INSECT-SYMBIONT INTERACTIONS Ecology of Symbiotes of Larval Black Flies (Diptera: Simuliidae): Distribution, Diversity, and Scale 1 2 2 JOHN W. MCCREADIE, PETER H. ADLER, AND CHARLES E. BEARD Environ. Entomol. 40(2): 289Ð302 (2011); DOI: 10.1603/EN10258 ABSTRACT Symbioses are major drivers in ecology and evolution. Although nearly omnipresent in Downloaded from https://academic.oup.com/ee/article/40/2/289/409195 by guest on 24 September 2021 ßowing waters, they remain poorly studied in these systems. To examine fundamental aspects of the ecology of symbioses in ßowing-water systems, we use larval black ßies as hosts and various fungi, nematodes, and protists as symbiotes, focusing on aspects of distribution, diversity, and scale. Most symbiotes of larval black ßies are considered parasitic, although the dynamic nature of the relationship is becoming apparent for some systems in which it shifts along a continuum involving commensalism, mutualism, and parasitism. Perspective also is moving from a pairwise view of symbiotic associations to a multispecies network of interactions. Distributions of symbiotes are related to scale-dependent processes that inßuence the hosts and the stream habitats of the hosts; thus, characteristics of streams, as well as hosts, can be useful in predicting spatial patterns of symbiotes. As the taxonomy of symbiotes improves, so too does the understanding of ecological relationships of symbiosis, such as host speciÞcity and patterns of diversity along spatial and temporal scales. KEY WORDS freshwater, microsporidia, nematodes, parasitism, streams The pursuit by ecologists to Þnd universal patterns of and diversity are the picture we wish to illustrate, scale diversity requires a broad understanding of species is the canvas on which they are drawn. interactions. The study of species interactions, how- Black ßies are ideal hosts for this exploration be- ever, has been biased, with predation and competition cause (1) the larvae play a critical role as ecosystem commanding a disproportionate amount of attention engineers in resource turnover and foodweb dynamics (Begon et al. 2006). However, multispecies microbial in lotic communities (Cummins 1988, Wotton et al. interactions are probably the prevailing form of spe- 1998, Malmqvist 2004); (2) they are taxonomically one cies interactions (Schmitt et al. 2007). Symbiosis is of the best-known groups of aquatic insects in many now recognized as a major force in the ecology and areas of the globe (Adler et al. 1999, 2004), facilitating evolution of organisms at both population and com- detection of host associations at the species level; and munity levels (Boucher 1985, Douglas 1994, Sapp 1994, (3) they are globally widespread in lotic systems Thompson 2005, Moran 2006) and as a driver of com- (Crosskey 1990), representing part of a prevailing munity structure and coevolutionary processes (Vo- symbiotic relationship. We emphasize North Ameri- gelsang et al. 2006, Moran 2007, Noda et al. 2007). can studies, but consult the world literature when Despite the ubiquitous nature and ecological im- relevant. We use our unpublished data when the lit- portance of symbiotic relationships, little is known erature lacks examples of particular patterns or pro- about the community structure and function of sym- cesses of symbiote ecology, and we reevaluate previ- bioses in freshwater habitats. To explore the ecology ously published data to provide insights into patterns of symbiosis in stream insects, we use the larval black of the symbiote assemblage. ßy host as a platform. To impose order on the review, we have selected a major theme of ecological thoughtÐ What Is Symbiosis? distribution. Indeed, ecology, broadly deÞned, is the study of factors and processes that determine the dis- Although ecologists appreciate the role of symbiosis tribution and abundance of organisms across a heter- in ecological communities, deÞning symbiosis has ogeneous landscape (Krebs 2008). The mechanisms been problematic. In its simplest form, symbiosis is an that control the distribution and diversity of species interspeciÞc interaction deÞned by Þtness effects on are scale dependent (Adler and McCreadie 1997, Mc- each participant and expressed simplistically as Ϫ,0, Creadie and Adler 1998, McGill 2010). If distribution or ϩ, with no indication of degree (Table 1). Mutu- alism, for example, is a ϩϩinteraction, with no im- 1 Corresponding author: Department of Biological Sciences, Uni- plied symmetry, that is, no assumption of whether versity of South Alabama, Mobile, AL 36688 (e-mail: jmccread@ both species beneÞt equally (symmetrical relation- jaguar1.usouthal.edu). 2 Department of Entomology, Soils & Plant Sciences, Clemson ship) or one participant receives greater beneÞt University, Clemson, SC 29634Ð0315. (asymmetrical relationship). 