William S. Arnold

AN EMPIRICAL TEST OF PREDICTIONS OF TWO COMPETING MODELS FOR THE MAINTENANCE AND FATE OF HYBRID ZONES: BOTH MODELS ARE SUPPORTED IN A HARD-CLAM HYBRID ZONE

Two models developed to discern the mode of selection in hybrid zones differ in some predictions. The tension‐zone model predicts that selection acts against hybrids and independently of the environment (endogenous selection) and that selection is invariant throughout the hybrid zone. The ecological selection‐gradient, or ecotone, model maintains that fitness of different genotypes varies in response to environmental variation (exogenous selection) and thus, that in a region of the zone, fitness of hybrids is at least equal to that of the parental species. Therefore, to assess the predominant mode of selection operating in a hybrid zone, it is fundamental to evaluate whether selection is acting specifically against hybrid individuals, that is, whether hybridity alone is the basis for deficiencies of hybrids, and to evaluate whether the relative fitness of hybrids versus that of pure species varies across the zone. In a hardclam (genus Mercenaria) hybrid zone located in a polyhaline lagoon in east‐central Florida, we used age‐specific and location‐specific analyses to determine that a hybrid deficit occurrs, that the deficit seems to be due to selection against hybrids, and that selection varies across the zone. Various measures of deviation from Hardy‐Weinberg equilibrium, linkage disequilibrium analyses, and shifts in allele frequencies at semidiagnostic loci support the idea that selection is strongest in the northern region of the lagoon, the zone of sympatry and hybridization. Southward, into the range of M. mercenaria (the numerically predominant species), the percentage of hybrids remains relatively high and selection against hybrids decreases. For some genetic linkage groups, selection for M. mercenaria alleles seems to be occurring, but selection seems to be acting principally against alleles characteristic of M. mercenaria and, to a lesser degree, for alleles characteristic of M. campechiensis (the rarer species). These findings and others from previous analyses we have done on this hybrid zone demonstrate that selection in the zone is complex, and that characteristics of both the tension‐zone and ecotone models are present. Supporting the tension‐zone model, selection against hybrids per se clearly occurs, but specific genotypes seem to be at a selective disadvantage, whereas others have a selective advantage, and selection operates differentially on the two parental species within the zone. Supporting the ecotone model, the strength of overall selection varies throughout the zone, and environmentally mediated selection in which each species and hybrids have an advantage in specific habitats occurs, but some selection against hybrids is invariant throughout the zone. Thus, the structure and genetic architecture of this hybrid zone appear to be products of a complicated interaction between both types of selective forces cited in the two competing models.

RANGE AND DISPERSAL OF A TROPICAL MARINE INVADER, THE ASIAN GREEN MUSSEL, PERNA VIRIDIS, IN SUBTROPICAL WATERS OF THE SOUTHEASTERN UNITED STATES

Abstract The tropical Asian green mussel, Perna viridis (Bivalvia: Mytilidae) is a recent invader in the Caribbean Basin, including the subtropical southeastern United States. In this study we examined the (1) range of P. viridis in the southeastern United States, (2) relative abundance of P. viridis across habitats and (3) density of P. viridis in Tampa Bay, FL. The invasion and spread of P. viridis in the southeastern United States was estimated by a combination of first-hand qualitative sampling and second-hand observations. There were apparently at least two discrete introductions, each followed by natural dispersal. The initial invasion was discovered in Tampa Bay in 1999, and was followed by rapid spread of P. viridis south as far as Marco Island, FL, but limited spread northward. In 2002, a second invasion occurred in northeast Florida, separated from the west Florida population by 650 km of coastline. On the east coast, P. viridis appeared to be distributed discontinuously between South Carolina and the Indian River Lagoon, FL by 2007. The literature concerning native distribution, habitat use and invasion history, and vectors of P. viridis is also reviewed.

