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Research Collection Doctoral Thesis Habitat fragmentation of alpine streams: implications for genetic structure and species diversity of aquatic insects Author(s): Monaghan, Michael Thomas Publication Date: 2002 Permanent Link: https://doi.org/10.3929/ethz-a-004385646 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Diss. ETH No. 14561 Habitat Fragmentation of Alpine Streams: Implications for Genetic Structure and Species Diversity of Aquatic Insects A Dissertation submitted to the ETH ZÜRICH (SWISS FEDERAL INSTITUTE OF TECHNOLOGY) for the degree of Doctor of Natural Sciences presented by Michael Thomas Monaghan B.S. Nat. Res. Manage. The Ohio State University M.S. Biol. Idaho State University born 13 October, 1971 Columbus, Ohio, USA accepted on the recommendation of Prof. Dr. J.V. Ward, examiner Dr. M. Sartori, co-examiner PD Dr. P. Spaak, co-examiner PD Dr. C.T. Robinson, co-examiner Zürich, 2002 Chapters 2 and 3 have been published: Monaghan, M.T., P. Spaak, C.T. Robinson, and J.V. Ward. (2001). Genetic differentiation of Baetis alpinus Pictet (Ephemeroptera: Baetidae) in fragmented alpine streams. Heredity 86:395-403. Monaghan, M.T., P. Spaak, C.T. Robinson, and J.V. Ward. (2002). Population genetic structure of 3 Alpine stream insects: influences of gene flow, demographics, and habitat fragmentation. Journal of the North American Benthological Society 21: 114-131. Chapter 6 is in press: Monaghan, M.T., M. Hieber, C.T. Robinson, P. Spaak, and J.V. Ward. (In Press). Spatial patterns of Ephemeroptera, Plectopera, and Trichoptera species diversity in fragmented alpine streams. Verhandlungen Internationale Vereinigung für Theoretisch und Angewandte Limnologie 28. pour marie, qui m'a toujours fait sentir que j'appartenais ici Table of Contents Summary 1 Zusammenfassung 4 1. Introduction and outline of the thesis 7 2. Genetic differentiation of Baetis alpinus Pictet 15 (Ephemeroptera: Baetidae) in fragmented alpine streams 3. Population genetic structure of 3 alpine stream insects: 31 influences of gene flow, demographics, and habitat fragmentation 4. Local differentiation and regional homogeneity: lack of 59 equilibrium in the population genetic structure of an aquatic insect 5. Taxon richness and nestedness of benthic macroinvertebrates in 73 fragmented alpine streams: implications for freshwater conservation 6. Spatial patterns of Ephemeroptera, Plecoptera, and Trichoptera 93 diversity in fragmented alpine streams 7. Thesis conclusions and recommendations for future research 105 Curriculum vitae 111 Acknowledgements 115 1 SUMMARY Habitat fragmentation of alpine streams, as defined herein, results from the presence of standing water bodies along stream courses that separate streams into discrete flowing reaches. The standing water bodies may be of natural (lakes) or anthropogenic (reservoirs) origin. This thesis consists of five studies that investigated the effects of alpine stream habitat fragmentation on the genetic structure and species richness of benthic macroinvertebrates. Three studies were conducted to examine the genetic structure of stream insect populations and two studies examined the composition of species assemblages. The first study used allozyme electrophoresis to examine the genetic structure of 23 populations of Baetis alpinus Pictet (Ephemeroptera: Baetidae) to determine whether lakes or reservoirs act as barriers to gene flow. Estimates of genetic differentiation (q) indicated little or no genetic difference between populations along 4 nonfragmented reference streams or across 2 lakes and 2 reservoirs, but marked differentiation across 5 lakes. Differentiation was unrelated to distance between fragments, but occurred only if lakes were situated in valleys that have been ice-free throughout the Holocene. If standing water bodies act as barriers to dispersal, the low q-values across geologically younger lakes and across reservoirs suggest that genetic differentiation was not detectable within the first 100 to 1000 years of habitat fragmentation. The second study analyzed 2 additional species of alpine stream insects and investigated the hierarchical genetic structure within and among the headwaters of major drainages of the Swiss Alps (Rhine, Inn, and Ticino rivers). Rhithrogena loyolaea (Heptageniidae) exhibited little genetic differentiation within and among streams but significant differentiation among drainages, suggesting that dispersal occurs among habitat fragments and among different streams but not across watersheds. Allogamus auricollis (Limnephilidae) did not exhibit genetic differentiation at any scale, suggesting that dispersal occurs throughout the geographical range of the study. In