April M. H. Blakeslee

Parasites alter community structure

Parasites often play an important role in modifying the physiology and behavior of their hosts and may, consequently, mediate the influence hosts have on other components of an ecological community. Along the northern Atlantic coast of North America, the dominant herbivorous snail Littorina littorea structures rocky intertidal communities through strong grazing pressure and is frequently parasitized by the digenean trematode Cryptocotyle lingua. We hypothesized that the effects of parasitism on host physiology would induce behavioral changes in L. littorea, which in turn would modulate L. littoreas influence on intertidal community composition. Specifically, we hypothesized that C. lingua infection would alter the grazing rate of L. littorea and, consequently, macroalgal communities would develop differently in the presence of infected versus uninfected snails. Our results show that uninfected snails consumed 40% more ephemeral macroalgal biomass than infected snails in the laboratory, probably because the digestive system of infected snails is compromised by C. lingua infection. In the field, this weaker grazing by infected snails resulted in significantly greater expansion of ephemeral macroalgal cover relative to grazing by uninfected snails. By decreasing the per-capita grazing rate of the dominant herbivore, C. lingua indirectly affects the composition of the macroalgal community and may in turn affect other species that depend on macroalgae for resources or habitat structure. In light of the abundance of parasites across systems, we suggest that, through trait-mediated indirect effects, parasites may be a common determinant of structure in ecological communities.

Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range

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.

Historical invasions of the intertidal zone of Atlantic North America associated with distinctive patterns of trade and emigration

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 (≈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.

A practical approach to implementation of ecosystem-based management: a case study using the Gulf of Maine marine ecosystem

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.

Marine invasions and parasite escape: updates and new perspectives.

Marine invasions have risen over time with enhanced globalization, and so has the introduction of non-native hosts and their parasites. An important and well-supported paradigm of invasion biology is the significant loss of parasites that hosts enjoy in introduced regions compared to native regions (i.e. parasite escape), yet less is known about the factors that influence parasite escape in marine systems. Here, we compile an up-to-date review of marine parasite invasions and test several hypotheses related to host invasion pathway that we suspected could influence parasite escape across the 31 host-parasite systems included in our investigation. In general, we continued to show significant support for parasite escape; however, escape varied among parasite taxa, with most taxa demonstrating moderate levels of escape and a few showing complete or no escape. Moreover, we revealed several important factors related to host taxa, geography, time, and vector of introduction that influenced parasite escape, and in some cases demonstrated significant interactions, revealing the complexity of the invasion pathway in filtering parasites from native to introduced regions. In some (but not all) cases, there was also evidence of invasive host advantages due to parasite escape, but more evidence is required to demonstrate clear support for the enemy release hypothesis. In general, our study revealed the need for further research across systems, especially in understudied regions of the world.

Establishment failure in biological invasions: a case history of Littorina littorea in California, USA.

Background The early stages of biological invasions are rarely observed, but can provide significant insight into the invasion process as well as the influence vectors have on invasion success or failure. Methodology/Principal Findings We characterized three newly discovered populations of an introduced gastropod, Littorina littorea (Linné, 1758), in California, USA, comparing them to potential source populations in native Europe and the North American East Coast, where the snail is also introduced. Demographic surveys were used to assess spatial distribution and sizes of the snail in San Francisco and Anaheim Bays, California. Mitochondrial DNA was sequenced and compared among these nascent populations, and various populations from the North American East Coast and Europe, to characterize the California populations and ascertain their likely source. Demographic and genetic data were considered together to deduce likely vectors for the California populations. We found that the three large California L. littorea populations contained only adult snails and had unexpectedly high genetic diversity rather than showing an extreme bottleneck as typically expected in recent introductions. Haplotype diversity in Californian populations was significantly reduced compared to European populations, but not compared to East Coast populations. Genetic analyses clearly suggested the East Coast as the source region for the California introductions. Conclusions and Significance The California L. littorea populations were at an early, non-established phase of invasion with no evidence of recruitment. The live seafood trade is the most likely invasion vector for these populations, as it preferentially transports large numbers of adult L. littorea, matching the demographic structure of the introduced California L. littorea populations. Our results highlight continued operation of live seafood trade vectors and the influence of vectors on the demographic and genetic structure of the resulting populations, especially early stages of the invasion process.

Are genes faster than crabs? Mitochondrial introgression exceeds larval dispersal during population expansion of the invasive crab Carcinus maenas

Biological invasions offer unique opportunities to investigate evolutionary dynamics at the peripheries of expanding populations. Here, we examine genetic patterns associated with admixture between two distinct invasive lineages of the European green crab, Carcinus maenas L., independently introduced to the northwest Atlantic. Previous investigations based on mitochondrial DNA sequences demonstrated that larval dispersal driven by advective currents could explain observed southward displacement of an admixture zone between the two invasions. Comparison of published mitochondrial results with new nuclear data from nine microsatellite loci, however, reveals striking discordance in their introgression patterns. Specifically, introgression of mitochondrial genomes relative to nuclear background suggests that demographic processes such as sex-biased reproductive dynamics and population size imbalances—and not solely larval dispersal—play an important role in driving the evolution of the genetic cline. In particular, the unpredicted introgression of mitochondrial alleles against the direction of mean larval dispersal in the region is consistent with recent models invoking similar demographic processes to explain movements of genes into invading populations. These observations have important implications for understanding historical shifts in C. maenas range limits, and more generally for inferences of larval dispersal based on genetic data.

