James Byers currently works at the Odum School of Ecology, University of Georgia. James does research in Ecology, Marine Biology and Parasitology. Their most recent publication is 'Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics'.
Skills and Expertise
Mar 2017 - Jun 2017
Pontifical Catholic University of Chile · Departamento de Ecología
Las Cruces, Chile
University of Georgia · Odum School of Ecology
Aug 2007 - May 2008
University of Wollongong
Digenean trematode parasites obligately utilize multiple host species to complete their life cycles. Trematode abundance therefore can be tightly coupled with the abundance of host species. Accordingly, we investigated whether trematodes could be used to index the abundance of intractable host species. Diamondback terrapins, Malaclemys terrapin, are a species of concern along the US eastern and gulf coasts; however, their population sizes are logistically difficult to quantify. Pleurogonius malaclemys is a terrapin-specific trematode that lives its larval life stages first inside mud snails (Ilyanassa obsoleta), and subsequently as an external metacercarial cyst on hard surfaces such as snail opercula. At each of 12 sites along the Georgia coast, we quantified the prevalence of internal trematode infection among the snail population and the prevalence and mean abundance of external trematode cysts on snail opercula and correlated those metrics with terrapin abundance estimated from mark-recapture methods. Our results demonstrate that the abundance of external cysts along with salinity predict ≥59% of the variability in terrapin abundance. We suggest that tight linkages in the life cycle stages of multi-host parasites make them valuable predictors of host species that are challenging to quantify directly.
Research Items (127)
Host-parasite systems have intricately coupled life cycles, but each interactor can respond differently to changes in environmental variables like temperature. Although vital to predicting how parasitism will respond to climate change, thermal responses of both host and parasite in key traits affecting infection dynamics have rarely been quantified. Through temperature-controlled experiments on an ectothermic host-parasite system, we demonstrate an offset in the thermal optima for survival of infected and uninfected hosts and parasite production. We combine experimentally derived thermal performance curves with field data on seasonal host abundance and parasite prevalence to parameterize an epidemiological model and forecast the dynamical responses to plausible future climate-warming scenarios. In warming scenarios within the coastal southeastern United States, the model predicts sharp declines in parasite prevalence, with local parasite extinction occurring with as little as 2 °C warming. The northern portion of the parasite's current range could experience local increases in transmission, but assuming no thermal adaptation of the parasite, we find no evidence that the parasite will expand its range northward under warming. This work exemplifies that some host populations may experience reduced parasitism in a warming world and highlights the need to measure host and parasite thermal performance to predict infection responses to climate change.
Established populations of introduced Pomacea maculata, a highly fecund, large species of apple snail native to South America, now occur throughout southeast Asia, in Spain and extensively across the southern United States. Substantial research on non-native apple snails takes place in Southeast Asia and has frequently identified apple snails as P. canaliculata. That these Asian populations represent at least two Pomacea species, P. canaliculata and P. maculata, has been confirmed through anatomical and genetic evidence. However, the two species are often still confused because of their similar shell morphologies and life history traits. This contribution reviews the distribution, life history, ecology and management of P. maculata introduced to the southern USA. So far the agricultural impacts of P. maculata in the USA fail to match those of non-native applesnails elsewhere, but the invasion of wetlands by this species suggests the need for increased vigilance to prevent further spread and avoid the ecological impacts that have been associated elsewhere with P. canaliculata.
Risk of infection by parasites can be driven by environmental heterogeneity, often at small scales. We quantified the effect of tidal elevation on infection patterns of two lethal parasites, Perkinsus marinus and Haplosporidium nelsoni, in an important coastal species, the eastern oyster, Crassostrea virginica. Within the southeastern US, oysters in Georgia and South Carolina are rarely found in the subtidal zone. Historically, it has been hypothesized that this pattern could be due to the increased exposure of hosts to waterborne parasites. We manipulated oysters at two tidal elevations (intertidal and subtidal) in a Georgia estuary to test if P. marinus, H. nelsoni, and co-infection by both parasites were different between tidal heights. We found that though P. marinus prevalence and co-infection prevalence of both parasites were not significantly different between tidal elevations, as has been found previously, P. marinus intensity and H. nelsoni prevalence were significantly higher intertidally than subtidally. These findings show that parasite infections can be higher in the host's natural (preferred) tidal height, and suggest that longer exposure to parasites in the subtidal is not a likely reason for the paucity of oysters at that tidal elevation in certain regions of the southeastern US. More broadly, our results provide further evidence that environmental effects on host-parasite interactions can vary by parasite species and across small (meter-long) spatial scales.
Small-scale armoring placed near the marsh-upland interface to protect single-family homes is widespread but understudied. Using a nested, spatially blocked sampling design on the coast of Georgia, USA, we compared the biota and environmental characteristics of 60 marshes adjacent to either a bulkhead, a residential backyard with no armoring, or an intact forest. We found that marshes adjacent to bulkheads were at lower tidal elevations and had features typical of lower elevation marsh habitats: high coverage of the marsh grass Spartina alterniflora, high density of crab burrows, and muddy sediments. Marshes adjacent to unarmored residential sites had higher soil water content and lower porewater salinities than the armored or forested sites, suggesting that there may be increased freshwater input to the marsh at these sites. Deposition of Spartina wrack on the marsh-upland ecotone was negatively related to elevation at armored sites and positively related at unarmored residential and forested sites. Armored and unarmored residential sites had reduced densities of the high marsh crab Armases cinereum, a species that moves readily across the ecotone at forested sites, using both upland and high marsh habitats. Distance from the upland to the nearest creek was longest at forested sites. The effects observed here were subtle, perhaps because of the small-scale, scattered nature of development. Continued installation of bulkheads in the southeast could lead to greater impacts such as those reported in more densely armored areas like the northeastern USA. Moreover, bulkheads provide a barrier to inland marsh migration in the face of sea level rise. Retaining some forest vegetation at the marsh-upland interface and discouraging armoring except in cases of demonstrated need could minimize these impacts.
Although cascading effects of top predators can help structure communities, their influence may vary across habitats that differentially protect prey. Therefore, to understand how and to what degree habitat complexity can affect trophic interactions in adjacent habitats, we used a combination of a broad regional-scale survey, manipulative field trials, and an outdoor mesocosm experiment to quantify predator–prey interaction strengths across four trophic levels. Within estuaries of the southeastern USA, bonnethead sharks (Sphyrna tiburo) hunt blue crabs on mudflats and adjacent oyster reefs, two habitats with vastly different aboveground structure. Using 12-h tethering trials of blue crabs we quantified habitat-dependent loss rates of 37% on reefs and 78% on mudflats. We hypothesized that the sharks’ predatory effects on blue crabs would cascade down to release a lower-level mud crab predator, which subsequently would increase juvenile oyster mortality, but that the cascade strength would be habitat-dependent. We experimentally manipulated predator combinations in split-plot mesocosms containing reef and mudflat habitats, and quantified oyster mortality. Bonnetheads exerted strong consumptive and non-consumptive effects on blue crabs, which ceased eating oysters in the sharks’ presence. However, mud crabs, regardless of shark and blue crab presence, continued to consume oysters, especially within the structural refuge of the reef where they kept oyster mortality high. Thus, bonnetheads indirectly boosted oyster survival, but only on the mudflat where mud crabs were less active. Our work demonstrates how structural differences in adjacent habitats can moderate trophic cascades, particularly when mesopredators exhibit differential use of structure and different sensitivities to top predators.
Despite its widespread use, the ecological effects of shoreline armoring are poorly synthesized and difficult to generalize across soft sediment environments and structure types. We developed a conceptual model that scales predicted ecological effects of shore-parallel armoring based on two axes: engineering purpose of structure (reduce/slow velocities or prevent/stop flow of waves and currents) and hydrodynamic energy (e.g., tides, currents, waves) of soft sediment environments. We predicted greater ecological impacts for structures intended to stop as opposed to slow water flow and with increasing hydrodynamic energy of the environment. We evaluated our predictions with a literature review of effects of shoreline armoring for six possible ecological responses (habitat distribution, species assemblages, trophic structure, nutrient cycling, productivity, and connectivity). The majority of studies were in low-energy environments (51 of 88), and a preponderance addressed changes in two ecological responses associated with armoring: habitat distribution and species assemblages. Across the 207 armoring effects studied, 71% were significantly negative, 22% were significantly positive, and 7% reported no significant difference. Ecological responses varied with engineering purpose of structures, with a higher frequency of negative responses for structures designed to stop water flow within a given hydrodynamic energy level. Comparisons across the hydrodynamic energy axis were less clear-cut, but negative responses prevailed (>78%) in high-energy environments. These results suggest that generalizations of ecological responses to armoring across a range of environmental contexts are possible and that the proposed conceptual model is useful for generating predictions of the direction and relative ecological impacts of shoreline armoring in soft sediment ecosystems.
Non-native species that escape their native range parasites may benefit not only from reduced infection pathology, but also from relaxed selection on costly immune defenses, promoting reallocation of resources towards growth or reproduction. However, benefits accruing from a reduction in defense could come at the cost of increased infection susceptibility. We conducted common garden studies of the shore crab Hemigrapsus sanguineus from highly-parasitized native (Japan) populations and largely parasite-free invasive (USA) populations to test for differences in susceptibility to infection by native-range rhizocephalan parasites, and to explore differences in host resource allocation. Non-native individuals showed at least 1.8 times greater susceptibility to infection than their native counterparts, and had reduced standing metabolic rates, suggesting that less of their energy was spent on physiological self-maintenance. Our results support an indirect advantage to parasite escape via the relaxation of costly physiological defenses. However, this advantage comes at the cost of heightened susceptibility, a tradeoff of parasite escape that is seldom considered. This article is protected by copyright. All rights reserved.
The identification of native sources and vectors of introduced species informs their ecological and evolutionary history and may guide policies that seek to prevent future introductions. Population genetics provides a powerful set of tools to identify origins and vectors. However, these tools can mislead when the native range is poorly sampled or few molecular markers are used. Here, we traced the introduction of the Asian seaweed Gracilaria vermiculophylla (Rhodophyta) into estuaries in coastal western North America, the eastern United States, Europe, and northwestern Africa by genotyping more than 2,500 thalli from 37 native and 53 non-native sites at mitochondrial cox1 and 10 nuclear microsatellite loci. Overall, greater than 90% of introduced thalli had a genetic signature similar to thalli sampled from the coastline of northeastern Japan, strongly indicating this region served as the principal source of the invasion. Notably, northeastern Japan exported the vast majority of the oyster Crassostrea gigas during the 20th century. The preponderance of evidence suggests G. vermiculophylla may have been inadvertently introduced with C. gigas shipments and that northeastern Japan is a common source region for estuarine invaders. Each invaded coastline reflected a complex mix of direct introductions from Japan and secondary introductions from other invaded coastlines. The spread of G. vermiculophylla along each coastline was likely facilitated by aquaculture, fishing, and boating activities. Our ability to document a source region was enabled by a robust sampling of locations and loci that previous studies lacked and strong phylogeographic structure along native coastlines.