contrast, B. alpinus showed moderate to substantial differentiation among streams, but a distinct lack of genetic differentiation among major drainages. Although a definitive explanation for this surprising result is not immediately apparent, the data suggest a lack of equilibrium between gene flow and genetic drift in B. alpinus. This lack of equilibrium results from historical gene flow that continues to mask reduced dispersal. A synthesis of the results from these three species and from additional species in other studies indicated that four consistent 2 patterns of genetic differentiation emerge when multiple spatial scales are considered. The patterns are indicative of taxon-specific dispersal ability and reflect whether taxa are in gene flow - genetic drift equilibrium. The third study further examined the relative importance of historical and contemporary processes in determining genetic structure of B. alpinus. The study used amplified fragment length polymorphism (AFLP) with the hypothesis that a molecular DNA marker such as AFLP would be more sensitive to genetic change than allozyme markers, and would therefore detect more recent population differentiation. Interestingly, results were very similar for the two markers. Population differentiation occurred only at the geologically older lakes, and small-scale differentiation and large- scale homogeneity suggested a lack of genetic drift - gene flow equilibrium. An examination of the variance in q for pairwise comparisons of all populations revealed that variance was larger for AFLP than for allozymes. Variance was unrelated to geographic distance between populations, suggesting gene flow between populations can be quite limited regardless of distance. The study concluded that the difference in variance of q reflects two stages of range expansion following recolonization of the Alps after the retreat of glaciers. The less sensitive allozymes reflect rapid upstream gene flow into alpine streams from a few glacial refugia, while AFLP markers reflect more recent, small-scale local differentiation within and among streams. The fourth and fifth studies investigated the effects of natural and anthropogenic habitat fragmentation on macroinvertebrate communities among the same study sites used for the population genetics studies. Total taxon richness, all sites combined, was 69 ranging from 6 to 27 for individual sites. While total richness was not significantly different between fragmented and unfragmented sites, both Ephemeroptera and Diptera (excluding Simuliidae) richness was significantly reduced in stream fragments. Assemblages in fragments were not nested subsets of unfragmented sites, indicating that site- and stream-specific habitat conditions, rather than extinction and lack of subsequent recolonization, were primary determinants of assemblage structure in all sites. Collectively, the results suggest taxon turnover among sites and among streams (b-diversity) is an important component of biodiversity in alpine streams. The fifth study comprised a finer-scale study of how the presence of lake-outlet habitats may affect Ephemeroptera, Plecoptera, and Trichoptera (EPT) richness in fragmented streams. Richness and turnover generally increased along longitudinal gradients of 200-300 m that 3 encompassed sites above lakes, lake outlet sites, and sites farther downstream. Eight of ten fragmented sites had reduced EPT richness, but total richness was greater in a given fragmented stream than in an unfragmented reference stream. This finding supports the contention that turnover at multiple spatial scales ( b -diversity) is an important measure of biodiversity in aquatic systems, and that lake outlets provide habitat conditions not present in unfragmented streams. One general conclusion from the combined studies is that dispersal ability is a species-specific trait; however, vagility generally is high for the benthic macroinvertebrates inhabiting alpine streams. The large number of species found only in a few widely separated fragments suggests they are capable of dispersal and that the suitability of local habitat conditions (e.g., flow and temperature regimes, disturbance, sediment structure, food resources, water velocity, water chemistry, competition, and predation) probably is the primary reason a species is present or absent in a fragment. A second conclusion concerned differences between natural and anthropogenic fragmentation in streams. Lakes and reservoirs had similar effects on taxon richness, but the effects on genetic differentiation were more pronounced in lakes. This suggests lakes and reservoirs can affect different aspects of total biodiversity and that the reduction of

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