Amy E. Fowler

'Caribbean Creep' chills out: climate change and marine invasive species.

Background New marine invasions have been recorded in increasing numbers along the worlds 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. Methodology/Principal Findings 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. Conclusions/Significance 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.

Reconstructing past biological invasions: niche shifts in response to invasive predators and competitors.

Studying historic invasions can provide insight into the ongoing invasions that threaten global biodiversity. In this study, we reconsider the impacts of Littorina littorea and Carcinus maenas on the rocky intertidal community of the Gulf of Maine. Past research using invader-removal experiments demonstrated strong top-down effects of L. littorea on algal community structure; however, such removal experiments may overlook the long-term effects of niche shifts and local extinctions caused by invasive species. We considered how a niche-shift in the native littorine, Littorina saxatilis, may change the interpretation of L. littorea impacts. Using a factorial experiment crossing predator presence/absence with L. littorea presence/absence, we found that L. saxatilis is able to exert top-down control on ephemeral algae similar to that exerted by L.␣littorea and that both competition by L. littorea and predation by C. maenas have strong, negative impacts on L. saxatilis. We also found higher predation rates on protected shores and at lower tidal heights and preferential predation on L.␣saxatilis compared to L. littorea. While movement experiments demonstrate that behavioral response to tidal height is the proximate cause of L. saxatilis exclusion from the lower intertidal, our study suggests that the ultimate causes are the additive effects of competition from and predation by invasive species.

An introduced species meets the local fauna: predatory behavior of the crab Rhithropanopeus harrisii in the Northern Baltic Sea

Crabs are some of the most successful introduced species among marine organisms, and they can be an important structuring force in marine communities. Recently, the North American white-fingered mud crab, Rhithropanopeus harrisii, has invaded the Northern Baltic Sea. This is an area where no native crab species exist, and the addition of a novel functional species to the low species diversity of the Baltic Sea could have large community-level impacts i.e. modifying biotic interactions and/or altering ecosystem functioning. We examined the predatory behavior of introduced R. harrisii both in the laboratory and field focusing in shallow, hard bottom habitats dominated by the alga Fucus vesiculosus. In the laboratory environment, R. harrisii was an effective predator of littoral grazers, readily consuming both sessile fauna (Mytilus trossulus) and also mobile species such as isopods (Idotea balthica) and gammarid amphipods (Gammarus sp.). When studying the predation of different sized prey items, R. harrisii preyed upon small and medium sized prey of both mobile and sessile species. However, in the field experiment with the native faunal community associated with F. vesiculosus, R. harrisii negatively impacted only the abundance of the snail Theodoxus fluviatilis, possibly through indirect effects. Nevertheless, R. harrisii significantly decreased both the prey species richness and diversity but not the total number of potential prey individuals associated with F. vesiculosus. In conclusion, predatory behavior of this novel crab has the potential to impact the native macroinvertebrate littoral community, but the realized predation pressure in the field is lower than could be expected from laboratory experiments.

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.

Early stages of a New Zealand invasion by Charybdis japonica (A. Milne-Edwards, 1861) (Brachyura: Portunidae) from Asia: behavioral interactions with a native crab species

The Asian paddle crab, Charybdis japonica (A. Milne-Edwards, 1861), is a relatively recent invader (approx. 10 years) to northeastern New Zealand, and its large size and aggressive nature makes it a potentially formidable competitor with native species. The only endemic, similarly sized, New Zealand paddle crab, Ovalipes catharus (White and Doubleday, 1843), overlaps frequently with C. japonica in both habitat and diet. To understand their probable interactions in the field, we performed a series of experimental behavioral trials in a closed laboratory system to determine whether the crabs interact antagonistically over a shared prey resource (Perna canaliculus (Gmelin, 1791) – green-lipped mussel). In interspecific trials, C. japonica frequently displaced both sexes of O. catharus from the prey, while O. catharus usually failed to acquire prey from feeding C. japonica. In addition, male C. japonica dominated both male and female O. catharus in one-on-one competition for food, regardless of which crab possessed the food initially. Overall, male C. japonica behaved aggressively towards O. catharus and conspecifics of equal size when competing for a prey item; O. catharus showed low levels of aggression throughout all trials and increased time spent evading C. japonica as compared to C. japonica’s high levels of aggression. Our research highlights the importance of understanding how aggressive behavior may influence establishment success of invading species.

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.

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.