Dispersal of many coastal marine species is mediated by flows with strong directionality; bathymetric and topographic effects lead to strong alongshore variability in this transport. Using a simple model of the population dynamics of competing benthic species in a coastal ocean, we found that alongshore variability in dispersal can lead to clustering of species range boundaries for species whose dispersal is dominated by coastal currents. Furthermore, species can be absent from areas where they would have a relative competitive advantage because the presence or absence of a species is determined not only by local conditions but also by propagule supply, which is often affected by larval transport from far upstream. Our model demonstrates the quantitative linkages between alongshore variation in coastal currents, spatial gradients in competitive strength, and the geographic extent of a species. We show that the predictions of the model are consistent with observed species distributions in the Gulf of Maine and Mid-Atlantic Bight, USA. A mechanism for extensive coexistence of competing species where range boundaries cluster is described. The implication of the clustering highlighted by our model suggests that for species whose dispersal is dominated by long-distance planktonic periods, climate change induced changes in the relative competitiveness of species will lead to abrupt changes in species range boundaries and not gradual range extension.
Illuminating the ecological and evolutionary dynamics of parasites is one of the most pressing issues facing modern science, and is critical for basic science, the global economy and human health. Extremely important to this effort are data on the disease-causing organisms of wild animal hosts (including viruses, bacteria, protozoa, helminths, arthropods and fungi). Here we present an updated version of the Global Mammal Parasite Database, a database of the parasites of wild ungulates (artiodactyls and perissodactyls), carnivores, and primates, and make it available for download as complete flat files. The updated database has more than 24,000 entries in the main data file alone, representing data from over 2,700 literature sources. We include data on sampling method and sample sizes when reported, as well as both "reported" and "corrected" (i.e., standardized) binomials for each host and parasite species. Also included are current higher taxonomies and data on transmission modes used by the majority of species of parasites in the database. In the associated metadata we describe the methods used to identify sources and extract data from the primary literature, how entries were checked for errors, methods used to georeference entries, and how host and parasite taxonomies were standardized across the database. We also provide definitions of the data fields in each of the four files that users can download. This article is protected by copyright. All rights reserved.
Parasites often alter host physiology and behavior, which can enhance predation risk for infected hosts. Higher consumption of parasitized prey can in turn lead to a less parasitized prey population (the healthy herd hypothesis). Loxothylacus panopaei is a non-native castrating barnacle parasite on the mud crab Eurypanopeus depressus along the Atlantic coast. Through prey choice mesocosm experiments and a field tethering experiment, we investigated whether the predatory crab Callinectes sapidus and other predators preferentially feed on E. depressus infected with L. panopaei. We found that C. sapidus preferentially consumed infected E. depressus 3 to 1 over visibly uninfected E. depressus in the mesocosm experiments. Similarly, infected E. depressus were consumed 1.2 to 1 over uninfected conspecifics in field tethering trials. We evaluated a mechanism behind this skewed prey choice, specifically whether L. panopaei affects E. depressus movement, making infected prey more vulnerable to predator attack. Counter to our expectations, infected E. depressus ran faster during laboratory trials than uninfected E. depressus, suggesting that quick movement may not decrease predation risk and seems instead to make the prey more vulnerable. Ultimately, the preferential consumption of L. panopaei-infected prey by C. sapidus highlights how interactions between organisms could affect where novel parasites are able to thrive.
Functional trait variation within and across populations can strongly influence population, community, and ecosystem processes, but the relative contributions of genetic vs. environmental factors to this variation are often not clear, potentially complicating conservation and restoration efforts. For example, local adaptation, a particular type of genetic by environmental (G*E) interaction in which the fitness of a population in its own habitat is greater than in other habitats, is often invoked in management practices, even in the absence of supporting evidence. Despite increasing attention to the potential for G*E interactions, few studies have tested multiple populations and environments simultaneously, limiting our understanding of the spatial consistency in patterns of adaptive genetic variation. In addition, few studies explicitly differentiate adaptation in response to predation from other biological and environmental factors. We conducted a reciprocal transplant experiment of first-generation eastern oyster (Crassostrea virginica) juveniles from six populations across three field sites spanning 1000 km in the southeastern Atlantic Bight in both the presence and absence of predation to test for G*E variation in this economically valuable and ecologically important species. We documented significant G*E variation in survival and growth, yet there was no evidence for local adaptation. Condition varied across oyster cohorts: Offspring of northern populations had better condition than offspring from the center of our region. Oyster populations in the southeastern Atlantic Bight differ in juvenile survival, growth, and condition, yet offspring from local broodstock do not have higher survival or growth than those from farther away. In the absence of population-specific performance information, oyster restoration and aquaculture may benefit from incorporating multiple populations into their practices.
Not all hosts, communities or environments are equally hospitable for parasites. Direct and indirect interactions between parasites and their predators, competitors and the environment can influence variability in host exposure, susceptibility and subsequent infection, and these influences may vary across spatial scales. To determine the relative influences of abiotic, biotic and host characteristics on probability of infection across both local and estuary scales, we surveyed the oyster reef-dwelling mud crab Eurypanopeus depressus and its parasite Loxothylacus panopaei, an invasive castrating rhizocephalan, in a hierarchical design across >900 km of the southeastern USA. We quantified the density of hosts, predators of the parasite and host, the host’s oyster reef habitat, and environmental variables that might affect the parasite either directly or indirectly on oyster reefs within 10 estuaries throughout this biogeographic range. Our analyses revealed that both between and within estuary-scale variation and host characteristics influenced L. panopaei prevalence. Several additional biotic and abiotic factors were positive predictors of infection, including predator abundance and the depth of water inundation over reefs at high tide. We demonstrate that in addition to host characteristics, biotic and abiotic community-level variables both serve as large-scale indicators of parasite dynamics.
Impacts of invasive species on ecosystems are often context dependent, making empirical assessments difficult when climatic baselines are shifting and extreme events are becoming more common. We documented a mass mortality event of the Asian clam, Corbicula fluminea, an abundant invasive clam, which has replaced native mussels as the dominant filter-feeding bivalve in the southeastern United States. During an extremely hot and dry period in the summer of 2012, over 99% of Corbicula died in our 10-km study reach of the Broad River, Georgia. Because Corbicula were the only filter-feeding organism in the ecosystem with substantial biomass, their death led to the nearly complete cessation of ecosystem services provided by filter-feeding bivalves. We estimate that following the mass mortality event, turnover time within the sampling reach (reach volume/total filtration) rose from approximately 5 h to over 1200 h. In addition to the loss of filtering capacity, concentrations of total dissolved phosphorus (TDP) and soluble reactive phosphorus (SRP) were also higher in areas where die-off was occurring than in an upstream area without mortality. Mass balance calculations and a manipulative mesocosm experiment predicted TDP and SRP concentrations much higher than our observed values, suggesting that rapid biotic or abiotic uptake of phosphorus may have occurred. Our study demonstrates that climate change can increase the temporal variability of populations of aquatic organisms that provide key ecosystem functions, and highlights that even pulsed, short-lived events can markedly affect systems of reduced diversity.
Baker's Law predicts uniparental reproduction will facilitate colonization success in novel habitats. While evidence supports this prediction among colonizing plants and animals, few studies have investigated shifts in reproductive mode in haplo-diplontic species in which both prolonged haploid and diploid stages separate meiosis and fertilization in time and space. Due to this separation, asexual reproduction can yield the dominance of one of the ploidy stages in colonizing populations. We tested for shifts in ploidy and reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla. Native populations in the northwest Pacific Ocean were nearly always attached by holdfasts to hard substrata and, as is characteristic of the genus, haploid-diploid ratios were slightly diploid-biased. In contrast, along North American and European coastlines, introduced populations nearly always floated atop soft-sediment mudflats and were overwhelmingly dominated by diploid thalli without holdfasts. Introduced populations exhibited population genetic signals consistent with extensive vegetative fragmentation, while native populations did not. Thus, the ecological shift from attached to unattached thalli, ostensibly necessitated by the invasion of soft-sediment habitats, correlated with shifts from sexual to asexual reproduction and slight to strong diploid bias. We extend Baker's Law by predicting other colonizing haplo-diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage. Labile mating systems likely facilitate colonization success and subsequent range expansion, but for haplo-diplontic species, the long-term eco-evolutionary impacts will depend on which ploidy stage is lost and the degree to which asexual reproduction is canalized. This article is protected by copyright. All rights reserved.
Movement of individuals links the effects of local variation in habitat quality with growth and persistence of populations at the landscape scale. When the populations themselves are linked by interspecifc interactions, such as predation, differential movement between habitats may lead to counterintuitive system-wide dynamics. Understanding the interaction between local drivers and dynamics of widely dispersed species is necessary to predict the impacts of habitat fragmentation and degradation, which may be transmitted across habitat boundaries by species' movements. Here we model predator-prey interactions across unaltered and degraded habitat areas, and we explore the additional effects of adaptive habitat choice by predators on the resilience of prey populations. We show how movement between habitats can produce the "bad neighbor effect," in which predators' response to localized habitat degradation causes system-wide loss of prey populations. This effect arises because adaptive foraging results in the concentration of predators in the more productive unaltered habitat, even when this habitat can not support the increased prey mortality. The mechanisms underlying this effect are especially sensitive to prey dispersal rate and adaptive predator behavior.
Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.
Dispersal and adaptation are the two primary mechanisms that set the range distributions for a population or species. As such, understanding how these mechanisms interact in marine organisms in particular – with capacity for long-range dispersal and a poor understanding of what selective environments species are responding to – can provide useful insights for exploration of biogeographic patterns. Previously, the barnacle Notochthamalus scabrosus has revealed two evolutionarily distinct lineages with a joint distribution that suggests an association with one of the two major biogeographic boundaries (~30°S) along the coast of Chile. However, spatial and genomic sampling of this system has been limited until now. We hypothesized that, given the strong oceanographic and environmental shifts associated with the other major biogeographic boundary (~42°S) for Chilean coastal invertebrates, the southern mitochondrial lineage would dominate or go to fixation in locations further to the south. We also evaluated nuclear polymorphism data from 130 SNPs to evaluate the concordance of the nuclear genome with the mitochondrial sample. Through application of standard population genetic approaches along with a Lagrangian ocean connectivity model, we describe the codistribution of these lineages through simultaneous evaluation of coastal lineage frequencies, an approximation of larval behavior, and current-driven dispersal. Our results show that this pattern could not persist without the two lineages having distinct environmental optima. We suggest that a more thorough integration of larval dynamics, explicit dispersal models, and near-shore environmental analysis can explain much of the coastal biogeography of Chile.
