Avian conservation studies frequently evaluate the effects of anthropogenic factors like disturbance, habitat destruction, edge effects and environmental contamination. Hostparasite interactions are an often-overlooked aspect of avian conservation studies, despite the fact that parasites have the ability to dramatically affect host populations. The history of common loon (Gavia immer) conservation work has borne this out â many studies document the negative effects disturbance, habitat destruction and mercury have on loons, yet little is known about loon black fly parasites and nothing is known about loon blood parasites. I conducted a study to investigate the effects loon parasites have on nest success by testing the specificity of a black fly species, Simulium annulus, to the common loon, and by examining the haemosporidian fauna of loons. A series of bird decoys were presented on northern Wisconsin lakes to test the specificity of S. annulus to the common loon and to explore the importance of chemical and visual cues used for black fly host attraction. These tests revealed that S. annulus is a highly specific parasite of the common loon and that chemical cues are of significant importance in attracting black flies. Blood was collected from breeding loon pairs and their chicks to describe and examine the blood parasite fauna of a population of breeding loons. The genera Leucocytozoon and Plasmodium were successfully detected in loons using PCR techniques. Furthermore, both the presence and the intensity of Leucocytozoon infection in adult loons were significantly explained by loon blood mercury levels. These studies provide a detailed description of various loon parasites and show that mercury may be immuno-compromising these birds.
TABLE OF CONTENTS List of Tables vii List of Figures viii Introduction to Loon Biology 1 Reproduction 2 Chick-rearing 3 Lifespan 3 Populations 4 Diet 4 Parasites 5 Chapter One: Testing the Specificity of Simulium annulus to the Common Loon 6 Introduction 6 Black Fly Ecology 6 Black Fly Effects on Bird Species 8 The Specificity of Simulium annulus to the Common Loon. 10 Simulium annulus Ecology 11 Methods 11 âOne-wingâ Presentations 12 âThree-wingâ Presentations 13 Data Collection 15 Statistical Analyses 16 Results 17 Discussion 22 Chapter Two: Haemosporidians, Mercury, and the Common Loon Immune Response 27 Introduction 27 Haemotozoans and Avian Reproductive Ecology 27 Avian Haemosporidian Surveys 28 Leucocytozoon Ecology 29 Haemoproteus Ecology 33 Plasmodium Ecology 34 Mercury and its Effects 36 Immune Function 37 Molecular Genetic Detection of Haemosporidians 38 Methods 39 Blood Collection and Analyses 39 DNA Analyses 40 Detectability and Repeatability 43 Statistical Analyses 44 Results 45 Discussion 53 Conclusion 60 Literature Cited 61 Appendices 66
INTRODUCTION TO LOON BIOLOGY Common loons (Gavia immer) are top-level piscivores of nearctic lacustrine habitats, and loon populations are often monitored as indicators of overall habitat quality. Loon reproduction is notably affected by human disturbance, habitat modification, predation, nest abandonment and fluctuating water levels (McIntyre 1988, personal observation), yet variability in nesting success remains partially unexplained. Historically it was common for ecologists and ornithologists to overlook the impact parasites have on bird demographics principally because parasites were viewed as âbenign symbiontsâ (Hudson and Dobson 1997). Yet both empirical data (Hudson et al. 1998) and population models (Anderson and May 1978) indicate that parasites can radically affect host population dynamics. Storer (2002) examined metazoan parasites of loons and explored the relationship of this parasite fauna to the loonâs evolutionary history and biology, but noted that there has been little attention paid to the influence black fly or haemosporidian parasites have on loon reproduction and ecology. In this thesis I will present field and laboratory studies performed to explore the relationships between common loons and their black fly (Diptera: Simuliidae) and haemosporidian (Protista: Haemosporida) parasites. Chapter one focuses on the proposed specificity of a black fly species, Simulium annulus, to the common loon, and investigates the cues that are important for black fly host attraction. Chapter two examines the detection and prevalence of loon haemosporidians that are known to be transmitted by black flies, and discusses the implications of haemosporidian infection. The loon immune response and the effects of blood mercury burdens are also discussed in relation to haemosporidian infection. 