For decades, ecologists have focused on antagonistic interactions such as competition and predation in studies of ecosystems and food webs. But in recent years it has become apparent that cooperative interactions among species, i.e., mutualisms, can be equally important to ecosystem structure and function. One widespread mutualism is that between pollinators and plants, which is of major economic importance to agricultural systems. However, other types of mutualisms are prevalent in nature, but poorly understood. This project will study a model system involving a cleaning mutualism, a species interaction in which one organism feeds by cleaning another. The mutualism involves crayfish and small annelid worms, which live on the gills of crayfish. The worms clean the crayfish gills by feeding on organisms that attach to the gills; this benefits both the worms and the crayfish. However, if the worms become too abundant relative to their food, they can switch to act as parasites, feeding directly on the crayfish?s gills. This shift from mutualism to parasitism is not unique to the crayfish-worm system. It has been hypothesized that such shifts may be widespread in nature in response to certain environmental changes. This project will test that general hypothesis using both field and laboratory experiments to study the crayfish-worm model system. The project will examine the importance of species behaviors and other traits in maintaining the interaction at mutually beneficial levels, and explore how the mutualism is shaped by environmental context. The project will also explore the broader consequences of a shift from mutualism to parasitism to the rest of the food web and stream ecosystem.

This project has substantial broader impacts; it is a collaboration among faculty at three universities, one of which is a predominantly undergraduate institution. Many undergraduate students will be training in aquatic ecology, and will participate in team-structured, multi-year research projects. A number of graduate students will also be supported by this project, and will lead outreach efforts through partnerships with local watershed associations and university extension programs.

Project Report

Most people are aware of, and fascinated by, mutualistic relationships – symbioses between species that benefit all involved. Well known mutualisms include cleaner shrimp removing parasites from fish and pollination of flowers by bees. A lesser-known mutualism involves crayfish and branchiobdellidan worms. These worms, which are closely related to earthworms and leeches, feed on material found on the surface of their crayfish hosts. Worms gain food, transportation, and a site for reproduction. Crayfish benefit by being cleaned of fouling organisms. Just as in our own relationships, the outcomes of this symbiosis can change over time. The relationship can change from benefiting both partners, to helping only one but not the other (commensalism), to harming one partner (parasitism). Understanding the factors that lead to shifts in symbiotic outcomes help scientists understand how changing environmental conditions can facilitate mutualisms or cause shifts to commensal or parasitic relationships in natural and aquaculture systems. We used red swamp crayfish (Proambarus clarkii) and their associated worms (Cambarincola barbarae) to investigate shifts between mutualistic, commensal, and parasitic relationships. Similar to previous studies, we found that crayfish in surface waters with a lot of organic material (leaves, sticks, etc.) exhibited better growth if they hosted worm symbionts. Contrary to previous studies that utilized different crayfish and worm species, the relationship remained beneficial to crayfish even when the worm population increased to >100 worms/crayfish. Worms did not switch to parasitism with increasing population density. The red swamp crayfish is the same species that is grown by farmers in Louisiana as an integral part of Cajun culture. Thus, rather than being "gross" and unhealthy, wormy crayfish in aquaculture ponds are likely to be larger and more healthy than crayfish without worms. We also found evidence that ecosystem function (any given process that occurs in an ecosystem) is influenced by the presence of worms on crayfish. Crayfish with worms processed (broke down) dead leaves in the water at a faster rate than crayfish that lacked branchiobdellidans. While many species of crayfish spend their entire lives in open water, some burrow during specific seasons while still others spend the majority of their lives in terrestrial burrows. Although there is likely much protection gained in residing in a burrow, there are also considerable tradeoffs. Our study showed that when P. clarkii shifted to burrows, they lost the beneficial relationship with worms. Worms were either greatly reduced or disappeared completely. The most likely explanation is that worms were either scraped off or dried out during the burrowing process. Thus, during the hot summer months and/or drought, red swamp crayfish must make a tradeoff: either stay in rapidly shrinking bodies of water and preserve the beneficial relationship with worms, or burrow underground to groundwater but sacrifice beneficial worms. This sacrifice may not be a tradeoff for all crayfish species. Red swamp crayfish are weak burrowers and become relatively dormant underground. Other crayfish species are strong burrowers and live active lives underground. Whereas the worm species in this study lives on the external carapace of its host, other worm species live inside the gill chambers of crayfish and would be protected during the burrowing phase. Gill dwelling worms may help keep gills of some crayfish species clean in the muddy burrow waters. Thus, the mutualistic relationship may be controlled not only by the environment that the crayfish chooses, but by the habitat within the crayfish where the worm has evolved to reside. There were multiple broader impacts of this study. We designed and refined a novel burrowing chamber design that allows researchers to easily conduct replicated, controlled experiments on burrowing organisms in the laboratory. Techniques developed in this study led to a collaborative project with the USFWS to study the life-history of a state-threatened crayfish: The Piedmont Blue Burrower (Cambarus harti). The NSF study led to development and publication of a special issue on crayfish ecology in the journal Freshwater Science, which in turn led the PI’s to initiate a collaborative effort to investigate the life histories of crayfish species of the Southeastern U.S. – the worldwide epicenter of crayfish diversity. Two graduate students and many undergraduates were trained and mentored during the course of this study, and projects that evolved from this study. Their efforts led to authorship of multiple peer-reviewed manuscripts as well as presentations at regional and international scientific conferences. Many of the undergraduates are now enrolled in, or actively applying to graduate school. Results of this project were disseminated to other students via guest lectures in various courses and departmental seminars as well as multiple tours of the South Auburn Fisheries Research Station and the Auburn University Museum of Natural History (AUMNH). Burrowing crayfish videos are posted on This research contributed multiple voucher specimens and served as a seed for a growing branchiobdellidan collection in the Invertebrate Collection at AUMNH.

National Science Foundation (NSF)
Division of Environmental Biology (DEB)
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Alan James Tessier
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Auburn University
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