0046-225X/11/0289Ð0302$04.00/0 ᭧ 2011 Entomological Society of America 290 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 2 Table 1. Simple two species interactions Interactiona Species 1 Species 2 Competition Ñ Ñ Predation ϩ (predator) Ϫ (prey) Parasitism ϩ (parasite) Ϫ (host) Grazing ϩϪ/ϩ Fig. 1. Cost of symbosis in a simple three-species inter- Mutualism ϩϩaction. The symbiote (S) imparts a cost (s) to the host (H) Commensalism ϩ 0 but returns nothing directly. If the host can transmit the Neutralism 0 0 symbiote to a competitor (C), then there are two possible costs of competition, that from an uninfected competitor a Ϫ,0,ϩ are expressed in terms of the directional effects on growth (CU) and that from an infected (CI) competitor. rate, survival, reproductive ability, and fecundity; based on Odum and Barrett (2005). tinuum of symbiotic associations (Hochberg et al. Downloaded from https://academic.oup.com/ee/article/40/2/289/409195 by guest on 24 September 2021 2000, Thompson and Cunningham 2002, Neuhauser We follow the original concept of symbiosis deÞned and Fargione 2004, McCreadie et al. 2005b). From an by de Bary (1879) and subsequently embraced by evolutionary perspective, natural selection should fa- Boucher (1985), Sapp (1994, 2004), Agnew et al. vor a shift from parasitism (ϩϪ) to commensalism (ϩ (2003), and Tamas and Andersson (2003): a relation- 0) and eventually to mutualism (ϩϩ) (Price 1997). ship in which two species live in close physical asso- Phylogenetic evidence suggests that certain fungal ciation, with a degree of dependence on the associa- pathogens have shifted from pathogenicity to a non- tion. To this deÞnition, we add a time element, with at lethal form of parasitism (Humber 2008). As a corol- least one species existing in the association for a sig- lary, prevalence of commensals (e.g., trichomycetes) niÞcant part of its life. Hence, relationships between in larval black ßies is typically greater, reaching 100% ßowering plants and animal pollinators, though mu- (Beard and Adler 2002), than prevalence of parasites tualistic, would not be symbiotic. Because a size dif- (e.g., microsporidia), which typically is below 5% ference typically exists between symbiotic partici- (McCreadie and Adler 1999). pants, we follow the usual convention of referring to Symbioses are set in communities and their inter- the smaller species as the symbiote and the larger actions and consequences can manifest across multi- species as the host. Some authors use the term “sym- ple taxa and different trophic levels (Klepzig et al. biosis” in a narrower sense, referring only to mutual- 2001, Omacini et al. 2001). The community in which ism (e.g., Hentschel et al. 2000, Gross et al. 2003). We symbioses operate also must be viewed in the context Þnd such a deÞnition too restrictive for three reasons. of the abitoic environment. An early example dem- First, the nature of the interactions between species onstrating the dynamic nature of symbiotic interac- living in close association is frequently unknown. Sec- tions in response to environmental conditions was ond, such a narrow deÞnition does not emphasize the documented for mycorrhizal associations with scotch ßuid nature among commensalism, mutualism, and heather (Calluna vulgaris [L.] Hull) (Wells et al. parasitism (e.g., McCreadie et al. 2005b). Third, hav- 1930). The relationship is mutualistic when soil nitro- ing symbiosis and “mutualism” as terms for the same gen is low, but turns pathogenic toward the heather as relationship is redundant. nitrogen increases. Understanding host-symbiote dy- A few comments about parasitism are in order. Par- namics thus requires a shift of perspective from a asitism occurs when one species beneÞts, usually the pairwise view of associations to a multispecies net- symbiote, and the other is harmed, typically the host. work of interactions (e.g., Stanton 2003) set within the Demonstrating a harmful effect by the parasite can be abiotic environment. difÞcult, although in some cases, the parasite causes A simple graphical model demonstrates how the patently deleterious effects to the host, including nature of symbiotic interactions can be viewed in a death. A parasite is often viewed as causing no great community network (Fig. 1). Symbiote S takes re- harm because eliminating the host would destroy the sources from host H but supplies nothing directly to parasiteÕs habitat. Begon et al. (2006), however, argue the host. The cost to the host is s, and if only this this view is incorrect and that selection should favor pairwise interaction is considered, the interaction rep- parasites that maximize their Þtness, which at times resents parasitism. When the host has a competitor might be achieved through decreased virulence to the (C), which by deÞnition is a ϪϪinteraction (Morin host but at other times by increased virulence. Many 1999), a cost is imparted to the host. If the host trans- pathogens of insects, for example, rely on killing their mits the symbiote to the competitor, two new costs host to increase transmissibility and Þtness. Hence, a arise from the perspective of the host: CU, the cost to pathogen can be considered an extreme parasite hav- the host when competing with an uninfected com- ing effects on a population similar to those of preda- petitor, and CI, the cost to the host when competing tors.