Evolutionary Constraints on Population Structure: The Parasites of <i>Fundulus zebrinus</i> (Pisces: Cyprinodontidae) in the South Platte River of Nebraska

Population and community descriptor values (parasites per host, prevalence per parasite species, variance/mean ratios, species density, and diversity indices) for the 7-species parasite community of 61 relatively homogeneous samples of Fundulus zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska, U.S.A., taken over a 14-yr period, are reported. South Platte River streamflow fluctuates over 2 orders of magnitude on several time scales-monthly, annually, and over multiple year wet-dry cycles. Relatively homogeneous sampling of a single host species with several parasite species provided a system that allowed assessment of the contribution of evolved parasite life cycles to population structure in an everchanging environment. No significant negative species-to-species associations were observed. Species abundance, order of abundance, and diversity were affected most strongly by streamflow, with high water reducing prevalence and abundance of larval trematode parasites. Each parasite species had its characteristic longand short-term patterns of variation in population descriptor values, with mostly longterm stability superimposed on sometimes extreme short-term fluctuations of descriptor values. The differences in these characteristic patterns were considered products primarily of the evolved life cycle traits and transmission mechanisms operating in the common fluctuating environment. The parasite community as a whole showed resilience, returning to preperturbation diversity following extended periods of high water. The Platte River system of Nebraska provides a natural laboratory in which abundant populations of small fish acquire various kinds of parasites under fluctuating transmission conditions. The South Platte River (headwaters in the Rocky Mountains west of Denver, Colorado) is particularly useful as a site for long-term studies of parasite population and community dynamics because streamflow, the primary factor influencing aquatic habitat diversity in the bed and channels, varies by up to 2 orders of magnitude. Furthermore, South Platte River streamflow is not regulated by dams and diversions to the same extent as other prairie rivers, e.g., the North Platte. Annual average South Platte River flow thus is determined mainly by Rocky Mountain snowpack, seasonal flow is melt dependent, and headwater storms can produce temporary surges in discharge. Streamflow fluctuations therefore occur on a number of time scales, from rapid responses to headwater events to multiyear dry-wet cycles. The Platte River system contains about 40 species of fish, at least half of which are minnows, but the cyprinodontid Fundulus zebrinus is abundant, widely distributed throughout the system, and infected with at least 7 different species or ecotypes of parasites (Janovy and Hardin, 1987, 1988). Parasite transmission is potentially affected by abiotic conditions, both directly, e.g., through concentration of hosts or changes in the current through which infective stages must pass, and indirectly, mainly through effects on intermediate host populations (Webbe, 1966a, 1966b; Camp and Huizinga, 1980; Granath and Esch, 1983a, 1983b; Stables and Chappell, 1986). The fish population can be considered a supply of patches that vary genetically and physiologically only within the limits of the host species and are colonized in ecological time by parasites that, in turn, are constrained by their evolved life cycle requirements (Dobson and Pacala, 1992). Among the parasite species are extreme specialists (the gill-inhabiting monogenean Salsuginus thalkeni, found only on F. zebrinus) and extreme generalists (larval Posthodiplostomum minimum, occurring in the eyes and body cavity, and reported from nearly 100 species of fish). These parasites also are transmitted through several different types of life cycles (Table I) and thus represent a variety of transmission mechanisms and potential responses to fluctuating abiotic conditions. At its most general level, the study of F. zebrinus parasite population and community dynamics is a study of the response of evolutionarily constrained parasite transmission systems (life cycles) to everchanging, and only partially predictable, transmission conditions. Finally, the entire system is easily modelled, leading to testable predictions, about such responses, applicable to natural systems more easily manipulated than the South Platte River and its inhabitants (Janovy and Kutish, 1988; Janovy et al., 1990, 1992, 1995). It is hypothesized that evolved parasite life cycles and the associated transmission mechanisms are major contributors to parasite species differences in population structure, especially over the long term. As a consequence of such contributions, these life cycles represent constraints against which the shorter, ecological time, transmission events operate. Thus, an observed parasite population structure (prevalence, mean, variance/mean ratio, frequency distribution of best fit, etc.) has both evolutionary and ecological components. The evolutionary component is held constant in ecological time by parasite genes, whereas the ecological component can be varied either experimentally or by nature. Such variation in the ecological component should reveal the contribution of the evolutionary component, which should be manifested as taxon-specific population structure responses to the varying, but shared, transmission conditions. The objective of the studies described in this paper was to assess the validity of the above ideas by determining the characteristic responses of several parasite species' population structures to fluctuating transmission environments over a relatively long period. When this project was initiated in the late 1970s it was felt that 5 yr was an adequate time to gather data (Janovy and Hardin, 1987, 1988). The subsequent 9 yr, however, provided data on processess not revealed by the earlier observations, e.g., evidence for overwinter mortality of fish infected with larval trematodes and the effects of sustained low Received 24 June 1996; revised 19 February 1997; accepted 19 February 1997.