Aquatic Invertebrate Ecology
How Introductions Shape Host-Parasite Relationships
Aquatic invertebrates can be parasitized by many different organisms that can impact population demography (i.e. growth, reproduction, and survivorship) and overall community structure (i.e. interacting with predation, competition, or both). Although parasites are often common in many systems, their roles are poorly understood, and they are easily overlooked; this is especially true for aquatic systems. Through several collaborations, our lab group has documented parasites in introduced aquatic invertebrates (Fowler, Loonam, and Blakeslee 2022), and examined how parasites and hosts differ in genetic founder effects in introduced populations (Blakeslee and Fowler 2012), the mechanisms and advantages of parasite escape in marine systems (Blakeslee, Fowler, and Keough 2013; Tepolt, Darling, Blakeslee, Fowler, et al. 2020; Tobias, Fowler, Blakeslee et al. 2021; Blakeslee, Pochtar, Fowler, et al. 2021), and the impacts of native parasites on the behavior and physiology of aquatic organisms (Blakeslee, Keough, Fowler, and Griffen 2015; Gooding, Kendrick, Brunson, Kingsley-Smith, Fowler, et al. 2020; Ro, Fowler, Wood, and Blakeslee 2022).
Parasites in non-native, freshwater Japanese mystery snailsRecent work has explored the demography and parasite fauna in introduced freshwater populations of mystery snails in Virginia and Maryland (Fowler et al. 2022a, 2022b). In many cases, introduced hosts experience parasite escape in their non-indigenous range by leaving behind some of their native parasite load during introduction. We showed that, at the majority of non-indigenous sites investigated, the Japanese mystery snail, Heterogen japonica, exhibited parasite escape. However, we found a moderate prevalence (up to 34%) of aspidogastrean trematode worms (the organism in the picture at the top) at two sites, and genetic data found at least two cryptic lineages of the worms. One lineage was shared between mystery snails and a native snail species, suggesting that host-switching has occurred.
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Parasites as modulators of host survival and behaviorIn our lab, we use a model system to explore various questions surrounding host-parasite dynamics. The estuarine mud crab Rhithropanopeus harrisii is parasitized by a non-native sacculinid castrating barnacle Loxothylacus panopaei along the US Atlantic coast. While L. panopaei is native to the Gulf of Mexico and Florida, it was introduced to the Chesapeake Bay with infected mud crabs associated with oysters transplanted from the Gulf. Since the 1960s, L. panopaei has parasitized US Atlantic coast populations of R. harrisii. Most notably, new populations of L. panopaei were found in NY in 2012 (Freeman, Blakeslee, and Fowler 2013). From initial infection, the crab undergoes a series of physiological and morphological changes, including complete castration and growth cessation. GMU undergraduate Allison Assur worked in the lab for the Fall 2018 research semester where her project “Personality persistence post-exposure to parasites: behavioral alterations in R. harrisii following exposure to the parasite Loxothylacus panopaei” won best poster at the GMU Biology Undergraduate Semester Research Colloquium. Her work showed that mud crabs exhibit reduced activity and boldness after infection, thus aiding the parasite in infecting the host. She is currently working to publish her findings.
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Impacts of salinity on host - parasite dynamics in estuariesR. harrisii and L. panopaei have different salinity tolerances, which may be driving spatial differences in parasite prevalence in estuaries (Blakeslee, Pochtar, Fowler et al. 2021). It is possible that hosts have a refuge from parasitism in lower saline systems. However, recently, we documented an isopod endoparasite also infecting R. harrisii even at low salinities (pictured here). Collaborators have identified this parasite as a new species of entoniscid isopod, mostly likely from the genus Cancrion. Despite the extensive knowledge on L. panopaei, there is limited knowledge on the life history or host relationships of entoniscid parasites in general, except that some species negatively impact host reproduction while others only castrate female hosts and still others that do not castrate the host at all. Of all the literature on entoniscid parasites, none discuss or mention Cancrion infecting R. harrisii, and Cancrion has not been reported from the Chesapeake Bay. We are currently uncovering how salinity shapes the spatio-temporal distribution of these host-parasite relationships, how salinity impacts the survival and metamorphosis of Cancrion larvae, and how the parasites impact R. harrisii reproduction and abundance.
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Impacts of Introduced Species on Community Dynamics
When aquatic species, especially those that provide or modify habitat, invade and become established, native species can undergo temporal changes in taxonomic and functional composition related to the invasive species’ density patterns (i.e., succession).
Novel mutualisms between native and introduced speciesAn invasive ecological engineer, the macroalga Gracilaria vermiculophyllum, has invaded virtually every temperate estuary in the Northern Hemisphere over the last 100 years. On some mudflats (e.g., SC and GA), G. vermiculophyllum went from nonexistent before 2003 to 80-100% cover in recent years. This high rate of invasion has fundamentally transformed many previously homogeneous communities that had been largely devoid of macroalgae prior to the invasion. The establishment of a foundation species like G. vermiculophyllum is fundamentally more significant to the invaded ecosystem because it does not merely use available habitat, but instead modifies and creates new habitat across biogeographical and environmental barrier. Data collected by myself and collaborators (AMH Blakeslee, East Carolina University and S Kreuger-Hadfield, University of Alabama, Birmingham) shows that G. vermiculophyllum provides habitat for a multitude of free-living macroinvertebrates and their parasites (Fowler et al., in prep). Additional work by Ph.D. candidate Alex Mott showed that a native marine tube-building polychaete worm consistently chooses to decorate its tube cap with the invasive species over native macroalgal choices (Mott et al. 2022). This work has led to further questions and hypotheses about this novel mutualism.