Parasites can impart heavy fitness costs on their hosts. Thus, understanding the spatial and temporal consistency in parasite pressure can elucidate the likeliness of parasites’ role as agents of directional selection, as well as revealing variable environmental factors associated with infection risk. We examined spatiotemporal variation in digenetic trematode infection in 18 populations of an intertidal host snail (Littorina littorea) over a 300 km range at an 11-yr interval, more than double the generation time of the snail. Despite a complete turnover in the snail host population, the average change in infection prevalence among populations was <1% over the 11-yr span, and all but three populations remained within 5 percentage points. This consistency of prevalence in each population over time suggests remarkable spatiotemporal constancy in parasite delivery vectors in this system, notably gulls that serve as definitive hosts for the parasites. Thus, despite gulls’ high mobility, their habitat usage patterns are ostensibly relatively fixed in space. Importantly, this spatiotemporal consistency also implies that sites where parasites are recruitment limited remain so over time, and likewise, that parasite hotspots stay hot.
The likelihood of invasion success increases when non-native species engage in mutualisms with a native or non-native species. Mutualisms formed between native and non-native species have been termed “novel mutualisms” and research in terrestrial systems has advanced our understanding of the ecological processes involved in their formation and persistence. However, documentation of novel mutualisms in marine systems is rare. In Atlantic estuaries of the southeastern United States, the native polychaete worm Diopatra cuprea actively decorates its tube with the non-native red seaweed Gracilaria vermiculophylla. We used field and laboratory experiments to test whether the Diopatra-Gracilaria interaction is mutualistic. Diopatra facilitates Gracilaria by securing the seaweed onto the soft-sediment benthos within a favorable tidal elevation for growth and where hard substrata for attachment are otherwise rare. A combination of lab and field experiments suggests that Gracilaria can enhance the growth of Diopatra by increasing access to epifaunal crustacean prey. However, field removal experiments show that the benefits of Gracilaria to Diopatra only occurred in some sites and years. We found no evidence that this invader has a significant negative effect on Diopatra, and it appears, in some instances to even benefit the worms, suggesting that Gracilaria (and its associated impacts on ecosystems) are likely to remain an important component of southeastern US estuaries .
Both parasitism and predation may strongly influence population dynamics and community structure separately or synergistically. Predator species can influence host-parasite interactions, either by preferentially feeding on infected (or uninfected) hosts-and thus altering parasite prevalence patterns-or by affecting host behavior in ways that increase host susceptibility to parasites. In this study, we tested if predators (the mud crab Panopeus herbstii and the blue crab Callinectes sapidus) influence interactions between the eastern oyster Crassostrea virginica and 2 of its most prevalent parasites, Perkinsus marinus and Haplosporidium nelsoni. Using a combination of field and laboratory experiments, we tested for predatory effects on the prevalence and intensity of parasite infections and on oyster immune response (phagocytic activity). Our results consistently demonstrated that crabs do not influence parasite infections in oysters at either individual or population levels. Thus, even though predators often have strong top-down direct and indirect effects on marine communities, we found their influence on host-parasite interactions to be minimal in this system.
Local adaptation may optimize an organism's investment in defenses in response to the risk of infection by spatially heterogeneous parasites and other natural enemies. However, local adaptation may be constrained if recruitment is decoupled from selective pressure experienced by the parent generation. We predicted that the ability of three intertidal littorinid snail species to defend against trematode parasites would depend on prior levels of population exposure to parasites and on larval dispersal mode, a proxy for population openness. In a common garden experiment, for two snail species with direct development and localized recruitment (Littorina obtusata and Littorina saxatilis), hosts from sites with high trematode infection risk were less susceptible to infection than hosts from low-risk sites. However, this relationship was not apparent for a third host species with broadcast larvae (Littorina littorea), suggesting that broad larval dispersal can impede local adaptation; alternatively, the lack of response in this species could owe to other factors that limited experimental infection in this host. Our findings support that locally recruiting hosts can adapt their defenses to scale with localized infection risk.
Strategies for managing biological invasions are often based on the premise that characteristics of invading species and the invaded environment are key predictors of the invader's distribution. Yet, for either biological traits or environmental characteristics to explain distribution, adequate time must have elapsed for species to spread to all potential habitats. We compiled and analyzed a database of natural history and ecological traits of 138 coastal marine invertebrate species, the environmental conditions at sites to which they have been introduced, and their date of first introduction. We found that time since introduction explained the largest fraction (20%) of the variability in non-native range size, while traits of the species and environmental variables had significant, but minimal, influence on non-native range size. The positive relationship between time since introduction and range size indicates that non-native marine invertebrate species are not at equilibrium and are still spreading, posing a major challenge for management of coastal ecosystems.
Microsatellite loci are popular molecular markers due to their resolution in distinguishing individual genotypes. However, they have rarely been used to explore the population dynamics in species with biphasic life cycles in which both haploid and diploid stages develop into independent, functional organisms. We developed microsatellite loci for the haploid–diploid red seaweed Gracilaria vermiculophylla, a widespread non-native species in coastal estuaries of the Northern hemisphere. Forty-two loci were screened for amplification and polymorphism. Nine of these loci were polymorphic across four populations of the extant range with two to eleven alleles observed. Mean observed and expected heterozygosities ranged from 0.265 to 0.527 and 0.317 to 0.387, respectively. Overall, these markers will aid in the study of the invasive history of this seaweed and further studies on the population dynamics of this important haploid–diploid primary producer.
Despite knowledge on invasive species' predatory effects, we know little of their influence as prey. Non-native prey should have a neutral to positive effect on native predators by supplementing the prey base. However, if non-native prey displace native prey, then an invader's net influence should depend on both its abundance and value relative to native prey. We conducted a meta-analysis to quantify the effect of non-native prey on native predator populations. Relative to native prey, non-native prey similarly or negatively affect native predators, but only when studies employed a substitutive design that examined the effects of each prey species in isolation from other prey. When native predators had access to non-native and native prey simultaneously, predator abundance increased significantly relative to pre-invasion abundance. Although non-native prey may have a lower per capita value than native prey, they seem to benefit native predators by serving as a supplemental prey resource. © 2015 John Wiley & Sons Ltd/CNRS.
Letter from several members of the EPA Science Advisory Board Panel on Ballast Water and the National Acedemy of Sciences/National Research Council Committee on Ballast Water claiming that the EPA misstated the SAB Panel's findings as support for its proposed discharge standards
Non-native species can serve as a prey resource for native predators. Yet because there is often no shared evolutionary history between the predator and prey, individuals within a predator population may vary greatly in their willingness to consume a recently introduced, yet profitable prey. Here, we measured individual variation in diet, behavior, and demographic traits of the native predatory mud crab, Panopeus herbstii, and evaluated how these traits influenced an individual’s consumption of a recently introduced, non-native crab, Petrolisthes armatus, using both simultaneous and no-choice assays. These same individual predatory mud crabs were also assayed to quantify their antipredator reaction and exploratory behavior. Results indicated significant variation in the diets of individual predators with 45% specializing on native mussels, 14% specializing on non-native Petrolisthes, and the remainder eating multiple prey species. When given a choice of alternative prey, individual Panopeus predators that consumed a larger proportion of Petrolisthes were female, smaller, and more likely to flee in response to predators. When given no choice of alternative prey, Petrolisthes was consumed more frequently by Panopeus that were female and less exploratory. We suggest that individuals that more readily consume non-native Petrolisthes may be attempting to reduce competition with conspecifics that are larger, more aggressive, exploratory, and male. Our results suggest that at least initially following invasion, adoption of a non-native prey species into the diet of a native predator may not occur universally within the population. Such nonuniform predation pressure could contribute to the non-native prey’s release from natural enemies.
Physical-biological coupling helps structure aquatic communities, yet physical factors can vary widely across large, biogeographic scales. The eastern oyster (Crassostrea virginica) is an ecosystem engineer that creates intertidal reefs, filters water, promotes denitrification, stabilizes shorelines, and provides habitat throughout the inner waters of the U.S. South Atlantic Bight (SAB). We quantified physical variables (temperature, salinity, duration and depth of water inundation), oyster reef properties (slope, vertical relief), and oyster recruitment, density, and biomass over a 1500 km scale across the SAB for one year. All oyster-level and many reef-level variables exhibited unimodal patterns with latitude that peaked in Georgia and South Carolina estuaries. Of the physical variables, salinity and duration of water inundation over reefs were similar across all sites, and temperature declined linearly with increasing latitude, except during summer when it had no relationship with latitude. Depth of water inundation over reefs was the only physical variable with a prominent unimodal distribution that may explain the oyster's biological responses. Similar durations of water inundation across all reefs coupled with higher water depths in the mid-latitude sites collectively indicate that these sites experience higher flow velocity, energy and net water volume delivery per unit time. The resultant higher accumulation of oyster biomass and heightened reef structure in areas of higher tidal energy emphasize that the physical forcing of the SAB (especially large cross-shelf gradients in tidal amplification) affects the biology of the eastern oyster, including its reef properties, with potential implications for community structure and ecosystem service delivery across a biogeographic scale.
Species face multiple selective pressures that may require opposing responses to mitigate. On rocky shorelines, fitness of the intertidal snail Littorina littorea is determined by both parasitism and predation. We experimentally demonstrated that L. littorea was at greatest risk of infection from trematode parasites high in the intertidal zone where it was in closest proximity to abundant gull feces (the vector for the snail's parasites). However, because of extreme, size-selective predation pressure at low tidal elevations, small snails often live high in the intertidal until they have grown sufficiently large. By prolonging their exposure to infection higher on the shore, ontogenetic responses to predation risk accentuate parasite risk. Counterintuitively, snails exhibited the highest trematode prevalence at the lowest tidal elevations where they had almost no risk of contracting infection. By carrying contracted infections into the lowest tidal zones, the larger, predation-resistant snails invert hotspots of infection risk and prevalence, underscoring that size-dependent selection pressures can decouple infection process and pattern even over small scales.
