W&M ScholarWorks VIMS Articles 10-5-2017 Bottom-Up Control of Parasites David S. Johnson Virginia Institute of Marine Science, [email protected] Richard Heard Gulf Coast Research Laborartory Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Aquaculture and Fisheries Commons, Environmental Health Commons, and the Parasitology Commons Recommended Citation Johnson, David S. and Heard, Richard, "Bottom-Up Control of Parasites" (2017). VIMS Articles. 2. https://scholarworks.wm.edu/vimsarticles/2 This Article is brought to you for free and open access by W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. Bottom-up control of parasites 1, 2 DAVID SAMUEL JOHNSON AND RICHARD HEARD 1Department of Biological Sciences, The College of William and Mary, Virginia Institute of Marine Science, 1375 Greate Road, Gloucester Point, Virginia 23062 USA 2Department of Coastal Sciences, Gulf Coast Research Laboratory, University of Southern Mississippi, 703 East Beach Street, Ocean Springs, Mississippi 39564 USA Citation: Johnson, D. S., and R. Heard. 2017. Bottom-up control of parasites. Ecosphere 8(10):e01885. 10.1002/ecs2.1885 Abstract. Parasitism is a fundamental ecological interaction. Yet we understand relatively little about the ecological role of parasites compared to the role of free-living organisms. Bottom-up theory predicts that resource enhancement will increase the abundance and biomass of free-living organisms. Similarly, para- site abundance and biomass should increase in an ecosystem with resource enhancement. We tested this hypothesis in a landscape-level experiment in which salt marshes (60,000 m2 each) received elevated nutri- ent concentrations via flooding tidal waters for 11 yr to mimic eutrophication. Nutrient enrichment ele- vated the densities of the talitrid amphipod, Orchestia grillus, and the density and biomass of its trematode parasite, Levinseniella byrdi. Strikingly, L. byrdi prevalence increased over time, up to 13 times higher in nutrient-enriched marshes (30%) relative to the mean prevalence in reference marshes (2.4%). The biomass density of infected amphipods was, on average, 11 times higher in nutrient-enriched marshes (1.1 kg/ha) than in reference marshes (0.1 kg/ha), when pooling across all years. Orchestia grillus biomass comprises 67% of the arthropod community biomass; thus, nutrient enrichment elicits a substantial surge in para- sitized biomass in the arthropod community. If our results are typical, they suggest that eutrophication can increase parasite abundance and biomass with chronic resource enhancement. Therefore, minimizing aquatic nutrient pollution may prevent outbreaks of parasites with aquatic hosts. Key words: coastal wetlands; disease ecology; eutrophication; fertilizer; host traits; intertidal. Received 3 March 2017; revised 16 May 2017; accepted 14 June 2017. Corresponding Editor: Andrew W. Park. Copyright: © 2017 Johnson and Heard. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected] INTRODUCTION roles. For instance, parasites can alter trophic interactions (Lafferty and Morris 1996), dominate Almost a century ago, Charles Elton, the father food-web links (Lafferty et al. 2008), and control of animal ecology, wrote “...it is best to treat a significant portion of the energy and biomass parasites as being essentially the same as carni- in an ecosystem (Kuris et al. 2008). vores...” (Elton 1927), thereby recognizing para- One ecological issue that remains unclear for sitism as a fundamental ecological interaction. parasites is the role of bottom-up control. Bot- Yet, almost a century later, the role of parasites in tom-up theory states that enhancing a limiting the ecological theater remains understudied and resource such as light, nutrients, or energy at one undervalued when compared to their free-living trophic level will lead to increased productivity counterparts. This is understandable given the at higher trophic levels. For example, phospho- expertise needed to identify parasites, which rus amendments to Arctic streams lead to often have complex, multi-host life cycles. Stud- increased epilithic algae, which fuels aquatic ies of parasite ecology in recent decades, how- insect production and in turn elevates fish pro- ever, have put a spotlight on their ecological duction (Slavik et al. 2004). From forests (Wallace ❖ www.esajournals.org 1 October 2017 ❖ Volume 8(10) ❖ Article e01885 JOHNSON AND HEARD et al. 1997, Kaspari et al. 2008) to lakes (Carpen- intermediate host, the semi-terrestrial, talitrid ter et al. 2001) to rocky shores (Menge 1992) amphipod Orchestia grillus, as our model system to estuaries (Johnson 2011), bottom-up control (Fig. 1; see Appendix S1 for details). Orchestia of free-living organisms is well established. The grillus is a numerically dominant arthropod in question remains, however, do parasite respon- the ecosystem of study (Johnson 2011) and ses to bottom-up factors parallel those of their amphipods infected with L. byrdi turn bright free-living counterparts? If resource enhance- orange (Fig. 2A, B), facilitating identification of ment elevates free-living biomass, then it should infected and uninfected individuals during field also increase parasite biomass in at least two collections. We hypothesized that nutrient ways. First, functional-response theory predicts enrichment would increase both amphipod host that greater host density (i.e., free-living organ- and trematode parasite density. isms) will lead to higher host encounter rates and therefore opportunities for infection (Holling MATERIALS AND METHODS 1959). Second, from an energetics perspective, more energy in the system may fuel greater pro- Site description duction of parasites within each host (e.g., higher Our study was conducted in the Plum Island fitness in the sense of reproductive output; John- Estuary in northeast Massachusetts, USA (42°450 son et al. 2007). N; 70°520 W). The system has twice-daily tides Elucidating the potential of bottom-up control (mean tide range 2.9 m; salinity 20–33 psu). Of on parasites may have implications for the role the total estuarine area of 59.8 km2, approxi- of anthropogenic activities on infectious disease mately 39.8 km2 is vegetated wetlands, most of (National Research Council 2001). Aquatic which is Spartina salt marsh. Spartina alterniflora ecosystems throughout the globe are enriched (smooth cordgrass; 130–200 cm in height) forms with nutrients (i.e., eutrophied; Smith 2003, Dee- a2–3 m wide band along tidal creek channels gan et al. 2012). Large-scale correlative studies and is flooded twice a day. Spartina patens (salt- suggest that eutrophication can increase parasite meadow cordgrass; 20–50 cm tall aboveground prevalence (Altman and Byers 2014), but this production) dominates the high-marsh platform effect may be confounded with other co-occur- and is flooded by ~30% of high tides and inun- ring stressors such as temperature (Johnson et al. dated ~4% of the time (Johnson et al. 2016). 2007). While controlled mesocosm experiments In the current study marsh, L. byrdi infects at alleviate the problem of confounding factors and least two talitrid amphipods, O. grillus and support the conclusions of correlative studies Uhlorchestia spartinophila (see Bousfield and (Johnson et al. 2010), they may miss ecological Heard 1986). Uhlorchestia spartinophila are limited interactions that occur at larger scales and are to the low marsh and do not co-occur in the important to parasite dynamics. For these irregularly flooded high marsh with O. grillus. reasons, the National Research Council has Another species, Uhlorchestia uhleri, which has called for an ecosystem-level approach and not been observed in our study sites, may also experiments that embrace parasite and host ecol- serve as a second intermediate host for L. byrdi ogy to understand disease emergence (National (see Bousfield and Heard 1986). Research Council 2001). Here, we take advantage of an ecosystem- Nutrient enrichment experiment scale, long-term nutrient enrichment experiment The nutrient manipulations are detailed in Dee- in salt marshes to explore parasite–host dynam- gan et al. (2012) and summarized here. The ics under varying resource levels. For 11 yr ecosystem-level experiment consisted of six (2004–2014), two salt marsh ecosystems experimental marsh units (three reference and (60,000 m2) in northeast Massachusetts were three nutrient enriched), comprised first-order enriched with nutrient levels corresponding to tidal creeks (~300 m long, 15 m wide at the moderately to highly eutrophic waters by adding mouth tapering to 2 m near terminus) and dissolved nutrients to the flooding tidal water 60,000 m2 of marsh area. To mimic eutrophica- À (Deegan et al. 2012). We chose the trematode tion, nitrogen was added as nitrate (NO3 ), the parasite Levinseniella byrdi and a second form that dominates land-derived eutrophication. ❖ www.esajournals.org 2 October 2017 ❖ Volume 8(10) ❖ Article e01885 JOHNSON AND HEARD Fig. 1. Levinseniella byrdi life cycle. Adult L. byrdi sexually reproduce within ceca and rectum of shore and marsh birds (definitive hosts). Eggs are passed in bird feces and consumed by hydrobiid snails (first intermediate host). Asexual sporocyst develops