Pathology, Effects, and Transmission of Black Gill in Commercial Penaeid Shrimp from the South Atlantic Bight

ABSTRACT Severe outbreaks of black gill (BG), heavily melanized gills of crustaceans, have been reported in white (Litopenaeus setiferus) and brown shrimp (Farfantepenaeus aztecus) from coastal Georgia and South Carolina during late summer and fall since the mid-1990s. The cause of this condition is an apostome ciliate that elicits the innate immune response of the shrimp, resulting in the formation of melanized nodules in shrimp gill tissue. In the absence of a definitive identification, the causative ciliate is referred to as the shrimp black gill (sBG) ciliate. During outbreaks, necrosis of gill tissue was often seen in microscopic sections; in some cases, there appeared to be penetration of the ciliate into gill tissue. Shrimp with BG exhibited reduced physical endurance and escape responses compared with shrimp without symptomatic BG. Physical impairment due to BG may contribute to higher predation rates and increased vulnerability to environmental conditions. The infection transmission rate of the sBG ciliate appears to be atypically low for apostome ciliates, raising the question of how epidemic levels of BG reoccur annually. Asymptomatic shrimp placed in direct contact with carcasses (heads) from BG symptomatic shrimp exhibited a significant increase in the development of BG symptoms after 7 days (P = 0.028), but waterborne transmission was not detected. A preliminary survey of sympatric crustacean species, including syntopic species of grass shrimp (Palaemonetes spp.), indicated the possible presence of the sBG ciliate, suggesting that other crustacean species may serve as infection reservoirs. These studies support the conclusion that BG is negatively impacting the penaeid shrimp fishery and highlight the challenges that remain in understanding and managing the ongoing sBG epidemic in the southeastern United States.

Spatial and Temporal Associations Between Native Crabs and the Invading Green Porcelain Crab, Petrolisthes armatus, Throughout Its Northernmost Invaded Range

Increasing ocean temperatures have led to poleward range expansions of many marine organisms. The green porcelain crab, Petrolisthes armatus, was first reported on intertidal oyster reefs near Charleston, South Carolina in the mid-1990s, an expansion from its tropical to sub-tropical native range. In order to investigate the relative abundances of this introduced crab and a portion of the native crab community, resident crab assemblages were sampled on intertidal oyster reefs across four seasons from 2015 to 2016. Sampling occurred at five locations extending from Savannah, Georgia where P. armatus is now well-established, to Wilmington, North Carolina, where its inter-annual presence is intermittent. Petrolisthes armatus was the numerically dominant crab species at all locations except Wilmington, where the species was not collected in the winter. Differences between northern and southern sample locations in the taxonomic composition of crab assemblages were most pronounced in the summer (June–September) and fall (October–January), with dissimilarities largely attributed to high abundances of P. armatus at southern locations. Crab abundances of all species peaked in the summer and were lowest in the winter (February–March). Petrolisthes armatus was less abundant toward the northern range edge, whereas native crabs did not differ in abundance throughout the sampling range. Throughout the study area, adult P. armatus sex ratios shifted from unbiased or female-biased in the summer to male-biased in the fall. Adults were collected in the spring (April–June), indicating they had overwintered. While native crab densities (Panopeus herbstii, Eurypanopeus depressus) stayed relatively constant across locations, P. armatus densities varied greatly, suggesting that resources, such as shelter and food, are not limiting factors for the coexistence of these native and invading crabs.

Spacing and movement in the green porcelain crab Petrolisthes armatus: evidence for male competition and mate guarding

Abstract The green porcelain crab, Petrolisthes armatus, is a common invasive species on inter-tidal oyster reefs in the South Atlantic Bight whose behavior is largely unknown. We assessed the effects of the presence of opposite-sex conspecifics on adult crab spacing at a low density to infer potential mate acquisition behaviors. Adult crabs held in all-male, all-female, and mixed-sex treatments were observed twice daily over five days to determine nearest-neighbor (NN) distances and relative activity. Males in the mixed-sex treatment with the shortest NN distances (NN1) were most commonly (1) closest to females, and, when compared to NN1 males in the all-male treatment, were (2) closer to their NN and (3) had lower activity levels. Female movement did not differ between treatments. Percent ovigerous females at the end of trials were higher in the mixed-sex treatment, reflecting mating activity, which when observed, involved inter-molt females. Mate guarding, rather than pure-searching behavior, was the mating behavior most consistent with observed spacing and movement patterns.