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Evolutionary Constraints on Population Structure: the Parasites of Fundulus Zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska

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Evolutionary Constraints on Population Structure: the Parasites of Fundulus Zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln John Janovy Publications Papers in the Biological Sciences 8-1997 Evolutionary Constraints on Population Structure: The Parasites of Fundulus zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska John J. Janovy Jr. University of Nebraska - Lincoln, [email protected] Scott D. Snyder University of Nebraska at Omaha, [email protected] Richard E. Clopton Peru State College, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/bioscijanovy Part of the Parasitology Commons Janovy, John J. Jr.; Snyder, Scott D.; and Clopton, Richard E., "Evolutionary Constraints on Population Structure: The Parasites of Fundulus zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska" (1997). John Janovy Publications. 37. https://digitalcommons.unl.edu/bioscijanovy/37 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in John Janovy Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 83(4), 1997 p. 584-592 ? American Society of Parasitologists 1997 EVOLUTIONARYCONSTRAINTS ON POPULATIONSTRUCTURE: THE PARASITESOF FUNDULUSZEBRINUS (PISCES: CYPRINODONTIDAE)IN THE SOUTH PLATTERIVER OF NEBRASKA J. Janovy, Jr., S. D. Snyder, and R. E. Clopton School of BiologicalSciences, Universityof Nebraska-Lincoln,Lincoln, Nebraska 68588-0118 ABSTRACT: Populationand communitydescriptor values (parasitesper host, prevalenceper parasitespecies, variance/meanratios, species density, and diversity indices) for the 7-species parasitecommunity of 61 relatively homogeneoussamples 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 streamflowfluctuates over 2 ordersof magnitudeon several time scales-monthly, annually,and over multipleyear wet-dry cycles. Relatively homogeneoussampling of a single host species with several parasitespecies provideda system that allowed assessmentof the contributionof evolved parasitelife cycles to populationstructure in an everchangingenvironment. No significantnegative species-to-speciesassociations were observed.Species abundance,order of abundance,and diversitywere affected most strongly by streamflow,with high water reducingprevalence and abundanceof larval trematodeparasites. Each parasitespecies had its characteristiclong- and short-termpatterns of variationin populationdescriptor values, with mostly long- term stability superimposedon sometimes extreme short-termfluctuations of descriptorvalues. The differencesin these charac- teristicpatterns were consideredproducts primarily of the evolved life cycle traitsand transmissionmechanisms operating in the common fluctuatingenvironment. The parasitecommunity as a whole showed resilience, returningto preperturbationdiversity following extendedperiods of high water. The Platte River system of Nebraska provides a natural lab- ity, and reported from nearly 100 species of fish). These para- oratory in which abundant populations of small fish acquire sites also are transmitted through several different types of life various kinds of parasites under fluctuating transmission con- cycles (Table I) and thus represent a variety of transmission ditions. The South Platte River (headwaters in the Rocky mechanisms and potential responses to fluctuating abiotic con- Mountains west of Denver, Colorado) is particularly useful as ditions. At its most general level, the study of F. zebrinus par- a site for long-term studies of parasite population and com- asite population and community dynamics is a study of the munity dynamics because streamflow, the primary factor influ- response of evolutionarily constrained parasite transmission encing aquatic habitat diversity in the bed and channels, varies systems (life cycles) to everchanging, and only partially pre- by up to 2 orders of magnitude. Furthermore, South Platte River dictable, transmission conditions. Finally, the entire system is streamflow is not regulated by dams and diversions to the same easily modelled, leading to testable predictions, about such re- extent as other prairie rivers, e.g., the North Platte. Annual av- sponses, applicable to natural systems more easily manipulated erage South Platte River flow thus is determined mainly by than the South Platte River and its inhabitants (Janovy and Ku- Rocky Mountain snowpack, seasonal flow is melt dependent, tish, 1988; Janovy et al., 1990, 1992, 1995). and headwater storms can produce temporary surges in dis- It is hypothesized that evolved parasite life cycles and the charge. Streamflow fluctuations therefore