HOST-PARASITE RELATIONSHIPS OF HELMINTHS IN A COYOTE POPULATION FROM SOUTHERN TEXAS WITH PARTICULAR REFERENCE TO THE DOG HOOKWORM by ANDREW ALAN RADOMSKI, B.S. A THESIS IN WILDLIFE SCIENCE Submitted to the Graduate Faculty of Texas Tech University In Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE Amijroved Accepted August, 1989 ec© © ANDREW A. RADOMSKI ACKNOWLEDGMENTS I would like to express my sincere appreciation to Dr. Danny B. Pence (chairman of my graduate committee, major professor, and employer), for his assistance, advice and guidance throughout my graduate program. Also, I am grateful to Dr. Stephen Demarais, Dr. Michael Willig, and Mr. Lamar Windberg for devoting their time and effort while serving on my thesis committee. Special thanks are extended to the following individuals of the Denver Wildlife Research Center for their technical support: L. A. Windberg and C. Bitler in Laredo, Texas; and F. F. Knowlton, D. Zemlicka, S. Olmstead, and S. Ebbert in Millville, Utah. Special thanks is also extended to Marianna Roetto for her assistance and dedication in animal care. Appreciation also is expressed to Lisa Bradley and Scott Henke for their editorial comments, fellow graduate students Doug Waid and Don Whittaker for their computer programming advice, and Dr. David B. Wester for his statistical advice. Lastly, I express my sincere appreciation to my parents, for a lifetime of encouragement and opportunity. 11 These studies were financially supported by the Department of Range and Wildlife Management at Texas Tech University (TTU), Department of Pathology at TTU Health Sciences Center, and the National Rifle Association of America. Ill TABLE OF CONTENTS ACKNOWLEDGMENTS ii ABSTRACT vii LIST OF TABLES xi CHAPTER I. INTRODUCTION 1 Literature Cited 9 II. NEONATAL MORTALITY OF COYOTES FROM HOOKWORM DISEASE 14 Introduction 14 Materials and Methods 17 Source of Hookworm Infection .... 17 Culture for Hookworm Larvae 18 Experimental Hosts 19 Experimental Infections 20 Data Collection and Analysis .... 22 Definitions 24 Results 24 Inoculum 24 Control Group 26 Experiment I 26 Experiment II 27 Histopathology 28 iv Survivalship 28 Discussion 32 Management Implications 39 Literature Cited 41 III. PERSISTENCE AND INTERRELATEDNESS OF RECURRENT GROUPS OF HELMINTH SPECIES IN COYOTES FROM SOUTHERN TEXAS: 1979-1987 47 Introduction 47 Study Area 53 Materials and Methods 55 Definitions 55 Collection of the Host Animals ... 57 Collection of Helminth Species ... 58 Analytical Methods 60 Results 63 The Helminth Fauna 63 Frequency Distributions of the Helminth Community 70 Recurrent Group Analysis 73 Persistence and Stability of Recurrent Group Species 82 Discussion 82 Literature Cited 89 APPENDICES A. DESCRIPTIVE STATISTICS (x ± S.E.) FOR EIGHT INTESTINAL HELMINTH SPECIES DELINEATED BY HOST SEX AND AGE 97 V B. MEASURE OF DEGREE OF AGGREGATION (Ji) IN EIGHT SPECIES OF INTESTINAL HELMINTHS DELINEATED BY HOST SEX AND AGE ^^^ C. RECURRENT GROUPS AND PAIRED RANK CORRELATIONS (KENDALL'S TAU) FOR INTESTINAL HELMINTH SPECIES COLLECTED ^^^ D. BASIC PROGRAM FAGERINDEX 125 VI ABSTRACT Prior to the development of proper management and effective control programs for coyotes (Canis latrans), general information regarding demographic data, particularly growth rates and mortality in the neonates, must be well understood. Chapter I reviews some of the current literature pertaining to natural mortality in coyotes and present control methods used on this predator. Chapter II examines certain facets of the question of whether or not a parasite can function as a mechanism to limit the population growth rate of its vertebrate host. This study was initiated to obtain additional information to support or refute the general hypothesis of coyote population regulation by hookworm disease. The specific objectives were to: (1) document the effects of hookworm infection (morbidity and mortality) on experimentally infected hand-reared coyote neonates; (2) determine if selective density-dependent pathogenicity of hookworm infection occurs in coyote neonates and, if so, obtain an estimate of hookworm densities required to cause clinical signs of morbidity and to cause mortality; and (3) determine if differential susceptibility exists among individuals within a litter. These objectives were Vll accomplished by experimentally inoculated 51 captive hand- reared coyote neonates from a captive coyote population in Utah. The strain of infective strongyliform dog hookworm (Ancylostoma caninum) larvae was cultured from the feces of a free-ranging coyote captured in southern Texas. Twenty-eight coyote neonates, 3- to 4-wk-old, were inoculated at random with 0 (control), 250, 500 or 1,500 hookworm larvae/kg body weight to establish threshold levels of