Habitat-specific growth of hard clams Mercenaria mercenaria (L.) from the Indian River, Florida

Abstract Microgeographic variation in shell growth rate of Mercenaria mercenaria (L.) among habitats within the Indian River, Florida, was studied to develop a baseline against which the significance of M. mercenaria shell growth rate differences observed over a larger geographic scale could be compared. Hard clams of the genus Mercenaria were collected from 525 randomly located stations within the Indian River during July and August, 1986. Clams ( n = 922) were returned to the laboratory and taxonomically identified using diagnostic protein loci. Clams identified as M. mercenaria ( n = 465) were isolated and their shell growth rate determined by internal shell growth-increment analysis. The annual pattern of internal shell growth-increment formation in genetically identified M. mercenaria from the Indian River was documented using specimens collected monthly from September 1987 through August 1988. The translucent (slow growth) increment was deposited during summer and fall, whereas the remainder of the year was characterized by formation of the opaque (rapid growth) increment. This pattern is similar to that described for other hard clam populations from the southeastern United States. To compare shell growth rates of M. mercenaria among habitats within the Indian River, we used the ω parameter of Gallucci and Quinn. The range of variation in ω among habitats within the Indian River was similar to that observed for hard clams in Narragansett Bay, Rhode Island, but less than that observed for hard clams from various sites throughout the state of Florida. Shell growth rates of M. mercenaria in the Indian River increased with decreasing depth, and shell growth rates were more rapid in areas characterized by the presence of submerged aquatic vegetation than in areas devoid of such vegetation. Results of this study indicate that comparisons of shell growth rates among hard clam populations over a wide geographic range must be tempered by a consideration of shell growth rate variation among habitats within each site.

Time-averaging, evolution, and morphologic variation

Abstract Many fossil assemblages are time-averaged, with multiple generations of organisms mixed into a single stratigraphic horizon. A time-averaged sample of a taxon should be more variable than a single-generation sample if enough morphologic change occurred during the interval of time-averaging. Time-averaging may also alter correlations between morphologic variables and obscure allometric relationships in an evolving population. To investigate these issues, we estimated the variability of six modern, single-generation samples of the bivalve Mercenaria campechiensis using Procrustes analysis and compared them with several time-averaged Pleistocene samples of M. campechiensis and M. permagna. Both the modern and the fossil samples ranged in variability, but these ranges were virtually identical. Morphology was quite stable over the hundreds to many thousands of years that passed as the assemblages accumulated, and the variabilities of the fossil samples could be used to estimate single-generation variability. At one fossil locality, the environment and paleocommunity changed partway through the collection interval; the morphology of Mercenaria appears stable above and below the transition but changes across it. This change is similar in magnitude to the differences between geographically separated modern populations, whereas temporal variation within single environmental settings is distinctly less than geographic variation. Analytical time-averaging (the mixing of fossils from different horizons) between paleocommunities increased variability slightly (but not significantly) above that found in living populations. While its constituent populations appear stable on millennial timescales, M. campechiensis has been evolutionarily static since at least the early to middle Pleistocene.

Application of Larval Release for Restocking and Stock Enhancement of Coastal Marine Bivalve Populations

The coastal zone in the United States and in other areas worldwide is under increasing stress from human population growth and associated development, and that stress extends to the animal populations that occupy coastal habitats. Considerable effort is being expended to restore the habitats and animals that characterize this biome. I herein describe historic and recent developments regarding the application of the larval release approach to marine animal population restocking efforts. Beginning with cod (Gadus morhua) larvae in the late 1800s, the larval form has been exploited for restocking of various fish and invertebrate species with mixed results. Success has been elusive when working with cod and hard clams (Mercenaria spp.), but efforts using striped bass (Morone saxatilis), abalone (Haliotis spp.), and most recently bay scallops (Argopecten irradians) have been at least partially successful. In the case of bay scallops, competent (ready-to-settle) larvae released into containment enclosures were tracked through the post-settlement, juvenile, and adult life stages. That sampling scheme provided evidence that the released larvae ultimately contributed to a substantial increase in the subsequent year-class. However, those results are equivocal, and rigorous genetic sampling will be required to fully document the linkage between larval release and subsequent year-class strength. It is concluded that larval release, while not suitable for all species in all situations, may be an effective strategy for rebuilding marine animal populations.