occur on a number of associated transmission mechanisms are major contributors to time scales, from rapid responses to headwater events to mul- parasite species differences in population structure, especially tiyear dry-wet cycles. over the long term. As a consequence of such contributions, The Platte River system contains about 40 species of fish, at these life cycles represent constraints against which the shorter, least half of which are minnows, but the cyprinodontid Fun- ecological time, transmission events operate. Thus, an observed dulus zebrinus is abundant, widely distributed throughout the parasite population structure (prevalence, mean, variance/mean system, and infected with at least 7 different species or ecotypes ratio, frequency distribution of best fit, etc.) has both evolu- of parasites (Janovy and Hardin, 1987, 1988). Parasite trans- tionary and ecological components. The evolutionary compo- mission is potentially affected by abiotic conditions, both di- nent is held constant in ecological time by parasite genes, rectly, e.g., through concentration of hosts or changes in the whereas the ecological component can be varied either exper- current through which infective stages must pass, and indirectly, imentally or by nature. Such variation in the ecological com- mainly through effects on intermediate host populations (Webbe, ponent should reveal the contribution of the evolutionary com- 1966a, 1966b; Camp and Huizinga, 1980; Granath and Esch, ponent, which should be manifested as taxon-specific popula- 1983a, 1983b; Stables and Chappell, 1986). The fish population tion structure responses to the varying, but shared, transmission can be considered a supply of patches that vary genetically and conditions. physiologically only within the limits of the host species and The objective of the studies described in this paper was to are colonized in ecological time by parasites that, in turn, are assess the validity of the above ideas by determining the char- constrained by their evolved life cycle requirements (Dobson acteristic responses of several parasite species' population and Pacala, 1992). Among the parasite species are extreme spe- structures to fluctuating transmission environments over a rel- cialists (the gill-inhabiting monogenean Salsuginus thalkeni, atively long period. When this project was initiated in the late found only on F. zebrinus) and extreme generalists (larval Pos- 1970s it was felt that 5 yr was an adequate time to gather data thodiplostomum minimum, occurring in the eyes and body cav- (Janovy and Hardin, 1987, 1988). The subsequent 9 yr, how- ever, provided data on processess not revealed by the earlier Received 24 June 1996; revised 19 February1997; accepted 19 Feb- observations, e.g., evidence for overwinter mortality of fish in- ruary 1997. fected with larval trematodes and the effects of sustained low 584 JANOVY ET AL.-PARASITES OF F. ZEBRINUS 585 TABLEI. Parasites, with life cycles and transmission mechanisms, of sex determined, occasionally during dissection if not obvious from ex- Fundulus zebrinus in the South Platte River of Nebraska. ternal characters. Body surface, eyes, gills (including both sides of each arch), intestine, and body cavity were examined for parasites, and num- bers of the various species were recorded for each infection site. Myx- Parasite; infection site; life intermediate host; transmission cycle; obolus funduli cysts were recorded as immature or mature (translucent stages or opaque), and S. thalkeni were recorded as immature, mature, or grav- id, but all individual parasites are included in the numbers reported in funduli tissues; indirect; freshwater Myxobolus (Myxozoa); gill oligo- this paper. chaetes?; spore-bearing triactinomyxons The data set consists of parasite counts per fish, per parasite species, Trichodina sp. (Ciliophora); gill surface; direct; swimming telotroch from 61 relatively homogeneous samples of 8-24 fish each (total 1,219), stage taken from 1982 to 1995. Actual collection dates (number of fish ex- Gyrodactylus bulbacanthus (Monogenea); gill surface; direct; vivipa- amined) are as follows: 1982: 5/20 (16), 7/19 (16), 8/2 (26); 1983: 6/9 rous, fish-to-fish contact and passing of juvenile worms (21), 6/15 (11), 7/14 (16), 7/25 (28); 1984: 6/1 (19), 6/19 (15), 7/25 5/25 6/8 6/15 6/27 6/29 Salsuginus thalkeni (Monogenea); gill surface; direct; egg, free-swim- (8); 1985: 5/20 (23), (27), (24), (24), (19), (23), 7/1 7/20 8/10 1986: 5/21 6/4 (24), 6/29 (24), 7/16 ming larva encounters host (22), (23), (19); (24), (14); 1987: 5/26 (24), 6/12 (20), 7/30 (22), 9/8 (24); 1988: 5/11 (16), Gyrodactylus stableri (Monogenea); body surface, fins; direct; vivipa- 6/1 (24), 6/19 (24),
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