oyster species were once vital ecosystem engineers, but their populations have collapsed worldwide because of overfishing and habitat destruction. In 2004, we initiated a vast (35-hectare) field experiment by constructing native oyster reefs of three types (high-relief, low-relief, and unrestored) in nine protected sanctuaries throughout the Great Wicomico River in Virginia, United States. Upon sampling in 2007 and 2009, we found a thriving metapopulation comprising 185 million oysters of various age classes. Oyster density was fourfold greater on high-relief than on low-relief reefs, explaining the failure of past attempts. Juvenile recruitment and reef accretion correlated with oyster density, facilitating reef development and population persistence. This reestablished metapopulation is the largest of any native oyster worldwide and validates ecological restoration of native oyster species.

Variable functional responses of a marine predator in dissimilar homogeneous microhabitats

Adult soft-shelled clams {Mya arenaria) persist at low densities in Chesapeake Bay sandy habitats despite intense predation by blue crabs {Callinectes sapidus). Clam persistence may be a consequence of variation in blue crab foraging rates as a function of clam density and sediment composition. In laboratory aquaria, we measured the functional responses (prey consumption per predator as a function of prey density) of large blue crabs to six densities of adult soft-shelled clams buried at natural depths in two sediment types (mud and sand). Functional responses in sand and mud were differentiated statistically by analyses of (1) residuals and residual sums of squares of discrete and continuous-time models, and (2) the exponent (3 of a general functional response model. Crab predation rates were significantly higher in mud than sand, and functional responses differed significantly between these two substrates. Blue crabs displayed type III (sigmoid) density-dependent functional responses in sand, and type II (decelerating rise to an upper asymptote) inversely density- dependent responses in mud. Risk of mortality for clams decreased sharply in sand at low densities similar to those observed in the field near the end of the annual period of active predation. These observations (1) suggest that variable blue crab functional responses result in microhabitat-specific mortality rates of benthic prey, and (2) indicate that functional responses can differ significantly according to the physical properties of topographically simple 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.

Cannibal-prey dynamics in young juveniles and postlarvae of the blue crab

Although cannibalism can act as a density-dependent regulator of population size in terrestrial systems, little is known of its effects in the marine environment. Herein we investigate the influence of cannibalism upon the early life history stages of the blue crab, Callinectes sapidus Rathbun, emphasizing cannibalism between juveniles and postlarvae (i.e. megalopae) of the same year class. In laboratory mesocosms we examined various factors modulating cannibal–prey dynamics, specifically: (1) the effects of habitat and presence of conspecifics on postlarval metamorphosis rate; (2) the effect of metamorphosis rate on the mortality of postlarvae from both intra- and inter-cohort cannibalism; (3) the effects of habitat and predator density on the functional response of young juvenile blue crab predators to varying densities of postlarval prey, and (4) the effects of prey size and habitat on predation mortality. n nInter-cohort cannibalism caused significant mortality in every crab size and habitat type combination, and was lower in grass than sand for all prey smaller than fifth instar. Cannibalism between postlarvae was associated with metamorphosis and was density-dependent in sand, but not present in grass. Metamorphosis rates of postlarvae were inversely density-dependent in sand, but density-independent and higher in grass, indicating that habitat and intra-cohort agonism likely affects postlarval metamorphosis rates. Inter-cohort cannibalism was negatively correlated with metamorphosis rates of postlarvae. The functional response of young juvenile cannibalistic blue crabs differed significantly between sand and grass habitats, and between medium and high predator densities. Juvenile crabs displayed a type II, inversely density-dependent functional response in sand, resulting in very high mortality at low densities of postlarval prey. In grass, the crabs displayed a weak type III, density dependent response, yielding significantly lower mortality at low prey densities. Thus, habitat complexity changes the form of the functional response in cannibal–prey interactions and grass provides a relative habitat refuge from cannibalism. Doubling the number of predators in grass decreased the consumption rates per predator significantly and eliminated the density-dependence, indicating that intraspecific density can qualitatively change the form of the functional response. In the crab size experiment, only prey smaller than fifth instars received a habitat refuge from cannibalism in grass, whereas fifth instars received a relative size refuge in sand. n nOur results demonstrate that intra-year class cannibalism can cause mortality upon settling megalopae and first juvenile instars that is dependent on prey density. We expect inter-cohort cannibalism to cause local extinction of cohorts settling in sand, especially at low settlement densities, and high mortality at moderate settlement densities in grass. Satiation of predators at high settlement densities in grass suggests that episodic settlement can overwhelm predators locally. Furthermore, density-dependent mutual interference within large cohorts in the grass beds likely reduces their predation efficiency, indicating that aggregation of conspecific predators in grass habitats does not necessary lead to an increase in predation pressure. Finally, a relative size-refuge from inter-cohort cannibalism for fifth instar crabs supports an ontogenetic habitat shift around this crab size, which may be influenced by density-dependent agonistic behavior within cohorts. We suggest that intra-year class cannibalism is a major process regulating both survival and dispersal in megalopae and juvenile blue crabs.

