Larval Trematode Communities as Indicators of Wetland Ecosystem Health

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Project Type: 
Research
Project Number: 
R/CE-130
Inception Date: 
2003
Completion Date: 
2005
Theme Area: 
Coastal Ecosystem and Public Health

Participants:

James Byers University of Georgia Principal Investigator
Todd Huspeni University of California Co-Principal Investigator
Mark Torchin University of California Co-Principal Investigator

Students Involved:

Irit Altman UNH - Department of Biological Sciences
April Blakeslee UNH - Department of Biological Sciences
Sarah Fierce Dartmouth College
Deb Zdankiewicz UNH - Institute for the Study of Earth, Oceans and Space
Chelsea Wood Dartmouth College
Erin Dewey University of New Hampshire
Amy Fowler UNH - Department of Biological Sciences
Ben Cilley UNH - Department of Biological Sciences
Lena Collins UNH - Department of Biological Sciences
Thais Fournier UNH - Department of Biological Sciences
Brielle Friedman UNH - Department of Biological Sciences
Abstract: 

Because of a typically large number of anthropogenic disturbances, efforts to identify the agents of degradation of salt marshes can be costly and difficult. Some of these agents include chemical pollution (e.g., eutrophication, PCBs, hydrocarbons, heavy metals), physical degradation (e.g., erosion; diking; alteration of current, temperature or salinity regime), and modification of biological structure and consequent trophic interactions.

We seek to develop an efficient, holistic method of assessing whether a marsh system is significantly degraded by analyzing the structure of digenetic trematode parasites within the marsh community. Digenetic trematodes are prime candidates to use as indicator species within a marsh because they obligately use several hosts to complete their complex life cycles. Thus, the parasites' presence necessitates the presence of all other host species in the cycle; if any link in the trematode's life cycle is compromised or missing, the parasite declines or is locally extirpated.

We hypothesize that variation in parasite diversity and abundance directly reflects variability in environmental quality and the abundance and density of the parasites' host populations. Because these parasites are trophically transmitted to the final host, these parasites also reveal the extent and strength of predator-prey interactions on a local scale.

In contrast to extensive surveys that approach impact assessment on a species-by-species or a stressor-by-stressor basis, this technique capitalizes on the trematode species' integration of stresses that may be acting on many species (hosts) at variable spatial and temporal scales. This process could drastically improve our detection of marsh degradation, which may be subtle or increase through time, and also eventually save tremendous time, effort and expense compared to traditional techniques to pinpoint environmental impacts within marshes.

Objectives: 

The objectives of this task are to determine the effectiveness of trematode parasites as biological indications of marsh degradation. Specifically, we address two main objectives:

1) What are the physical, chemical and biological attributes within salt marshes across a regional scale that influence trematode diversity and abundance in first intermediate host snails?

2) Can the presence (or absence) of individual trematode species in first intermediate host snails predict the presence (or absence) of other host species in the parasites' life cycle?

Methodology: 

We will monitor physical (temperature, salinity, currents, pH), chemical (e.g., N, P, lead, mercury), and biological (number of birds, crabs, bivalves, snails and fish, and chlorophyll) variables in at least 20 sites throughout northern New England. At each site we will collect mature snails (Littorina littorea, Ilyanassa obsoleta) to examine for trematode parasite infection. Parasite species richness and prevalence of infection within each snail host population will be analyzed with multivariate analyses to determine which environmental factors are most influential on parasite diversity and prevalence.

Rationale: 

We propose a supplemental tool to assess the ecosystem health of estuaries using a single metric--the abundance and diversity of digenetic trematode parasites. By monitoring a suite of trematodes that are obligately dependent on the presence of healthy, viable populations of other marsh species that serve as hosts, we integrate the detection of impacts occurring at a variety of trophic levels within the marsh. Marine resource managers in New England (The Nature Conservancy, NH Estuaries Project, NH Fish and Game, NH Coastal Program and the NOAA NERR System) will benefit from our project.

Accomplishments: 
Impacts
 
This project led to several findings of major importance to scientific and resource management communities, including:
 
1. Trematode parasites alter community structure
 
2. The most abundant, conspicuous snail throughout the northeastern coastline of North America (Littorina lttorea) is in fact a non-native species
 
3. Trematodes provide a holistic metric of wetland health because their life histories integrate many host taxa and the trematodes are directly sensitive to environmental perturbation.
 