Predator–prey interactions are often highly co-evolved, with selection over time for prey with morphological and behavioral traits that minimize predation risk. Consequently, in many environments prey choose among potential habitats according to their refuge value. It is unclear, however, when presented with new habitats, if prey are able to evaluate the predation risk of these relative to familiar habitats and utilize these in accordance with their value. We tested whether, along the east coast of the USA, native mud crabs Panopeus herbstii utilize the non-native alga Gracilaria vermiculophylla according to its relative refuge value. Experiments examining predation by blue crabs Callinectes sapidus on mud crabs revealed that the non-native alga had an intermediate refuge value relative to native oysters, which were the most protective, and unvegetated sediment, which was the least. In subsequent choice experiments, mud crabs selected oysters over alga over unvegetated sediment, in accordance with habitat refuge values. Further, in field experiments, the use of Gracilaria by mud crabs was inversely related to the proximity of the alga to the preferred habitat type, oysters, and was reduced by the presence of a blue crab predator. Consequently, mud crabs are utilizing the non-native alga Gracilaria in accordance with its intermediate refuge value. The relative refuge value of non-native vs native habitat-forming species may provide a baseline expectation against which to measure the speed of learning and opportunism in the response of native prey to novel protective habitats.
Classic biogeographic studies emphasized differences in species composition between regions to define biogeographic provinces and delimit biogeographic boundaries. Here we analyze the permeability of biogeographic boundaries to different species to gain mechanistic insight into the processes that maintain species boundaries in the coastal ocean. We identify sites with high frequencies of range boundaries using almost 1800 benthic marine invertebrates along the northwestern Atlantic coast and address whether their magnitude and location vary as a function of species’ taxonomy, pelagic larval duration and depth distribution. We observed clusters of species boundaries at Cape Hatteras, Cape Cod and the Bay of Fundy that are largely independent of taxonomic group. However, the boundaries were permeable and asymmetric, with a higher percentage of species shared across boundaries in the equatorward direction (82%) than in the reverse direction (59%). This pattern was particularly strong for shallow species (median occurrence depth < 20 m). Pelagic larval duration was more important to explain distributions of boundaries for deep species (median occurrence depth > 20 m), where species with long larval dispersal had significantly higher occurrence of boundaries than species with short larval dispersal. When they do exist, species boundaries seem to be set by the interaction of currents, depth distribution and pelagic larval duration. Importantly, species boundaries tend to be pinned to regions of reduced water transport, which might explain why species boundaries are concentrated in narrow geographical areas.
Nonnative species that form novel habitats strongly affect ecosystem processes. The effects of these ecosystem engineers can be both positive and negative but the mechanisms behind their effects are not well described. In this study we determined the relative importance of three main mechanisms by which invasive ecosystem engineers can facilitate native fauna. The engineer may provide new physical structure that reduces harsh abiotic conditions or gives refuge from predation (both engineering mechanisms), or provide a new profitable food resource (a trophic mechanism). The invasive seaweed Gracilaria vermiculophylla is a novel addition to estuarine intertidal mudflats of the southeastern United States. The epifaunal amphipod Gammarus mucronatus is up to 100 times more abundant on Gracilaria-invaded mudflats compared to uninvaded mudflats. Feeding assays, a survivorship experiment and stable isotope analysis demonstrated that Gammarus consumes little Gracilaria and cannot survive on Gracilaria alone. However, the structural engineering effects of Gracilaria greatly enhanced the survivorship of Gammarus in the presence of predators during high tide and when exposed to harsh abiotic conditions during low tide. Our results demonstrate that invasive ecosystem engineers can dramatically affect the distribution and abundance of native species by providing a novel protective structure.
Parasites are integral members of natural communities, but large-scale determinants of their abundance and diversity, including the importance of biotic and abiotic factors, both natural and anthropogenic, are often not well understood. Here, we examine which factors best predict larval trematode communities in the mudsnail host Ilyanassa obsoleta across a regional landscape. At 15 salt marsh sites spanning 200 km, we quantified the diversity of trematodes and the prevalence (i.e., proportion) of infected hosts and sampled a broad array of potential parasite predictors including abundance of intermediate and definitive hosts, habitat, nutrients, metals, roads, and sediment characteristics. We identified the set of best performing models to explain variability associated with five metrics of trematode prevalence and diversity using an information-theoretic approach. Results indicate that several anthropogenic factors associate with this trematode community and that the direction of their influence differs. Road density around sites was a strong negative predictor of all trematode prevalence and species richness metrics. Nitrogen, another human influenced variable, was a strong positive predictor for the most abundant trematode species in the system. In addition, the abundance of definitive fish hosts was a positive predictor in several models, confirming the importance of this direct biological link to parasites. Other influential variables included sediment composition and heavy metals (arsenic, copper, lead, and zinc). We discuss possible direct and indirect mechanisms to explain these findings including that anthropogenic factors may be directly influencing free-living stages of trematodes, or be acting as proxies of hard-to-measure hosts.
Invasions by non-native species are a threat to biodiversity because invaders can impact native populations, communities and entire ecosystems. To manage this threat, it is necessary to have a strong mechanistic understanding of how non-native species affect local species and communities. We reviewed 259 published papers (1972–2012) that described field experiments quantifying the impact of aquatic non-native species, to examine whether various types of study biases are limiting this understanding. Our review revealed that invasion impacts had been experimentally quantified for 101 aquatic non-native species, in all major freshwater and marine habitats, on all continents except Antarctica and for most higher taxonomic groupings. Over one-quarter (26%) of studies included tests for impacts on local biodiversity. However, despite this extensive research effort, certain taxa, habitats and regions remain poorly studied. For example, of the over one hundred species examined in previous studies, only one was a marine fish and only six were herbivores. Furthermore, over half (53%) the studies were from the USA and two-thirds (66%) were from experiments conducted in temperate latitudes. By contrast, only 3% of studies were from Africa and <2% from high latitudes. We also found that one-fifth (20%) of studies were conducted in estuaries, but only 1% from coral reefs. Finally, we note that the standard procedure of pooling or not reporting non-significant treatments and responses is likely to limit future synthetic advancement by biasing meta-analysis and severely limiting our ability to identify non-native species with none or negligible ecological impacts. In conclusion, a future focus on poorly-studied taxa, habitats and regions, and enhanced reporting of results, should improve our understanding and management of impacts associated with aquatic non-native species.
Predators can indirectly benefit prey populations by suppressing mid-trophic level consumers, but often the strength and outcome of trophic cascades are uncertain. We manipulated oyster reef communities to test the generality of potential causal factors across a 1000-km region. Densities of oyster consumers were weakly influenced by predators at all sites. In contrast, consumer foraging behaviour in the presence of predators varied considerably, and these behavioural effects altered the trophic cascade across space. Variability in the behavioural cascade was linked to regional gradients in oyster recruitment to and sediment accumulation on reefs. Specifically, asynchronous gradients in these factors influenced whether the benefits of suppressed consumer foraging on oyster recruits exceeded costs of sediment accumulation resulting from decreased consumer activity. Thus, although predation on consumers remains consistent, predator influences on behaviour do not; rather, they interact with environmental gradients to cause biogeographic variability in the net strength of trophic cascades.
To understand what makes some species successful invaders, it is critical to quantify performance differences between native and introduced regions, and among populations occupying a broad range of environmental conditions within each region. However, these data are not available even for the world’s most notorious invasive species. Here we introduce the Global Garlic Mustard Field Survey, a coordinated distributed field survey to collect performance data and germplasm from a single invasive species: garlic mustard (Alliaria petiolata) across its entire distribution using minimal resources. We chose this species for its ecological impacts, prominence in ecological studies of invasion success, simple life history, and several genetic and life history attributes that make it amenable to experimental study. We developed a standardised field survey protocol to estimate population size (area) and density, age structure, plant size and fecundity, as well as damage by herbivores and pathogens in each population, and to collect representative seed samples. Across four years and with contributions from 164 academic and non-academic participants from 16 countries in North America and Europe thus far, we have collected 45,788 measurements and counts of 137,811 plants from 383 populations and seeds from over 5,000 plants. All field data and seed resources will be curated for release to the scientific community. Our goal is to establish A. petiolata as a model species for plant invasion biology and to encourage large collaborative studies of other invasive species.
Non-native species can alter ecosystem functions performed by native species often by displacing influential native species. However, little is known about how ecosystem functions may be modified by trait-mediated indirect effects of non-native species. Oysters and other reef-associated filter feeders enhance water quality by controlling nutrients and contaminants in many estuarine environments. However, this ecosystem service may be mitigated by predation, competition, or other species interactions, especially when such interactions involve non-native species that share little evolutionary history. We assessed trophic and other interference effects on the critical ecosystem service of water filtration in mesocosm experiments. In single-species trials, typical field densities of oysters (Crassostrea virginica) reduced water-column chlorophyll a more strongly than clams (Mercenaria mercenaria). The non-native filter-feeding reef crab Petrolisthes armatus did not draw down chlorophyll a. In multi-species treatments, oysters and clams combined additively to influence chlorophyll a drawdown. Petrolisthes did not affect net filtration when added to the bivalve-only treatments. Addition of the predatory mud crab Panopeus herbstii did not influence oyster feeding rates, but it did stop chlorophyll a drawdown by clams. However, when Petrolisthes was also added in with the clams, the clams filtered at their previously unadulterated rates, possibly because Petrolisthes drew the focus of predators or habituated the clams to crab stimuli. In sum, oysters were the most influential filter feeder, and neither predators nor competitors interfered with their net effect on water-column chlorophyll. In contrast, clams filtered less, but were more sensitive to predators as well as a facilitative buffering effect of Petrolisthes, illustrating that non-native species can indirectly affect an ecosystem service by aiding the performance of a native species.
The evolutionary pressures that drive long larval planktonic durations in some coastal marine organisms, while allowing direct development in others, have been vigorously debated. We introduce into the argument the asymmetric dispersal of larvae by coastal currents and find that the strength of the currents helps determine which dispersal strategies are evolutionarily stable. In a spatially and temporally uniform coastal ocean of finite extent, direct development is always evolutionarily stable. For passively drifting larvae, long planktonic durations are stable when the ratio of mean to fluctuating currents is small and the rate at which larvae increase in size in the plankton is greater than the mortality rate (both in units of per time). However, larval behavior that reduces downstream larval dispersal for a given time in plankton will be selected for, consistent with widespread observations of behaviors that reduce dispersal of marine larvae. Larvae with long planktonic durations are shown to be favored not for the additional dispersal they allow, but for the additional fecundity that larval feeding in the plankton enables. We analyzed the spatial distribution of larval life histories in a large database of coastal marine benthic invertebrates and documented a link between ocean circulation and the frequency of planktotrophy in the coastal ocean. The spatial variation in the frequency of species with planktotrophic larvae is largely consistent with our theory; increases in mean currents lead to a decrease in the fraction of species with planktotrophic larvae over a broad range of temperatures.
