Investigations of Altered Aquatic Ecosystems: Biomonitoring, Disease, and Conservation
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Investigations of Altered Aquatic Ecosystems: Biomonitoring, Disease, and Conservation by Kevin Bryce Lunde A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Environmental Science, Policy, and Management in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Vincent H. Resh, Chair Professor Adina M. Merenlender Professor G. Mathias Kondolf Fall 2011 Investigations of Altered Aquatic Ecosystems: Biomonitoring, Disease, and Conservation Copyright 2011 by Kevin Bryce Lunde ABSTRACT Investigations of Altered Aquatic Ecosystems: Biomonitoring, Disease, and Conservation by Kevin Bryce Lunde Doctor of Philosophy in Environmental Science, Policy, and Management University of California, Berkeley Professor Vincent H. Resh, Chair Changes to hydrology, water chemistry, physical habitat, and the landscape surrounding aquatic ecosystems can have profound effects on their biological communities, potentially reducing important ecosystem services and functions provided to wildlife and humans. In this dissertation, I examine how environmental variables, human activities, and management practices have affected stream and wetland biota throughout Northern California. The parasitic trematode Ribeiroia ondatrae has been shown to cause limb malformations in amphibian species through laboratory studies, but these small-scale experiments lacked important ecological co-factors that could alter parasite transmission rates and host susceptibility. Therefore, I conducted a multi-year, nested experiment at Hog Lake in Mendocino County to test host responses to Ribeiroia infection. The addition of Ribeiroia-infected snails to half of Hog Lake caused an increase in severe limb malformations in Pacific chorus frogs (Pseudacris regilla) and monitoring at different spatial scales revealed unique dose-response relationships because of ecological interactions and environmental co-factors. To determine if the parasite might contribute to population declines, I monitored juvenile and adult P. regilla at Hog Lake and a second wetland for four years. The consistently low (< 5%) malformation prevalence in adult frogs despite a generally high malformation prevalence (30-50%) in juvenile frogs confirmed that malformed amphibians do not survive to adulthood, indirect evidence that Ribeiroia may cause population declines. Multi-year surveys at 17 Northern California wetlands showed a strong dose-response relationship among the parasite and P. regilla malformation levels, providing evidence that Ribeiroia is an important cause of limb malformations in this region. Effective conservation of wetland species depends on understanding how anthropogenic stress, natural environmental variables, and management activities affect biological communities. To identify which of these explanatory variables were most influential and determine the conservation value of created wetlands, I sampled amphibians and insects from a total of 49 stormwater ponds, stockponds, and natural ponds in Northern California. Overall, landscape variables (i.e., percent urban and natural, number of ponds within 1 km, and elevation) were associated with differences in macroinvertebrate community structure, but specific conductance and percent littoral vegetation present were important co-factors. Compared to natural ponds, stockponds supported the most similar invertebrate assemblages and greater amphibian species richness. Light cattle-grazing of areas surrounding natural ponds and stockponds was associated 1 with increased amphibian richness, whereas the addition of exotic fishes was associated with mild differences in invertebrate populations. This research showed that stockponds are conservation resources for amphibians and invertebrates but that proper management is necessary to maximize this potential. To objectively quantify the ambient condition of wetlands, ecologists use the plants and animals found in aquatic habitats as biological indicators. Because no biological indicator has been developed for wetlands in California, I designed an index of biotic integrity (IBI) to determine the ecological condition of the wetland based on macroinvertebrate community structure. Eight metrics that showed significant responses to urbanization, had adequate range, and lacked redundancy with each other were incorporated into the IBI. The IBI was successfully validated and showed no bias along natural gradients (e.g., ecoregion, elevation, and precipitation), except that non-perennial and perennial ponds did support slightly different communities, indicating that the IBI is applicable across this region. Although biomonitoring data have been successfully used to quantity the ecological condition of perennial streams in many regions of California, no analysis tool (e.g., IBI) has been developed for the San Francisco Bay Area, a region which contains a large proportion of non- perennial streams. To identify least-disturbed reference sites in a highly urban region and examine how inter-site and temporal variability affect bioassessment data, I analyzed a large (> 400 sites) stream bioassessment dataset. I found that using geographic information system (GIS) watershed analysis and local physical habitat data were both necessary to identify least- disturbed reference sites. Among reference sites, the macroinvertebrate assemblages of perennial streams were different from non-perennial streams, a result which demonstrates the need for separate IBIs for these two habitat types. Interannual variability was moderate across 2000 to 2007, with index scores ranging from 10-15 out of 100 points, but some sites showed extreme variation of more than 50 points. In summary, this dissertation shows that effective management of wetlands and streams can be accomplished with the use of biomonitoring data to infer ecological condition and that stockponds are valuable conservation resources when properly managed. 2 TABLE OF CONTENTS Table of contents.............................................................................................................................. i Acknowledgments........................................................................................................................... ii Introduction.................................................................................................................................... iv CHAPTER 1: A practical guide for the study of malformed amphibians and their causes ................1 CHAPTER 2: Beyond laboratory experiments: Using an ecosystem-level manipulation to understand host-parasite dynamics ....................................................................................31 CHAPTER 3: Macroinvertebrate and amphibian assemblages in stormwater ponds, stockponds, and natural ponds in Northern California: The conservation value of created wetlands...68 CHAPTER 4: Development and validation of a macroinvertebrate index of biotic integrity (IBI) for assessing urban impacts to Northern California freshwater wetlands .............................100 CHAPTER 5: Identifying reference sites and quantifying biological variability within the benthic macroinvertebrate community at Northern California streams .......................................138 CHAPTER 6: Conclusions and future research..............................................................................168 i ACKNOWLEDGMENTS I would have not been able to complete this dissertation without the help of many individuals. First and foremost, I want to thank my advisor, Vince Resh. He has been a superb mentor during my tenure at UC Berkeley. His encouragement and support were invaluable in helping me write this dissertation. He allowed me the freedom to explore my ideas and provided the emotional, intellectual, and financial support I needed to complete this research. His dedication to teaching and mentoring undergraduate and graduate students was an inspiration. I would also like to thank my orals committee members Joe McBride (chair), Bob Lane, Adina Merenlender and Matt Kondolf for guiding me to important papers in their respective fields and helping me develop my prospectus, which formed the basis of this dissertation research. I want to thank my dissertation committee members Adina Merenlender and Matt Kondolf for providing valuable feedback on my dissertation chapters. I thank my long-time colleague and friend Pieter Johnson (University of Colorado Boulder) for his intellectual involvement with Chapters 1 and 2. His advice and encouragement were an immense help during graduate school. I am indebted to many Resh Lab graduate students for their support, advice, and friendship. I thank Leah Béche for being a role model when I started graduate school, Rafi Mazor for his statistical advice and encouragement to delve further into the data, Tina Mendez for being a “big sister”, Chris Solek for helping me apply the results of my dissertation, Matt Cover for getting me hooked on bioassessment research and for connecting me with the Water Board Surface Water Ambient Monitoring Program, Alison Purcell for teaching me ordination methods to analyze biomonitoring data, Wendy Renz for her insights on vernal pool and pond ecosystems, Kaua Fraiola for his infectious excitement about ecology and his company, Joanie Ball for her assistance with GIS analyses, Justin Lawrence for our research collaborations, and Lisa Hunt for sharing her knowledge regarding how science work in the real world. I also thank “honorary”