Aquatic Introductions and Genetic Founder Effects: How do Parasites Compare to Hosts?

Aquatic parasites have intrigued researchers over the past several decades due to their often unique and complex life cycles, which can require multiple hosts to progress from larval to adult reproductive stages (Shoop, 1998). Parasites are also integral in community and ecosystem functioning and have the potential to impact community structure through direct (e.g., affecting host growth, reproduction, and survivorship) or indirect (e.g., influencing host predation and/or competition) means (Lafferty & Morris, 1996; Torchin et al., 2002; Blakeslee et al., 2009). Recently, parasites have become recognized not only as interesting biological/model species, but also as useful indicator species and biological tools for resolving ecological questions. For example, parasites can be indicators of ecosystem health (Huspeni & Lafferty, 2004) or even utilized to more accurately resolve questions surrounding cryptic species invasions (Blakeslee et al., 2008) or biogeographic movements of hosts (Criscione et al., 2006). Even with these recent developments in aquatic parasite research, and although parasites are known to represent a fundamental component of aquatic systems worldwide (Kuris et al., 2008), genetic diversity patterns of aquatic parasites are much less understood than they are for free-living species. This is especially true for hosts/parasites with broad habitat ranges across bioregions and those introduced to new locations through anthropogenic transport. We believe these knowledge gaps exist for two major reasons: 1) parasites are less visible than free-living species and 2) parasites are logistically more challenging to study (i.e., often requiring destructive sampling, knowledge of parasite taxonomy, and parasite specific genetic markers). Even still, parasites have numerous interesting and important ecological, evolutionary, and conservation implications, including those related to their population genetics in introduced versus native regions. Aquatic parasites thereby represent an important, but overlooked, ecological group. In addition, aquatic invasions are on the rise in recent years (Carlton & Geller, 1993; Ruiz et al., 2000); yet the importance of parasites in those invasions (which have increased both in frequency and in distribution) is often less understood and/or tracked. Therefore, for this chapter, we focus on aquatic parasites, closely exploring how species introductions may affect genetic diversity patterns differently in parasites versus their free-living hosts.

Estuarine fouling communities are dominated by nonindigenous species in the presence of an invasive crab

Interactions between anthropogenic disturbances and introduced and native species can shift ecological communities, potentially leading to the successful establishment of additional invaders. Since its discovery in New Jersey in 1988, the Asian shore crab (Hemigrapsus sanguineus) has continued to expand its range, invading estuarine and coastal habitats in eastern North America. In estuarine environments, H.sanguineus occupies similar habitats to native, panopeid mud crabs. These crabs, and a variety of fouling organisms (both NIS and native), often inhabit man-made substrates (like piers and riprap) and anthropogenic debris. In a series of in situ experiments at a closed dock in southwestern Long Island (New York, USA), we documented the impacts of these native and introduced crabs on hard-substrate fouling communities. We found that while the presence of native mud crabs did not significantly influence the succession of fouling communities compared to caged and uncaged controls, the presence of introduced H. sanguineus reduced the biomass of native tunicates (particularly Molgulamanhattensis), relative to caged controls. Moreover, the presence of H. sanguineus favored fouling communities dominated by introduced tunicates (especially Botrylloides violaceous and Diplosoma listerianum). Altogether, our results suggest that H. sanguineus could help facilitate introduced fouling tunicates in the region, particularly in locations where additional solid substrates have created novel habitats.

Assessing the Effects of Trematode Infection on Invasive Green Crabs in Eastern North America

A common signature of marine invasions worldwide is a significant loss of parasites (= parasite escape) in non-native host populations, which may confer a release from some of the harmful effects of parasitism (e.g., castration, energy extraction, immune activation, behavioral manipulation) and possibly enhance the success of non-indigenous species. In eastern North America, the notorious invader Carcinus maenas (European green crab) has escaped more than two-thirds its native parasite load. However, one of its parasites, a trematode (Microphallus similis), can be highly prevalent in the non-native region; yet little is known about its potential impacts. We employed a series of laboratory experiments to determine whether and how M. similis infection intensity influences C. maenas, focusing on physiological assays of body mass index, energy storage, and immune activation, as well as behavioral analyses of foraging, shelter utilization, and conspicuousness. We found little evidence for enduring physiological or behavioral impacts four weeks after experimental infection, with the exception of mussel handling time which positively correlated with cyst intensity. However, we did find evidence for a short-term effect of M. similis infection during early stages of infection (soon after cercarial penetration) via a significant drop in circulating immune cells, and a significant increase in the crabs’ righting response time. Considering M. similis is the only common parasite infecting C. maenas in eastern North America, our results for minimal lasting effects of the trematode on the crab’s physiology and behavior may help explain the crab’s continued prominence as a strong predator and competitor in the region.