mortality. Mean weight gains and hematocrit values were recorded over a 30-day study period. An initial threshold level of 250 to 500 hookworm larvae/kg was estimated to cause 50% mortality (LD50) among neonates in Experiment I. Lesions in neonates included initial pneumonitis and pulmonary consolidation as a result of larval migration, with severe hemoglobinopathy and anemia associated with localization of hookworms in the small intestine over time. Differences in susceptibility among neonates within the same litter, as well as a more accurate estimate of hookworm larvae densities required to cause morbidity and mortality, were examined in Experiment II. Differential susceptibility was observed within litters administered the same dose of hookworm larvae. A threshold level of > 300 hookworm larvae/kg was determined to be the lethal number of hookworm larvae needed to cause mortality based upon 23 neonates in 7 different litters I I I Vlll used in Experiment II. The absolute number of hookworms recovered in these experimental studies corresponded to the number of hookworms reported from naturally-infected free-ranging juvenile coyotes in southern Texas; suggesting that this infection could result in density- dependent pathogenicity in natural populations of this vertebrate host. Thus, hookworm can be considered as a potential factor in the regulation of coyote population growth rates in the in southern Texas. Chapter III examines the persistence and interrelatedness of a recurrent group of macroparasitic helminths from the small intestine in a free-ranging population of coyotes in southern Texas at 4-yr intervals (1979 to 1987), as well as across seasons (spring and fall 1979) and over a 1-yr period (fall 1986 and fall 1987). The study was designed to strengthen the data concerning the community ecology of the intestinal helminth species operating in this host population. The ^ priori hypothesis was that a stable recurrent group of helminth species persists over time and that the respective helminth species in this recurrent group are stable in terms of their frequency distributions and abundances. This hypothesis was addressed by examining the effects of the intrinsic factors of host sex and age on the population dynamics of a helminth community in coyotes ix from southern Texas. Eight species of helminths (Alaria marciana^r A. caninum. Mesocestoides lineatus. Qncicola canis. Physaloptera rara. Taenia multiceps, T. pisiformis. and Toxascaris leonina) composed the community occurring along the small intestinal gradient of coyotes in southern Texas. Computation of the Eager index and subsequent recurrent group analysis and rank correlations indicated the persistence of a small group of recurring species along with several affiliated species. These results provide information on the inter-relationships of these intestinal helminths that remain as a persistent recurrent group within coyotes in southern Texas and provides further documentation of the species that could most effect this coyote population (i.e., be an additive mortality factor in conjunction with hookworm to affect host population dynamics). X LIST OF TABLES 2.1 Pretrial test determining the quantities of hookworms to be inoculated into the coyote neonates 25 2.2 Number of hookworms recovered from coyote neonates inoculated with 200 hookworm larvae/kg of body weight in Experiment II ... 30 2.3 Number of hookworms recovered from coyote neonates inoculated with 300 hookworm larvae/kg of body weight in Experiment II ... 31 2.4 Differences in survivability within coyote litters inoculated with 200 and 300 hookworm larvae/kg in Experiment II 33 2.5 Proportion of inoculated neonates surviving based on all treatments 34 3.1 Descriptive statistics (x ± S.E.) for number of intestinal helminths collected from a coyote (Canis latrans) population in southern Texas during spring and fall 1979, and fall 1983, 1986, and 1987 64 3.2 Prevalence, intensity, and abundance of intestinal helminth species collected from coyotes (Canis latrans) in southern Texas during spring of 1979 (n = 96) 65 3.3 Prevalence, intensity, and abundance of intestinal helminth species collected from coyotes fCanis latrans) in southern Texas during fall 1979 (n = 81) 66 3.4 Prevalence, intensity, and abundance of intestinal helminth species collected from coyotes (Canis latrans) in southern Texas during fall 1983 (n = 42) 67 XI 3.5 Prevalence, intensity, and abundance of intestinal helminth species collected from coyotes (Canis latrans) in southern Texas during fall 1986 (n = 46) 68 3.6 Prevalence, intensity, and abundance of intestinal helminth species collected from coyotes (Canis latrans) in southern Texas during fall 1987 (n = 64) 69 3.7 Determination of overdispersion in eight species