RESTORATION OF BAY SCALLOP (ARGOPECTEN IRRADIANS (LAMARCK)) POPULATIONS IN FLORIDA COASTAL WATERS: PLANTING TECHNIQUES AND THE GROWTH, MORTALITY AND REPRODUCTIVE DEVELOPMENT OF PLANTED SCALLOPS

Abstract Bay scallops (Argopecten irradians [Lamarck]) are a culturally and economically important component of Floridas nearshore marine community. However, many of the local populations that compose the bay scallop metapopulation in Florida have virtually disappeared since the 1950s. This study reports the results of a 3-year effort to restore bay scallop populations at 4 sites along the west central coast of the state (Tampa Bay, Anclote, Homosassa and Crystal River). During late summer of 1997, 1998 and 1999, wild adult scallops were retrieved from each of those four target sites and induced to spawn in the laboratory. The resultant offspring were grown to at least 20-mm shell height in a nursery setting and then transplanted to cages deployed at the site where their parents were originally harvested. The growth, survival and reproductive development of the planted scallops were recorded on an approximate 6-week schedule. Results suggest that caged scallops generally grew more slowly than their wild counterparts and that at most of the planting sites mortality was high, especially during late summer. Reproductive development and spawning, although delayed in the caged scallops relative to their wild conspecifics, appears to have proceeded in an otherwise normal fashion. Approximately 1,100 scallops survived and spawned during the first year of the project, whereas ~4,700 and 12,000 scallops survived to spawn in the second and third years of the project, respectively. Studies were also conducted to determine the optimal stocking density and the best placement of the cages. Results of the density study indicate that planting at lower densities increased growth and survival but did not necessarily result in more live scallops at the time of spawning. Results of the cage-placement study, which compared scallops planted in cages either inside or outside of a seagrass bed and either mounted on legs or placed directly on the sediment, revealed that scallops planted directly on the substrate within a seagrass bed suffered higher mortality and slower growth than did scallops planted in the other three treatment combinations. Overall results of this 3-year project suggest that planting cultured scallops in cages can be a successful strategy for increasing the local spawner stock density of bay scallops in depleted populations and, ultimately, for increasing larval supply to the metapopulation.

Contemporaneous deposition of annual growth bands in Mercenaria mercenaria (Linnaeus), Mercenaria campechiensis (Gmelin), and their natural hybrid forms

Abstract We analyzed the periodicity of annual band deposition in the shells of each of three hard clam genotype classes ( Mercenaria mercenaria (Linnaeus), Mercenaria campechiensis (Gmelin), and hybrid forms of the two species) collected from the Indian River lagoon, Florida. Terminal growth bands from each of 396 genetically identified specimens were studied, using the translucent–opaque staging method, to determine the seasonality of rapid vs. slow shell growth. The pattern of terminal growth-band formation that we describe for M. mercenaria from the Indian River is similar to patterns observed for conspecifics collected from Georgia and North Carolina; the translucent growth band (indicative of relatively slow shell growth) is formed during summer and fall, and the opaque growth band (indicative of relatively rapid shell growth) is formed during winter and spring. During summer and fall, growth-band formation in M. campechiensis and hybrid forms is similar to that observed for M . mercenaria . In contrast, during winter and spring subtle but significant deviations from the M . mercenaria growth pattern were noted. For M . campechiensis , relatively equal proportions of the translucent and opaque growth stages were recorded among specimens collected during both the winter and spring seasons. Hybrid forms exhibited a seasonal pattern of terminal growth-band formation reflecting characteristics of each of the two parental species. During winter, translucent and opaque terminal growth bands were equally represented among hybrids (as in M . campechiensis ), whereas in spring significantly more hybrids were in the opaque growth stage (as in M . mercenaria ). The consistency that we describe among genotype classes in the seasonal pattern of growth-band formation suggests that previously described geographic differences in those patterns are primarily mediated by environmental factors rather than by inherent genotypic differences among populations. Nevertheless, subtle differences in the proportions of opaque vs. translucent growth bands observed between species during the rapid-growth stage and the intermediate nature of the hybrid growth pattern at that time suggest that some genetically mediated divergence in the seasonality of growth has occurred during the evolution of these two species.