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Impacts of two functionally different aquatic invaders in freshwater streamsWe were funded by the Mid-Atlantic Panel on Aquatic Invasive Species to examine upstream and downstream tributaries of the Prettyboy Reservoir in Baltimore County, MD that are currently invaded by two functionally different aquatic invaders: the diatom Didymosphenia geminata and the New Zealand mud snail Potamopyrgus antipodarum. First, we surveyed streams to document invasive and native snail distribution and parasite loads to determine if parasite prevalence may be influencing snail abundance patterns. Second, we performed a field succession and facilitation experiment to examine spatiotemporal changes in the turnover of macroinvertebrate communities over one year (in the case of succession) and two months (for facilitation) as a function of seasonality and invasive species taxon and density. Densities of both species, in general, declined downstream from the reservoir, creating a natural density gradient. Integrated into our experimental design was the inclusion of citizen scientists, who participated in field and laboratory aspects of this study. In this study, we integrated the interdisciplinary fields of community ecology, parasitology, and field ecology to create and support new knowledge assessing the health, function, and threats to freshwater ecosystems and communities by invasive species. Instead of providing a snapshot on a local and reduced temporal scale, our study linked patterns in community-level processes mediated by invasive species through time and space to understand community ecology (Fowler et al., in prep).
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Human Dimensions of Invasive Species
Rapid Assessment Survey
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Live Maine Marine Baitworm Trade as a Vector for Introduced SpeciesWhile a postdoctoral researcher at the Smithsonian Environmental Research Center (SERC), I was funded through Maryland Sea Grant to examine the live baitworm trade as a vector for introducing marine and estuarine species. Maine polychaetes (Glycera dibranchiata) are used extensively as bait in the Mid-Atlantic and abroad, and dealers ship live baitworms from Maine packed in live algae globally over-night. Packing algae used are associated with numerous organisms (mostly small invertebrates), which can hitchhike with bait shipments, thus providing opportunities for possible introductions. Our study assessed diversity and abundance of macro-organisms associated with baitworms/packing algae from source to recipient regions. I counted and identified over 30,000 invertebrates to the lowest taxonomic level seasonally from 2011-2012, and the data showed that the diversity and abundance of associated biota decreases from source to recipient regions. However, there remains a large number and diversity of viable invaders arriving in recipient regions. Given the active nature of this vector, results from our study reflect the risk of introduction to other recipient regions, including global destinations like Europe, and serve as a model system for understanding live bait vectors around the world (Fowler et al., 2016; Blakeslee, Fowler et al., 2016). I continue to work on this project as a PI and co-PI with SERC and collaborators at East Carolina University (April Blakeslee), SERC (Drs. Greg Ruiz and A. Whitman Miller) and University of California - Davis (Edwin Grosholz) as we explore pathways of intervention working with local focus groups in Maine and consumers in the Mid-Atlantic and California (Wieland, Miller, and Fowler 2018; Fowler et al., in prep.).
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Long-term Monitoring in the Tidal Potomac River
As part of the Potomac Environmental Research and Education Center (PEREC) team, I serve as a Co-PI and the aquatic invertebrate ecologist for two funded projects monitoring the long-term effects of nutrient reduction in wastewater treatment effluent on the invertebrate community in Gunston Cove (funded by Fairfax County) and Hunting Creek (funded by Alexandria Renew Enterprises), both of which are tributaries of the Potomac River. These communities are sampled monthly throughout the summer and fall and assessed for changes related to environmental conditions. These samples are also used for additional undergraduate and graduate student projects, such as methods for monitoring endangered and native mussels and the fate and flow of pharmaceutical and personal care products through these tidal freshwater biotic communities. These topics are central to the PEREC mission on documenting changes to the environmental health of the Potomac River. Moving forward, both of these projects are active parts of my research program and are expected to be continued sources of funding.
Undergraduate Mentoring and Research
Between 2016 and 2020, Dr. Fowler led the PEREC team in mentoring between 5 and 10 GMU undergraduates each summer in the vein of a National Science Foundation (NSF)-funded Research Experience for Undergraduates (REU) program. Dr. Fowler led the writing and secured 5 grants to fund students to use samples obtained from our larger Gunston Cove and Hunting Creek grants. This has amounted to $180,000 from the Office of Student Scholarship, Creative Activities, and Research at GMU, the Patriot Green Fund at GMU, and Virginia Sea Grant. We were also successful in recruiting students from underrepresented groups in STEM and first-generation college students. Dr. Fowler's ultimate goal is to lead a NSF REU site at the Potomac Science Center.
International Research on Introduced Species
Introduced species are now considered one of the most important threats to natural biodiversity. However, many questions regarding the processes and patterns of successful invasions remain unanswered due to a lack of basic biological and/or ecological knowledge of the particular species in question. As crabs are among the most widespread taxa in the oceans and are among the most successful invasive marine species, they are model organisms for investigating the theories surrounding invasion biology.
Atlantic mud crab - Rhithropanopeus harrisii
As the mud crab R. harrisii is also a global invader to over 23 different countries, I initiated a global monitoring effort throughout North America and Europe during my postdoc at SERC to describe biogeographical changes in demography and morphology of its many invasive populations (Fowler et al. 2013). I received a grant from a Finnish marine laboratory in Helsinki to continue this work, which has led to a sustained collaboration with invasion scientists in Finland. Since then, I have mentored undergraduate students and served as an unofficial co-supervisor for a graduate thesis, which has led to several publications concerning the ecology of introduced species (Forsström et al. 2015, 2016, 2018; Puntila-Dodd et al. 2019). While abroad, I collaborated with researchers in Poland who were investigating the impacts of the introduced Chinese mitten crab on blue mussels, and we published the results of those experiments as well (Wojcik et al. 2015). I continue to collaborate with Scandinavian researchers, and co-authored an international manuscript concerning the addition of invasive species to maritime spatial planning (Liversage et al. 2019).