Two dominant drivers of species distributions are climate and habitat, both of which are changing rapidly. Understanding the relative importance of variables that can control distributions is critical, especially for invasive species that may spread rapidly and have strong effects on ecosystems.Here, we examine the relative importance of climate and habitat variables in controlling the distribution of the widespread invasive freshwater clam Corbicula fluminea, and we model its future distribution under a suite of climate scenarios using logistic regression and maximum entropy modelling (MaxEnt).Logistic regression identified climate variables as more important than habitat variables in controlling Corbicula distribution. MaxEnt modelling predicted Corbicula's range expansion westward and northward to occupy half of the contiguous United States. By 2080, Corbicula's potential range will expand 25–32%, with more than half of the continental United States being climatically suitable.Our combination of multiple approaches has revealed the importance of climate over habitat in controlling Corbicula's distribution and validates the climate-only MaxEnt model, which can readily examine the consequences of future climate projections.Given the strong influence of climate variables on Corbicula's distribution, as well as Corbicula's ability to disperse quickly and over long distances, Corbicula is poised to expand into New England and the northern Midwest of the United States. Thus, the direct effects of climate change will probably be compounded by the addition of Corbicula and its own influences on ecosystem function.
Impacts of marine invaders on local biodiversity have not been analyzed across invasive species and invaded habitats. We conducted a meta-analysis of 56 field experiments published in 29 papers that examined the effects of marine invaders on local species richness, diversity, and/or evenness. We show that invaders, across studies, typically have negative effects on biodiversity within a trophic level but positive effects on biodiversity of higher trophic levels. For example, both plants and sessile filter-feeders had positive effects on richness and diversity of mobile consumers. The contrasting negative and positive effects on similar versus higher trophic levels are potentially manifested through community-wide antagonism (competition and consumption) versus facilitation (habitat and food provisioning) interactions, respectively. These relation ships extended to functional interactions, as sessile invaders had negative effects on the biodiversity of sessile communities (intra-functional interactions) but positive effects on the biodiversity of mobile communities (inter-functional interactions). Our analyses highlight the importance of pairing attributes of the invader and the impacted organisms to obtain simple predictions of how the diversity of entire communities may respond to species invasions on local scales. We also note that our analysis did not require information on co-evolutionary history but that such data, coupled with long-term large-scale mensurative data, are needed to gain a comprehensive predictive insight into invasion impact.
Drivers of large-scale variability in parasite prevalence are not well understood. For logistical reasons, explorations of spatial patterns in parasites are often performed as observational studies. However, to understand the mechanisms that underlie these spatial patterns, standardized and controlled comparisons are needed. Here, we examined spatial variability in infection of an important fishery species and ecosystem engineer, the oyster (Crassostrea virginica) by its pea crab parasite (Zaops ostreus) across 700 km of the southeastern USA coastline. To minimize the influence of host genetics on infection patterns, we obtained juvenile oysters from a homogeneous source stock and raised them in situ for 3 months at multiple sites with similar environmental characteristics. We found that prevalence of pea crab infection varied between 24 and 73 % across sites, but not systematically across latitude. Of all measured environmental variables, oyster recruitment correlated most strongly (and positively) with pea crab infection, explaining 92 % of the variability in infection across sites. Our data ostensibly suggest that regional processes driving variation in oyster recruitment similarly affect the recruitment of one of its common parasites.
Predicting population establishment based on initial population size is a theoretically and empirically challenging problem whose resolution informs a multitude of applications. Indeed, it is a central problem in the management of introduced, endangered, harvested, and pathogenic organisms. We focus here on introduced species. We synthesize the current state of modeling in this predictive enterprise and outline future directions in the application of these models to developing regulations intended to prevent the establishment of invaders. Descriptive and mechanistic models of single-population introductions are fairly well developed and have provided insight into invasion risk in laboratory and field conditions. However, many invasions stem from large-scale and repeated releases of a multitude of species from relatively indiscriminate invasion vectors associated with international trade and travel. Vector-scale models of invasion risk are less well developed and are characterized largely by the use of untested proxy variables for propagule pressure. We illustrate the problems associated with proxy variables and introduce a more mechanistic theoretical formulation characterizing vector-scale invasion pressure in terms of propagule pressure (number of introduced individuals) and colonization pressure (number of introduced species). We outline key questions to be addressed in applying both single-population and vector-scale models to the development of threshold-based invasion regulations. We illustrate these ecological and applied questions using examples from terrestrial, aquatic, and marine systems. We develop in detail examples from ballast-water transport that, as one of the best-characterized global invasion vectors and one that is subject to emerging international threshold-based biosecurity regulations, provides a rich case study.
Background/Question/Methods Exotic producers can have far-reaching effects on invaded ecosystems, especially where invasion transforms the physical structure of affected environments. One invader that may have such effects is the macroalga Gracilaria vermiculophylla, which has significantly altered the structure and productivity of the estuarine mudflats of Georgia. These intertidal habitats were previously largely devoid of macrophytes, so these changes are likely to affect native fauna living within these systems. However, the nature of these effects will be influenced by whether resident organisms select for or against invaded patches, as well as how the presence of Gracilaria alters their performance. In intertidal habitats, the consequences of these choices are more complex, as both habitat preferences as well as the invader’s effect on species performance may vary depending on whether the mudflat is exposed or inundated. We determined how Gracilaria affects habitat usage of benthic invertebrates during both high and low tide by seasonally manipulating the presence of this invasive macroalga within study plots both above and below mean water level at four sites. Samples were collected the following day through the use of lift baskets (high tide) and by scraping exposed plots (low tide). Field and lab trials then tested the effect of Gracilaria on the survival of resident species during each tidal stage. Results/Conclusions The immigration of invertebrates such as amphipods, shrimp, and crabs into Gracilaria plots exceeded immigration into uninvaded plots. The retention of fauna on the exposed mudflat during low tide was also increased by the presence of Gracilaria. Structural mimics increased immigration and retention, as well, emphasizing the importance of engineering effects as a component of this invasion. Subsequent field and lab trials revealed that Gracilaria can influence the survival of these organisms by providing refuge from predation during high tide as well as shelter from desiccation during low tide. Gracilaria therefore influences resident species both through effects arising from small scale habitat selection (i.e. invaded vs. uninvaded patches) as well as more large scale alterations in habitat usage (i.e. increased retention on the mudflat during tidal drop).
Habitat‐forming invasive species have complex impacts on native communities. Positive above ground and negative below ground impacts are reported, suggesting that habitat‐forming invasive species may affect community components differently. Furthermore, such effects may vary depending on the density of the invader. We determined the responses of community components to different densities of the invasive green alga Caulerpa taxifolia in southeastern Australia. Initially we investigated differences in soft‐sediment faunal communities (above and below ground) across a biomass gradient at two invaded sites. Caulerpa taxifolia biomass was positively associated with the composition and abundance of the epifaunal community, but negatively correlated with the abundance of infauna. To examine the response of common community members in more detail, we caged two species of mollusk (the infaunal bivalve, Anadara trapezia and the epifaunal gastropod, Batillaria australis) across the same biomass gradient to determine lethal and sublethal effects of C. taxifolia biomass on individuals. Survivorship of A. trapezia was low when C. taxifolia was above 300 g m−2. Negative sublethal effects were also density‐dependent with A. trapezia tissue weight being lowest above this same C. taxifolia biomass. The proportion of B. australis surviving was unaffected by C. taxifolia biomass. However, the total number of live B. australis recovered in cages increased as C. taxifolia biomass increased, providing further evidence of positive density dependent effects (in line with the survey data) of C. taxifolia on epifauna. Finally, we removed C. taxifolia from plots of differing C. taxifolia biomass and followed community change for 5 months. Community change following C. taxifolia removal was also density dependent as recovery 5 months post‐removal depended on the initial biomass of C. taxifolia, suggesting a lag in the recovery of communities due to residual environmental effects post‐removal (i.e. hysteresis). We have shown that the effects of a habitat‐forming invasive species are biomass dependent and also affect community components differently, suggesting that, globally, the impact of these types of invaders may be context dependent.
A fundamental assumption in invasion biology is that most invasive species exhibit enhanced performance in their introduced range relative to their home ranges. This idea has given rise to numerous hypotheses explaining "invasion success" by virtue of altered ecological and evolutionary pressures. There are surprisingly few data, however, testing the underlying assumption that the performance of introduced populations, including organism size, reproductive output, and abundance, is enhanced in their introduced compared to their native range. Here, we combined data from published studies to test this hypothesis for 26 plant and 27 animal species that are considered to be invasive. On average, individuals of these 53 species were indeed larger, more fecund, and more abundant in their introduced ranges. The overall mean, however, belied significant variability among species, as roughly half of the investigated species (N=27) performed similarly when compared to conspecific populations in their native range. Thus, although some invasive species are performing better in their new ranges, the pattern is not universal, and just as many are performing largely the same across ranges.
As marine environments change, the greatest ecological shifts-including resource usage and species interactions-are likely to take place in or near regions of biogeographic and phylogeographic transition. However, our understanding of where these transitional regions exist depends on the defining criteria. Here we evaluate phylogeographic transitions using a bootstrapping procedure that allows us to focus on either the strongest genetic transitions between a pair of contiguous populations, versus evaluation of transitions inclusive of the entire overlap between two intraspecific genetic lineages. We compiled data for the Atlantic coast of the United States, and evaluate taxa with short- and long-dispersing larval phases separately. Our results are largely concordant with previous biogeographic and phylogeographic analyses, indicating strong biotic change associated with the regions near Cape Cod, the Delmarva Peninsula, and eastern Florida. However, inclusive analysis of the entire range of sympatry for intraspecific lineages suggests that broad regions-the Mid-Atlantic Bight and eastern Florida-already harbor divergent intraspecific lineages, suggesting the potential for ecological evaluation of resource use between these lineages. This study establishes baseline information for tracking how such patterns change as predicted environmental changes take place.
Predicting the potential range of invasive species is essential for risk assessment, monitoring, and management, and it can also inform us about a species' overall potential invasiveness. However, modeling the distribution of invasive species that have not reached their equilibrium distribution can be problematic for many predictive approaches. We apply the modeling approach of maximum entropy (MaxEnt) that is effective with incomplete, presence-only datasets to predict the distribution of the invasive island apple snail, . This freshwater snail is native to South America and has been spreading in the USA over the last decade from its initial introductions in Texas and Florida. It has now been documented throughout eight southeastern states. The snail's extensive consumption of aquatic vegetation and ability to accumulate and transmit algal toxins through the food web heighten concerns about its spread. Our model shows that under current climate conditions the snail should remain mostly confined to the coastal plain of the southeastern USA where it is limited by minimum temperature in the coldest month and precipitation in the warmest quarter. Furthermore, low pH waters (pH <5.5) are detrimental to the snail's survival and persistence. Of particular note are low-pH blackwater swamps, especially Okefenokee Swamp in southern Georgia (with a pH below 4 in many areas), which are predicted to preclude the snail's establishment even though many of these areas are well matched climatically. Our results elucidate the factors that affect the regional distribution of , while simultaneously presenting a spatial basis for the prediction of its future spread. Furthermore, the model for this species exemplifies that combining climatic and habitat variables is a powerful way to model distributions of invasive species.