Increase in Bay Scallop (Argopecten irradians) Populations Following Releases of Competent Larvae in Two West Florida Estuaries

ABSTRACT We propose the release of ready-to-set pediveliger larvae as a restoration strategy for bivalve shellfish. In this study, bay scallop (Argopecten irradians) larvae were released within two West Florida estuaries (Pine Island Sound and Boca Cicga Bay) currently closed to scallop harvest and where local scallop populations arc severely depleted relative to historical abundances. Populations in both estuaries appear to have limited larval supply and show no tendency toward natural recovery after decades of decline. Larvae were either released into enclosures or free released on four separate dates in each estuary. On a given day we used 1, 2, 3, or 4 enclosures per site; multiple release sites; and multiple releases within a year. Assessments were made via several methods, including larval recruitment to collectors, juvenile quadrat surveys, adult timed surveys, and adult transect surveys. In Pine Island Sound, following the initial larval releases in 2003, an isolated recovery in adult scallops was observed at the release site in 2004 followed by a massive resurgence in the local population in 2005. This population declined dramatically in 2006, however, and had completely collapsed by 2007. In Boca Ciega Bay, the series of larval releases did not immediately produce any detectable scallop patches, but the combined releases did immediately precede a population resurgence to levels greater than had been observed in the past three decades. Scallop abundance increased 10-fold at 10 stations in Boca Ciega Bay from 2007 to 2008. In both Pine Island Sound and Boca Ciega Bay, the increases in scallop populations were probably the result of successful survival, growth, and reproduction of the released larvae, followed by successful recruitment and growth of the subsequent generation.

Biological Assessment of Eastern Oysters (Crassostrea virginica) Inhabiting Reef, Mangrove, Seawall, and Restoration Substrates

The eastern oyster, Crassostrea virginica, plays an essential functional role in many estuarine ecosystems on the east and Gulf coasts of the USA. Oysters form biogenic reefs but also live on alternative intertidal substrates such as artificial surfaces and mangrove prop roots. The hypothesis tested in this study was that non-reef-dwelling oysters (i.e., those inhabiting mangrove, seawall, or restoration substrates) were similar to their reef-dwelling counterparts based upon a suite of biological parameters. The study was carried out at six sites in three zones in Tampa Bay on the west coast of Florida using monthly samples collected from October 2008–September 2009. The timing of gametogenesis and spawning, fecundity, and juvenile recruitment were the same for oysters in all four habitats. Oyster size (measured as shell height), density, and Perkinsus marinus infection intensity and prevalence varied among habitats. This study indicates that oysters on mangroves, seawalls, and oyster restoration substrates contribute larvae, habitats for other species, and likely other ecosystem benefits similar to those of intertidal oyster reefs in Tampa Bay. Oysters from alternative intertidal substrates should be included in any system wide studies of oyster abundance, clearance rates, and the provision of alternate habitats, especially in highly developed estuaries.

Isotope sclerochronology of Mercenaria mercenaria, M. Campechiensis, And their natural hybrid form: Does genotype matter?

Abstract Isotopic variation in northern and southern hard clam (quahog) shells is used in studies including paleoecology, paleoclimatology, and archaeology. It is unknown, however, whether species-specific isotopic differences exist. Three genotypes—Mercenaria mercenaria, M. campechiensis, and their natural hybrid form—are found in coastal Florida waters and differentiation of genotypes can be difficult to determine morphologically. This issue may be problematic when using archaeological shells as paleoclimate archives, because genetic analysis cannot be done on such specimens. Their co-occurrence in coastal Florida waters provides a unique opportunity to study whether all three genotypes of modern individuals record the same environmental information preserved as variation in oxygen and stable carbon isotope ratios. A random sample of 49 individuals collected alive at the same time and from the same locality in Pine Island Sound were classified to genotype using allozyme electrophoresis. Three juveniles from each genotype were selected for isotopic analysis to control for ontogenetic effects. Timing of growth increment formation inferred from oxygen isotope ratios reveals similar overall patterns wherein dark (slow growth) increments formed in mid- to late spring and light (fast growth) increments formed in late fall. Results of the mixed model ANOVA (analysis of variance) indicate that no significant species-related differences exist in the variation of oxygen and carbon isotope ratios, although the Kolmogorov-Smirnov goodness-of-fit test detected a systematic difference among δ13C values of M. mercenaria and M. campechiensis comparison and M. mercenaria and the hybrid shell comparison. Any genotype or combination thereof is, thus, suitable for environmental and climate reconstruction using oxygen isotope ratios. The utility of carbon isotope ratios as an environmental proxy, however, remains questionable.