We believe this latter point will lead to the development of trematodes as an important estuarine indicator species in New England marshes and estuaries. We are in the process of consulting with NERR managers in N.H. and Maine to explain the findings of our results.

 

Success in Meeting Objectives

 
To quantify the effectiveness of trematode parasites as biological indications of marsh degradation I set forth two main objectives:
 
1) What are the physical, chemical and biological attributes within salt marshes across a regional scale that influence trematode diversity and abundance in first intermediate snail hosts?
 
To answer this question I investigated trematode infection in two of the most abundant snails occurring in marine environments in northern New England, the common periwinkle Littorina littorea and the mudsnail Ilyanassa obsoleta. This objective has been assessed in great detail for Littorina littorea. Gull abundance (a definitive host for trematodes) and snail size (a proxy for age) are far and away the most influential determinants of trematode infection in the snail host. What we know to date is that host abundance, road density, and certain organic chemicals correlate strongly with trematode species richness and abundance in New England salt marshes.
 
2) Can the presence (or absence) of individual trematode species in first intermediate host snails predict the presence (or absence) of other host species in the parasites’ life cycle?
 
This objective was also met, though it proved tougher than objective 1. Details of this analysis will also be forthcoming in the next couple of months. The difference in most marshes was not in terms of presence/absence of species but rather in regards simply to abundance. Thus we mostly explored how abundance and prevalence of trematodes in snails correlated with abundance of second and definitive hosts and their prevalence levels.
 
New Research Directions Pursued During the Course of the Project
 
The trematode prevalence in Littorina littorea in salt marshes proved to be so low that it was not enhancing the resolution gained by looking at the trematodes of Ilyanassa alone (the two snails are infected by a non-overlapping suite of trematode species). So we examined our salt marsh project on Ilyanassa obsolete only. Determined not to completely give up on Littorina littorea, we sampled it heavily on the coast, which is the snail’s predominant habitat. And sure enough, its trematode rates were higher there. This led us into a lengthy, but profitable study on the large scale determinants of trematodes infection in Littorina littorea on a New England-wide scale. We showed that infection is largely determined by local processes favoring high gull abundance. In fact the lack of gulls (an important definitive host for L. littorea trematodes) seemed to be why Littorea littorea was so lightly parasitized in marshes.  
 

Because of our success in the coastal Littorina littorea system and the strength of our analyses, we decided to conduct a study on the effects of trematodes on the ecological community in which they are based. We were able to show that by affecting snail grazing rates, trematodes can influence the structure of algae. This is the first time anyone had documented a trickle-down, community-wide influence of parasites.
 
Impacts of Research on Society
 
This work should increase the possible options for salt marsh managers to monitor the biological health of marshes. Surveying fauna is difficult and time consuming. While identifying trematodes is not necessarily easy either, with the right collaboration it can be a fast and effective approach.

Publications

Available from the National Sea Grant Library (use NHU number to search) or NH Sea Grant

Journal Article

  • Blakeslee, A., I. Altman, A. Miller, J. Byers, C. Hamer and G. Ruiz. Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges. Journal of Biogeography 39(3):609-622, March 2012.
  • Altman, I. and J. Byers (2014). Large-scale spatial variation in parasite communities influenced by anthropogenic factors. Ecology 95(7):1876-1887, July 2014.
  • Byers, J., A. Blakeslee, E. Linder, A. Cooper and T. Maguire (2008). Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89(2):439-451, 2008.
  • Blakeslee, A. and J. Byers (2008). Using parasites to inform ecological history: comparisons among three congeneric marine snails. Ecology 89(4):1068-1078, 2008.
  • Blakeslee, A., J. Byers and M. Lesser (2008). Solving cryptogenic histories using host and parasite molecular genetics: the resolution of "Littorina littorea's" North American origin. Molecular Ecology 17(16):3684-3696, 2008.

Thesis/Dissertation

  • Wood, C. (2006). Effects of the trematode "Cryptocotyle lingua" on the behavioral ecology of "Littorina littorea" in the New England rocky intertidal zone. Undergraduate Honor's Thesis, Dartmouth College.
  • Altman, I. (2010). Trematode parasites of the mudsnail "Ilyanassa obsoleta": an analysis of parasite communities at different scales. Doctoral Dissertation, University of New Hampshire.

Proceeding

  • Wood, C., J. Byers, K. Cottingham, I. Altman, M. Donahue and A. Blakeslee (2007). Parasites alter community structure. Proceedings of the National Academy of Sciences 104(22):9335-9339, May 29, 2007.