Invasive ecosystem engineers can have far-reaching effects on systems, especially if they provide structure where none was before. The non-native seaweed Gracilaria vermiculophylla has proliferated on estuarine mudflats throughout the southeastern US, including areas (South Carolina and Georgia) that historically were extremely low in seaweed biomass. Quantitative field surveys across 150 km of high salinity estuaries revealed that the density of the native onuphid polychaete Diopatra cuprea and the aboveground height of its biogenic tubes, which Diopatra decorates with drifting debris and seaweed, positively influenced Gracilaria biomass. The abundance of Gracilaria epifauna, composed primarily of amphipods and small snails, increased with Gracilaria biomass at many locations in our field surveys. To examine whether epifauna were facilitated by Gracilaria we experimentally manipulated Gracilaria biomass in two locations. Consistent with the field surveys, we found that increasing Gracilaria biomass facilitated epifauna, particularly amphipods and snails. Epifaunal densities on Gracilaria were higher than on a biologically-inert structural mimic of Gracilaria (plastic aquarium alga), indicating that epifauna colonize Gracilaria because Gracilaria provisions both physical structure and a biological resource. We also quantified the seaweed’s net rate of productivity and decomposition. Primary production of Gracilaria was variable, but massive in some areas (up to 200 % net biomass increase in 8 weeks). The seaweed rapidly degraded upon burial in silty sediments (79 % loss in mass within 10 days) and thus may represent an important new addition to detrital foodwebs. As a copious, novel source of primary production, detritus, and desirable habitat for epifauna, Gracilaria has the potential to transform southeastern US estuaries.
Introduced species disrupt native communities and biodiversity worldwide. Parasitic infections (and at times, their absence) are thought to be a key component in the success and impact of biological invasions by plants and animals. They can facilitate or limit invasions, and positively or negatively impact native species. Parasites have not only direct effects on their hosts, but also indirect effects on the species with which their hosts interact. Indirect effects include density-mediated effects (resulting from parasite-induced reduction in host reproduction and survival) as well as trait-mediated indirect effects (resulting from parasite-induced changes in host phenotype, behaviour or life history). These effects are not mutually exclusive but often interact. The importance of these indirect interactions for invasion success, and the extent to which these effects ramify throughout communities and influence ecosystems undergoing biological invasion provide the focus of our review. Examples from the animal and plant literature illustrate the importance of parasites in mediating both competitive and consumer-resource interactions between native and invasive species. Parasites are involved in indirect interactions at all trophic levels. Furthermore, the indirect effects of parasitic infection are important at a range of biological scales from within a host to the whole ecosystem in determining invasion success and impact. To understand the importance of parasitic infection in invasion success and in the outcomes for invaded communities requires an interdisciplinary approach by ecologists and parasitologists, across animal and plant systems. Future research should develop a framework integrating community ecology, evolution and immunology to better understand and manage the spread of invasive species and their diseases.
1. Introduced species disrupt native communities and biodiversity worldwide. Parasitic infections (and at times, their absence) are thought to be a key component in the success and impact of biological invasions by plants and animals. They can facilitate or limit invasions, and positively or negatively impact native species. 2. Parasites have not only direct effects on their hosts, but also indirect effects on the species with which their hosts interact. Indirect effects include density-mediated effects (resulting from parasite-induced reduction in host reproduction and survival) as well as trait-mediated indirect effects (resulting from parasite-induced changes in host phenotype, behavior or life history). These effects are not mutually exclusive but often interact. 3. The importance of these indirect interactions for invasion success, and the extent to which these effects ramify throughout communities and influence ecosystems undergoing biological invasion provide the focus of our review. Examples from the animal and plant literature illustrate the importance of parasites in mediating both competitive and consumer–resource interactions between native and invasive species. 4. Parasites are involved in indirect interactions at all trophic levels. Furthermore, the indirect effects of parasitic infection are important at a range of biological scales from within a host to the whole ecosystem in determining invasion success and impact. 5. To understand the importance of parasitic infection in invasion success and in the outcomes for invaded communities requires an interdisciplinary approach by ecologists and parasitologists, across animal and plant systems. Future research should develop a framework integrating community ecology, evolution and immunology to better understand and manage the spread of invasive species and their diseases.
Invasive habitat-forming ecosystem engineers modify the abiotic environment and thus represent a major perturbation to many ecosystems. Because native species often persist in these invaded habitats but have no shared history with the ecosystem engineer, the engineer may impose novel selective pressure on native species. In this study, we used a phenotypic selection framework to determine whether an invasive habitat-forming ecosystem engineer (the seaweed Caulerpa taxifolia) selects for different phenotypes of a common co-occurring native species (the bivalve Anadara trapezia). Compared to unvegetated habitat, Caulerpa habitat has lower water flow, lower dissolved oxygen, and sediments are more silty and anoxic. We determined the performance consequences of variation in key functional traits that may be affected by these abiotic changes (shell morphology, gill mass, and palp mass) for Anadara transplanted into Caulerpa and unvegetated habitat. Both linear and nonlinear performance gradients in Anadara differed between habitats, and these gradients were stronger in Caulerpa compared to unvegetated sediment. Moreover, in Caulerpa alternate phenotypes performed well, and these phenotypes were different from the dominant phenotype in unvegetated sediment. By demonstrating that phenotype-performance gradients differ between habitats, we have highlighted a role for Caulerpa as an agent of selection on native species.
Co-occurring foundation species can determine biological community structure via facilitation cascades. We examined the density dependencies of facilitation cascades, including how the density of a basal foundation species influences the density of secondary foundation species, and how the density of secondary foundation species influences community structure. The system in which we assessed density dependencies was a temperate mangrove forest in which pneumatophores trap the fucoid alga Hormosira banksii and provide substrate for the oyster, Saccostrea glomerata. The alga and oyster in turn determine benthic community structure. In the field, algal biomass was positively correlated with pneumatophore density. Oysters, by contrast, were highly over-dispersed and correlated with the presence/absence of pneumatophores. Epifaunal abundance and species richness were positively correlated with algal and oyster abundance, but their effects were independent. The positive effect of pneumatophore density on epifauna was primarily an indirect effect of trapping more algae. Pneumatophores did not directly influence invertebrate communities. Experiments revealed that, at very low pneumatophore densities, algal retention was insufficient to facilitate epifauna above that found on pneumatophores alone. At higher densities, however, increasing the density of pneumatophores increased algal retention, and the density and diversity of associated invertebrates. Shading by the mangrove canopy reduced algal biomass but did not modify the density-dependent nature of the cascade. Our results extend facilitation theory by showing that the density of both basal and secondary foundation species can be critical in triggering facilitation cascades. Our study also reveals that, where foundation species co-occur, multiple, independent cascades may arise from a single basal facilitator. These findings enhance our understanding of the role of density-dependent facilitation cascades in community assembly.
Invasive habitat-forming species cause large changes to the abiotic environment, which may lead to lethal and sublethal effects on native fauna. In this study, we tested whether morphological anti-predator traits of an infaunal bivalve, Anadara trapezia, differed between areas invaded by the habitat-forming seaweed Caulerpa taxifolia and uninvaded habitats in estuaries in New South Wales, Australia. Caulerpa changes the abiotic environment in ways that may affect traits of native species. In particular, there is lower water flow, lower dissolved oxygen in the water and sediments are more silty and anoxic than in unvegetated habitat. To test our hypotheses, we collected Anadara from Caulerpa and uninvaded habitats and measured shell thickness, shell strength and resistance to opening of valves. We found that all three traits were reduced in Anadara from Caulerpa habitat compared with Anadara from uninvaded habitats. These findings are consistent with the idea that trait modifications in native fauna in response to invasive habitat-forming species can potentially increase susceptibility to predation.
Aim To use a comparative approach to understand parasite demographic patterns in native versus introduced populations, evaluating the potential roles of host invasion history and parasite life history. Location North American east and west coasts with a focus on San Francisco Bay (SFB). Methods Species richness and prevalence of trematode parasites were examined in the native and introduced ranges of two gastropod host species, Ilyanassa obsoleta and Littorina saxatilis. We divided the native range into the putative source area for introduction and areas to the north and south; we also sampled the overlapping introduced range in SFB. We dissected 14,781 snails from 103 populations and recorded the prevalence and identity of trematode parasites. We compared trematode species richness and prevalence across the hosts’ introduced and native ranges, and evaluated the influence of host availability on observed patterns. Results Relative to the native range, both I. obsoleta and L. saxatilis have escaped (lost) parasites in SFB, and L. saxatilis demonstrated a greater reduction of trematode diversity and infection prevalence than I. obsoleta. This was not due to sampling inequalities between the hosts. Instead, rarefaction curves suggested complete capture of trematode species in native source and SFB subregions, except for L. saxatilis in SFB, where infection was extremely rare. For I. obsoleta, infection prevalence of trematodes using fish definitive hosts was significantly lower in SFB compared to the native range, unlike those using bird hosts. Host availability partly explained the presence of introduced trematodes in SFB. Main conclusions Differential losses of parasite richness and prevalence for the two gastropod host species in their introduced range is probably the result of several mechanistic factors: time since introduction, propagule pressure, vector of introduction, and host availability. Moreover, the recent occurrence of L. saxatilis’ invasion and its active introduction vector suggest that its parasite diversity and distribution will probably increase over time. Our study suggests that host invasion history and parasite life history play key roles in the extent and diversity of trematodes transferred to introduced populations. Our results also provide vital information for understanding community-level influences of parasite introductions, as well as for disease ecology in general.
Conservation of biodiversity is a major aim of marine reserves; however the effects of reserves on non-native species, a major threat to biodiversity globally, is not widely known. Marine reserves could resist non-native species due to enhanced native diversity and biomass that heightens biotic resistance. Or non-native species could be enhanced by reserves by at least three mechanisms, including protection from harvesting, increased fishing pressure outside reserves facilitating invasions at a regional scale and increasing the exposure of reserves to more potential invaders, and increased propagule pressure from human visitation. We exhaustively searched the literature and found 13 cases that contained quantitative data on non-native species inside and outside marine reserves. In no cases did reserves resist non-native species. Of the seven cases where reserves were established prior to the arrival of the non-native species, five had no effect on the non-native species and two enhanced non-native species. Of the six cases where reserves were established in areas that had pre-existing non-native species, two had no effect on the non-native species and four enhanced the non-native species. These results suggest that while non-native species do equally well or better within marine reserves, too few data are currently available to draw broad, general conclusions regarding the effects of marine reserves on non-native species. Management plans for marine reserves rarely include guidelines for preventing or managing non-native species. If the trends we have detected here are supported by future studies, non-native species should be a priority for management of marine reserves.