Density-Dependent Settler-Recruit-Juvenile Relationships in Blue Crabs

Current theory on the population dynamics of marine species with complex life history patterns posits that a suite of physical and biotic forces (e.g., habitat structure and density-dependent predation or emigration) control survival and abundance in early life history, particularly after settlement. We have conducted a long-term sampling effort accompanied by a series of field and laboratory experiments examining the joint effects of habitat type, body size, and population density upon abundance and survival of early juveniles of the blue crab, Callinectes sapidus. In addition, the chance occurrence of a tropical storm during one set of experiments provided an opportunity to assess the impact of a physical disturbance upon newly settled blue crab survival and abundance. In the 10- yr sampling effort, we quantified relationships between sequential life history stages (ju- venile crab instars) in seagrass beds, the initial nursery habitat for blue crabs in the lower Chesapeake Bay. Inter-instar relationships were defined as the densities of larger instars as dependent on the densities of smaller instars. Inter-instar relationships for the youngest instars are described by hyperbolic functions-until crabs begin to emigrate to unvegetated habitats at approximately the fifth instar. Inter-instar relationships between crabs larger than the fifth instar and smaller crabs become either parabolic or linear functions and decay as the number of instars between sequential life history stages increases. While both the hyperbolic and parabolic functions are indicative of populations regulated by density-de- pendent processes, either predation or emigration, the decay in the functions describing the inter-instar relationships for crabs larger than the fifth instar indicates that the suite of processes regulating this segment of the population changes qualitatively. In laboratory and field experiments, the effects of vegetated and unvegetated habitats and size-specific predation on newly settled juveniles were tested. Tethering was used to quantify relative rates of predation, and a laboratory study was conducted to determine if tethering induced treatment-specific bias. We found no statistically significant interactions between the tethering treatment and the factor treatments of crab size and habitat during the laboratory study, indicating that tethering did not produce treatment-specific bias. Thus, tethering provided a relative measure of predation that allowed comparisons between treat- ments of habitat and crab size on crab survival. In both laboratory and field experiments, survival was significantly higher in vegetated habitats and with increasing size until the ninth instar, when survival did not differ by habitat. This difference explains the dispersal from vegetated to unvegetated habitats that occurred between the fifth and seventh instars. In addition, survival of all crabs was significantly increased both during and after Tropical Storm Danielle compared to pre-storm conditions. A model is developed that describes juvenile survival as a function of crab size and habitat type. Survival curves in both habitats are represented by similar sigmoid functions with survival higher in vegetated habitats. Subsequently, the survival of newly settled blue crabs is likely dependent on the availability of complex habitat. Thus, a suite of biotic and physical processes, both density-dependent and density-independent, control the early life history after settlement for the blue crab.

Effects of seagrass habitat fragmentation on juvenile blue crab survival and abundance

Seagrasses form temporally dynamic, fragmented subtidal landscapes in which both large- and small-scale habitat structure may influence faunal survival and abundance. We compared the relative influences of seagrass (Zostera marina L.) habitat fragmentation (patch size and isolation) and structural complexity (shoot density) on juvenile blue crab (Callinectes sapidus Rathbun) survival and density in a Chesapeake Bay seagrass meadow. We tethered crabs to measure relative survival, suction sampled for crabs to measure density, and took seagrass cores to measure shoot density in patches spanning six orders of magnitude (ca. 0.25–30,000 m2) both before (June) and after (September) seasonally predictable decreases in seagrass structural complexity and increases in seagrass fragmentation. We also determined if juvenile blue crab density and seagrass shoot density varied between the edge and the interior of patches. In June, juvenile blue crab survival was not linearly related to seagrass patch size or to shoot density, but was significantly lower in patches separated by large expanses of unvegetated sediment (isolated patches) than in patches separated by 3000 m2) or very small (<1 m2). Large isolated patches had the lowest shoot densities, which may have allowed predators to easily find tethered crabs. Very small isolated patches had the highest shoot densities and consequently a high abundance of predators (=juvenile conspecifics). Though shoot density did not differ between the edge and the interior of patches, crabs were more abundant in the interior of patches than at the edge. These results indicate that seagrass fragmentation does not have an overriding influence on juvenile blue crab survival and density, and that crab cannibalism and seasonal changes in landscape structure may influence relationships between crab survival and seagrass habitat structure. Habitat fragmentation, structural complexity, faunal density, and time all must be incorporated into future studies on faunal survival in seagrass landscapes.

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.

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.