2 This introduction serves to provide background information on common loon ecology that will be relevant in the subsequent chapters. Common loons are migratory birds that breed in freshwater northern temperate forest lakes throughout Canada and the northern United States during the summer months, and inhabit coastal salt water habitats in the winter (McIntyre and Barr 1997). It has been speculated that young common loons stay on their wintering/non-breeding grounds until they are between four to seven years of age (McIntyre and Barr 1997) and do not return to their breeding grounds until they have reached sexual maturity. Upon return to their breeding grounds in early spring, adult common loons form monogamous pairs and defend a breeding territory throughout the summer (McIntyre 1988, Piper et al. 1997). Ideal territories are generally sheltered areas of large oligotrophic lakes or entire small lakes (McIntyre 1994, McIntyre and Barr 1997) that provide good nest sites, ample food supply and little human disturbance (McIntyre 1988). Reproduction Nesting begins in early spring (late April and early May) and nests are built predominately of mud and vegetation on small islands and wetland shorelines through July (McIntyre 1988). Loons generally lay two-egg clutches and males and females share incubation responsibilities during the approximate 28-day incubation period (McIntyre and Barr 1997). If a nest attempt fails early in the breeding season, loons will re-nest, generally in an alternate location (McIntyre 1988). Nest predation, human disturbance, fluctuating water levels, and nest abandonment have all been documented causes of nest failure (McIntyre 1988, personal observation). Black flies are common pests to loons and loons may be especially vulnerable to black fly predation during nest incubation, at times causing nest abandonment (McIntyre 3 1988). Common loon nest predators are crows (Corvus brachyrhynchos), ravens (Corvus corax), bald eagles (Haliaeetus leucocephalus), raccoons (Procyon lotor), skunks (Mephitis mephitis), mink (Mustela vison), weasels (Mustela frenata) and possibly otters (Lutra canadensis) (McIntyre and Barr 1997, Mike Meyer, Wisconsin DNR, personal communication). Chick-rearing Chicks are fed and tended to by both adults who introduce their semi-precocial young to the water within a day of hatching (McIntyre and Barr 1997). Although it varies from family to family, loon chicks are not completely independent of their parents until approximately 12 to 15 weeks of age (McIntyre and Barr 1997). It has been suggested that parenting skills improve with experience and age. Paruk et al. (2000) found that reproductive success of common loon pairs increased with an increased length of pair bond at Seney National Wildlife Refuge. Chick survival is often affected by food availability, sibling rivalry, predation, and trauma inflicted by watercraft accidents or territorial conflict (McIntyre and Barr 1997). Predators of loon chicks include large fish such as northern pike (Esox lucieus) and muskellunge (Esox masquinongy), snapping turtles (Chelydra serpentine), and bald eagles (McIntyre and Barr 1997). Lifespan There is little published data on the lifespan of the common loon and until recently, many of the longevity estimates for the species were purely speculative, spanning from 25 to 30 years (McIntyre 1988). However, an increase in long-term studies of color-marked individuals will allow the collection of more accurate data in the future. Banding and recapture efforts of the Wisconsin DNR have already discovered loons that are at least 20 years old. As this research 4 progresses, more information will be available on common loon longevity (M.W. Meyer, Wisconsin DNR, personal communication). Populations Common loon population density appears to be dependent on the amount of suitable habitat. Loons generally do not use lakes less than 10 acres (approximately 4 ha) in size for foraging or nesting due to their need for a relatively large surface area for flight initiation, (M.W. Meyer, Wisconsin DNR, personal communication). Loons aggressively defend territories for breeding, chick rearing, and foraging which limits the number of loons on any territorial lake. Lakes less than 200 acres are usually home to only one territorial pair of loons unless the shoreline is undulating and the lake is broken into distinct bays or coves in which case multiple pairs may exist (M.W. Meyer, Wisconsin DNR, personal communication). Diet Common loons are primarily piscivorous and over 30 species of fish have been documented as prey items, including brown bullhead (Ameiurus nebulosus), northern pike (Esox lucius), white sucker (Catostomus commersonii), common bluegill (Lepomis macrochirus), trout (Salmonidae), alewives (Alosa pseudoharengus), smelt (Osmeridae), sea lamprey (Petromyzon marinus), coregonid spp. (Salmonidae: Coregonus), mottled sculpin (Cottus bairdi), and yellow perch (Perca flavescens) (McIntyre 1988, Evers 1994). When fish are unavailable or conditions are unfavorable for fish capture, loons will consume crayfish (Cambarus spp.), leeches (Hirudinea), mollusks (Mollusca), caddisflies (Trichoptera), amphipods (Amphipoda), dragonfly nymphs (Odonata), and on rare occasions, vegetation (McIntyre 1988, Evers 1994). 5 Loon chicks are fed exclusively by their parents until about eight weeks of age, when they are able to capture approximately 50% of their daily food intake on their own. By week 11, chicks are capable of capturing 90-100% of their daily food (McIntyre and Barr 1997). Chicks feed primarily on small fish including minnows and perch as well as aquatic insects and crayfish (McIntyre 1988, Evers 1994). Parasites A number of internal helminths have been described in common loons including digenean trematodes (Trematoda), tapeworms (Cestoda), spiny-headed worms (Acanthocephala) and round worms (Nematoda). Blood sucking ectoparasites such as mites (Acarina), lice (Phthiraptera) and flies (Diptera), including black flies, are also parasitic on common loons (Storer 2002). However, little is known about the effects of parasitic infection in common loons, and no haematozoa have been previously described in the species.