Summary: A great diversity of organisms modify the physical structure of estuarine and coastal environments. These physical ecosystem engineers – particularly, dune and marsh plants, mangroves, seagrasses, kelps, reef-forming corals and bivalves, burrowing crustaceans and infauna – often have substantive functional impacts over large areas and across distinct geographic regions. Here we use a general framework for physical ecosystem engineering to illustrate how these organisms can exert control on sedimentary processes, coastal protection and habitat availability to other organisms. We then discuss the management implications of coastal and estuarine engineering, ending with a brief prospectus on research and management challenges.
New marine invasions have been recorded in increasing numbers along the world's coasts due in part to the warming of the oceans and the ability of many invasive marine species to tolerate a broader thermal range than native species. Several marine invertebrate species have invaded the U.S. southern and mid-Atlantic coast from the Caribbean and this poleward range expansion has been termed 'Caribbean Creep'. While models have predicted the continued decline of global biodiversity over the next 100 years due to global climate change, few studies have examined the episodic impacts of prolonged cold events that could impact species range expansions. A pronounced cold spell occurred in January 2010 in the U.S. southern and mid-Atlantic coast and resulted in the mortality of several terrestrial and marine species. To experimentally test whether cold-water temperatures may have caused the disappearance of one species of the 'Caribbean Creep' we exposed the non-native crab Petrolisthes armatus to different thermal treatments that mimicked abnormal and severe winter temperatures. Our findings indicate that Petrolisthes armatus cannot tolerate prolonged and extreme cold temperatures (4-6 °C) and suggest that aperiodic cold winters may be a critical 'reset' mechanism that will limit the range expansion of other 'Caribbean Creep' species. We suggest that temperature 'aberrations' such as 'cold snaps' are an important and overlooked part of climate change. These climate fluctuations should be accounted for in future studies and models, particularly with reference to introduced subtropical and tropical species and predictions of both rates of invasion and rates of unidirectional geographic expansion.
In a single well-mixed population, equally abundant neutral alleles are equally likely to persist. However, in spatially complex populations structured by an asymmetric dispersal mechanism, such as a coastal population where larvae are predominantly moved downstream by currents, the eventual frequency of neutral haplotypes will depend on their initial spatial location. In our study of the progression of two spatially separate, genetically distinct introductions of the European green crab (Carcinus maenas) along the coast of eastern North America, we captured this process in action. We documented the shift of the genetic cline in this species over 8 y, and here we detail how the upstream haplotypes are beginning to dominate the system. This quantification of an evolving genetic boundary in a coastal system demonstrates that novel genetic alleles or haplotypes that arise or are introduced into upstream retention zones (regions whose export of larvae is not balanced by import from elsewhere) will increase in frequency in the entire system. This phenomenon should be widespread when there is asymmetrical dispersal, in the oceans or on land, suggesting that the upstream edge of a species' range can influence genetic diversity throughout its distribution. Efforts to protect the upstream edge of an asymmetrically dispersing species' range are vital to conserving genetic diversity in the species.
While well-recognized as an important kind of ecological interaction, physical ecosystem engineering by organisms is diverse with varied consequences, presenting challenges for developing and using general understanding. There is also still some uncertainty as to what it is, and some skepticism that the diversity of engineering and its effects is amenable to conceptual integration and general understanding. What then, are the key cause/effect relationships and what underlies them? Here we develop, enrich and extend our extant understanding of physical ecosystem engineering into an integrated framework that exposes the essential cause/effect relationships, their underpinnings, and the interconnections that need to be understood to explain or predict engineering effects. The framework has four cause/effect relationships linking four components: 1. An engineer causes structural change; 2. Structural change causes abiotic change; 3. Structural and abiotic change cause biotic change; 4. Structural, abiotic and biotic change can feedback to the engineer. The first two relationships describe an ecosystem engineering process and abiotic dynamics, while the second two describe biotic consequence for other species and the engineer. The four relationships can be parameterized and linked using time-indexed equations that describe engineered system dynamics. After describing the relationships we discuss the utility of the framework; how it might be enriched; and briefly how it can be used to identify intersections of ecosystem engineering with fields outside ecology.
Aim To determine timing, source and vector for the recent introduction of the European green crab, Carcinus maenas (Linnaeus, 1758), to Newfoundland using multiple lines of evidence. Location Founding populations in Placentia Bay, Newfoundland, Canada and potential source populations in the north-west Atlantic (NWA) and Europe. Methods We analysed mitochondrial and microsatellite genetic data from European and NWA populations sampled during 1999–2002 to determine probable source locations and vectors for the Placentia Bay introduction discovered in 2007. We also analysed Placentia Bay demographic data and shipping records to look for congruent patterns with genetic analyses. Results Demographic data and surveys suggested that C. maenas populations are established and were in Placentia Bay for several years (c. 2002) prior to discovery. Genetic data corroboratively suggested central/western Scotian Shelf populations (e.g., Halifax) as the likely source area for the anthropogenic introduction. These Scotian Shelf populations were within an admixture zone made up of genotypes from both the earlier (early 1800s) and later (late 1900s) introductions of the crab to the NWA from Europe. Placentia Bay also exhibited this mixed ancestry. Probable introduction vectors included vessel traffic and shipping, especially vessels carrying ballast water. Main conclusions Carcinus maenas overcame considerable natural barriers (i.e., coastal and ocean currents) via anthropogenic transport to become established and abundant in Newfoundland. Our study thus demonstrates how non-native populations can be important secondary sources of introduction especially when aided by human transport. Inference of source populations was possible owing to the existence of an admixture zone in central/western Nova Scotia made up of southern and northern genotypes corresponding with the crab’s two historical introductions. Coastal vessel traffic was found to be a likely vector for the crab’s spread to Newfoundland. Our study demonstrates that there is considerable risk for continued introduction or reintroduction of C. maenas throughout the NWA.
Digenean trematode parasites require multiple host species to complete their life cycles, and their abundance can often be strongly correlated with the abundance of their host species. Species richness and abundance of parasites in easily sampled host species may yield an accurate estimate of the species richness and abundance of other hosts in a parasite's life cycle that are difficult to survey directly. Accordingly, we investigated whether prevalence and mean abundance of trematodes could be used to estimate the abundance of one of their host species, diamondback terrapins (Malaclemys terrapin), which are difficult to sample and are designated as near threatened (by the International Union for Conservation of Nature [IUCN Red List]) along some U.S. coasts. As an adult the trematode Pleurogonius malaclemys is specific to terrapins. Its larval stages live first inside mud snails (Ilyanassa obsoleta) and are subsequently shed into the environment where they form external metacercarial cysts on hard surfaces such as snail opercula. The life cycle of P. malaclemys is completed when terrapins ingest these cysts. At 12 sites along the coast of Georgia (U.S.A.), we determined the prevalence of internal P. malaclemys larvae in mud snails (proportion of infected snails in a population) and the prevalence and mean abundance of external trematode cysts. We examined whether these data were correlated with terrapin abundance, which we estimated with mark-recapture methods. The abundance of external cysts and salinity explained ≥59% of the variability in terrapin abundance. We suggest that dependent linkages between the life stages of multihost parasites make them reliable predictors of host species' abundance, including hosts with abundances that are challenging to quantify directly.
Background/Question/Methods Parasites are important and abundant members of communities; thus it is critical to understand their influences within and among bioregions. Specifically, understanding how parasite diversity patterns are affected by anthropogenic dispersal of their hosts and the effect differing vectors may have on those patterns is largely unexplored. We therefore assembled a comparative study of trematode parasite diversity in two snail hosts (Ilyanassa obsoleta and Littorina saxatilis) introduced to the west coast of North America from native east coast populations. Although these snail species have overlapping geographic ranges on both North American coasts, they have highly differentiated invasion histories: I. obsoleta was introduced to the west coast via intentional (failed) oyster transplantation from the east coast in the early 1900s, while L. saxatilis was introduced via the live seafood/baitworm trade in the 1990s. Results/Conclusions Results of our analyses showed that both snail species had significantly lower total and average site-level trematode richness and prevalence in the introduced versus native regions. However, L. saxatilis escaped about 1.8 times more parasites than I. obsoleta, which we attributed to several potential, non-mutually exclusive mechanisms: time since introduction, introduction vectors, propagule pressure, parasite prevalence in source populations, and available hosts. In both species, but especially I. obsoleta, we found close links between native source populations and introduced populations, especially for non-native San Francisco Bay populations, which probably represent one of the oldest non-native founding areas. Host availability and parasite-specific life cycle strategies were also found to have important influences on resulting parasite diversity patterns in introduced populations, and definitive host availability was found to be especially important. On the whole, understanding our hosts’ particular ecological and invasion histories was integral for comprehending the parasite biogeographic patterns we observed across native and introduced ranges. We also demonstrated that time since introduction, vector pathways, source information, host availability, and propagule pressure all played strong roles in determining parasitism in introduced locations. Because both snail species, and particularly L. saxatilis, have escaped many parasite species in their introduced region, they may possess an advantage in competitive interactions and overall success on the west coast just by the fact that their health and reproductive fitness are less hampered by these castrating parasites. Further research over time can help reveal community level (including native biota) impacts of these introduced parasite systems on the US west coast.
Habitat-modifying invasive species can influence rates of predation on native prey either directly by providing protective structure or indirectly by modifying traits of prey species responding to the habitat. The alga Caulerpa taxifolia is one of the most successful invasive species of shallow-water marine systems globally, often provisioning habitat in areas previously lacking in vegetated structure. We experimentally evaluated the direct effect of Caulerpa to provide refuge for the native clam Anadara trapezia and how this balances with its influence on two trait-mediated indirect interactions that may increase Anadara's susceptibility to predators. Specifically, Caulerpa's alteration of physical and chemical properties of the surrounding water and sediment deteriorate Anadara's condition and predator resistance properties and also cause Anadara, though normally buried, to project from beneath the sediment, exposing it to predators. Our results show that Anadara are somewhat (but not consistently) protected from predators by living among Caulerpa. Shallow burial depth did not counteract this protective effect. However at times of year when predator activity diminishes and conducive environmental conditions develop, negative effects of Caulerpa habitat such as hypoxia and lowered flow may dominate. Under such situations, poor clam condition accentuates Anadara's susceptibility to mortality. Ultimately, a slight and inconsistent positive effect of Caulerpa to protect Anadara from predators is exceeded by the strong negative effect of Caulerpa on clam mortality, which is heightened by clams' weakened condition produced by chronic exposure to Caulerpa. Our results show that invasive habitat-modifying species can affect mortality of native species not simply through obvious positive direct effects of their protective structure, but indirectly through contrasting negative modification of the traits of prey species responding to the habitat.
Utilizing marine protected areas (MPAs) to isolate the ecological effects of human influence can help us understand our effect on systems and foster ecosystem-based approaches to management. Specifically, examining invertebrate prey community dynamics inside and outside an MPA may provide a measure of how altering human influence (i.e., certain fishing pressures) affects ecosystem interactions. We measured trophic interactions inside and outside a deep-water temperate MPA over 2years. Predation rates on tethered, preferred groundfish prey (crabs) were initially identical inside and outside the MPA, but decreased outside the MPA after the commercial groundfish fishing season commenced. Predation trials using a ubiquitous prey species (brittle stars) and a less preferred prey species (urchins) served as controls, showing no MPA effect. Our experiments quantify differential predatory activity resulting from differences in human activity driven by an MPA, demonstrating important effects of fishing and regulations on the strength of trophic interactions.
Habitat-forming invasive species cause large, novel changes to the abiotic environment. These changes may elicit important behavioural responses in native fauna, yet little is known about mechanisms driving this behaviour and how such trait-mediated responses influence the fitness of native species. Low dissolved oxygen is a key abiotic change created by the habitat-forming invasive seaweed, Caulerpa taxifolia, which influences an important behavioural response (burrowing depth) in the native infaunal bivalve Anadara trapezia. In Caulerpa-colonised areas, Anadara often emerged completely from the sediment, and we experimentally demonstrate that water column hypoxia beneath the Caulerpa canopy is the mechanism instigating this "pop-up" behaviour. Importantly, pop-up in Caulerpa allowed similar survivorship to that in unvegetated sediment; however, when we prevented Anadara from popping-up, they suffered >50% mortality in just 1 month. Our findings not only highlight the substantial environmental alteration by Caulerpa, but also an important role for the behaviour of native species in mitigating the effects of habitat-forming invasive species.
The application of ecosystem-based management (EBM) in marine environments has been widely supported by scientists, managers, and policy makers, yet implementation of this approach is difficult for various scientific, political, and social reasons. A key, but often overlooked, challenge is how to account for multiple and varied human activities and ecosystem services and incorporate ecosystem-level thinking into EBM planning. We developed methods to systematically identify the natural and human components of a specific ecosystem and to qualitatively evaluate the strength of their interactions. Using the Gulf of Maine marine ecosystem as a case study, we show how these methods may be applied, in order to identify and prioritize the most important components to be included in an EBM plan -particularly the human activities that are the strongest drivers of ecosystem change and the ecosystem services most threatened by cumulative and indirect effects of these activities.
Although introduced species often interact with one another in their novel communities, the role of parasites in these interactions remains less clear. We examined parasite richness and prevalence in 2 shorecrab species with different invasion histories and residency times in an introduced region where their distributions overlap broadly. On the northeastern coast of the USA, the Asian shorecrab Hemigrapsus sanguineus was discovered 20 yr ago, while the European green crab Carcinus maenas has been established for over 200 yr. We used literature and field surveys to evaluate parasitism in both crabs in their native and introduced ranges. We found only 1 parasite species infecting H. sanguineus on the US East Coast compared to 6 species in its native range, while C. maenas was host to 3 parasite species on the East Coast compared to 10 in its native range. The prevalence of parasite infection was also lower for both crabs in the introduced range compared to their native ranges; however, the difference was almost twice as much for H. sanguineus as for C.maenas. There are several explanations that could contribute to C. maenas' greater parasite diversity than that of H. sanguineus on the US East Coast, including differences in susceptibility, time since introduction, manner of introduction (vector), distance from native range, taxonomic isolation, and the potential for parasite identification bias. Our study underscores not just that non-native species lose parasites upon introduction, but that they may do so differentially, with ramifications for their direct interactions and with potential community-level influences.
Behavioural interactions between ecosystem engineers may strongly influence community structure. We tested whether an invasive ecosystem engineer, the alga Caulerpa taxifolia, indirectly facilitated community diversity by modifying the behaviour of a native ecosystem engineer, the clam Anadara trapezia, in southeastern Australia. In this study, clams in Caulerpa-invaded sediments partially unburied themselves, extending >30% of their shell surface above the sediment, providing rare, hard substrata for colonization. Consequently, clams in Caulerpa had significantly higher diversity and abundance of epibiota compared with clams in unvegetated sediments. To isolate the role of clam burial depth from direct habitat influences or differential predation by habitat, we manipulated clam burial depth, predator exposure and habitat (Caulerpa or unvegetated) in an orthogonal experiment. Burial depth overwhelmingly influenced epibiont species richness and abundance, resulting in a behaviourally mediated facilitation cascade. That Caulerpa controls epibiont communities by altering Anadara burial depths illustrates that even subtle behavioural responses of one ecosystem engineer to another can drive extensive community-wide facilitation.
Aquatic prey encounter an array of threat cues from multiple predators and killed conspecifics, yet the vast majority of induced defenses are investigated using cues from single predator species. In most cases, it is unclear if odors from multiple predators will disrupt defenses observed in single-predator induction experiments. We experimentally compared the inducible defenses of the common marine mussel Mytilus edulis to waterborne odor from pairwise combinations of three predators representing two attack strategies. Predators included the sea star, Asterias vulgaris (=Asteriasrubens), and the crabs Carcinus maenas and Cancer irroratus. The mussels increased adductor muscle mass in response to cues from unfed Asterias (a predatory seastar that pulls mussel shells open) and increased shell thickness in response to unfed Carcinus, a predatory crab that crushes or peels shells. However, the mussels did not express either predator specific response when exposed to the combined cues of Asterias and Carcinus, and mussels did not increase shell thickness when exposed to cues from Cancer alone or any pairwise combination of the three predators. Shell closure or ‘clamming up’ did not occur in response to any predator combination. These results suggest that predator-specific responses to the Asterias and Carcinus are poorly integrated and cannot be expressed simultaneously. Simultaneous cues from multiple predators affect the integration of predator specific defenses and predator odors from functionally similar predators do not necessarily initiate similar defenses. Ultimately, the degree that prey can integrate potentially disparate defenses in a multiple predator environment may have ecological ramifications and represent a seldom explored facet of the evolution of inducible defenses.
Early invasions of the North American shore occurred mainly via deposition of ballast rock, which effectively transported pieces of the intertidal zone across the Atlantic. From 1773-1861, >880 European ships entered Pictou Harbor, Nova Scotia, as a result of emigration and trade from Europe. The rockweed Fucus serratus (1868) and the snail Littorina littorea ( approximately 1840) were found in Pictou during this same period. With shipping records (a proxy for propagule pressure) to guide sampling, we used F. serratus as a model to examine the introductions because of its relatively low genetic diversity and dispersal capability. Microsatellite markers and assignment tests revealed 2 introductions of the rockweed into Nova Scotia: 1 from Galway (Ireland) to Pictou and the other from Greenock (Scotland) to western Cape Breton Island. To examine whether a high-diversity, high-dispersing species might have similar pathways of introduction, we analyzed L. littorea, using cytochrome b haplotypes. Eight of the 9 Pictou haplotypes were found in snails collected from Ireland and Scotland. Our results contribute to a broader understanding of marine communities, because these 2 conspicuous species are likely to be the tip of an "invasion iceberg" to the NW Atlantic from Great Britain and Ireland in the 19th Century.
Assessing the implications of species invasion for native communities requires determining whether effects of invaders are novel, or are redundant with effects of species that are already present. Using a pair of field experiments conducted over two successive years, we examined factors that influence community impacts of a recent predatory crab invader (Hemigrapsus sanguineus) and a previously established invasive crab (Carcinus maenas) on New England coasts. We demonstrate that effects of these species differ temporally with changes in the ambient prey community, and are influenced by density differences between the two species and by different strengths and types of indirect effects that each elicits. Our study highlights the importance of including bottom-up processes (i.e., prey recruitment) when examining the redundancy of consumers.
Growing evidence indicates parasite inclusion in food-web analyses is a logical default. Comparisons of food webs including and excluding host-parasite interactions demonstrate the influence of parasites on community dynamics. Although including parasites is undoubtedly informative, the necessary level of detail exists for only a handful of systems. In a recent Ecology Letters article, Lafferty et al. pose many good questions to catalyze discussions for determining when and how parasites should be incorporated into food-web analyses.
Competition is a negative interaction between two or more species that utilize the same shared, limiting resource (Connell 1983). Although competition can have large local, immediate effects, (e.g. on demography, resource use, etc.), competition in many marine systems is often assumed to have minimal effect on population persistence, primarily due to characteristics of the dominant life histories of marine organisms. Notably, a large proportion of marine species have pelagic larvae and thus often reside in open populations where the supply of progeny is decoupled from progeny production. Thus, although competition can still affect adults, future generations are supplied from distant populations that can “rescue” populations of inferior competitors from being excluded. Even in relatively closed marine habitats, e.g., bays or estuaries, a constant influx of larvae in ballast water (Verling et al. 2005) may make many populations effectively open, subsidizing populations of species that would otherwise be excluded. The open nature of larval production and delivery applies to food resources as well. The preponderance of filter feeders, which feed on a food resource that is typically replenished frequently (e.g., with tidal cycle) and whose supply is often decoupled from consumptive pressure by resident organisms, may reduce the occurrence of resource competition.
Existing estimates of the downstream invasion speed of newly introduced species or novel genotypes with planktonic larvae have usually found that they invade much less rapidly downstream than would be expected from the mean alongshore currents in their habitat. For example, a new, genetically-distinct population of Carcinus maenas was introduced at the northern-edge of its range in Cape Breton, Nova Scotia (Roman 2006). Recently, we have found that this newly introduced genotype is being transported south- westward along the coast by the prevailing currents, displacing established populations of C. maenas. However, the rate of southward spread of the northern genotype is much less than what we would expect from the mean currents along the Scotian Shelf and Gulf of Maine. We examine four reasons for errors in the naive estimates of the rate of spread of an introduced species or genotype from mean currents. 1) Cross-shelf shear in the alongshore currents can interact with cross-shelf dispersion of larvae to bias larval settlement towards larvae which have spent more time in the weaker nearshore currents. 2) Weakly retentive embayments and other coastal features, even if unable to retain larvae for more than a small fraction of their planktonic duration, will tend to reduce the alongshelf transports of those larvae and increase the likelihood that they remain close enough to the coast to successfully recruit. This will reduce the mean alongshore transport of the larvae that recruit. 3) Alongshore gradients in the population density of competing species/genotypes will, if the population density increases in the direction of the mean currents, tend to retard the downstream spread of an introduced species/genotype. 4) Greater relative fitness or competitiveness in the downstream genotype/species will retard the spread of the upstream genotype/species. Examples of and evidence for and against these possible explanations will be provide for C. maenas in the Gulf of Maine