Skip to main content
Article thumbnail
Location of Repository

Studies Investigating the Outcome of a Host-Parasite Interaction Using the Stickleback-Schistocephalus Model System

By Vicki Macnab

Abstract

This thesis firstly investigates the effect of the cestode parasite Schistocephalus solidus on the reproduction of its intermediate host, the three spined stickleback. The results indicated that the parasite reduced host reproduction and the physiological basis behind this was established. In males, parasite infection reduced the fish’s ability to produce 11-ketotestosterone which resulted in reduced reproductive behaviour and sexual development. In infected females, vitellogenin production was reduced which prevented egg maturation. The adaptive nature of these changes seemed to be variable among different populations. This variation may result from genetic differences in the host or parasite population, co-evolutionary processes or reflect differences in the environmental conditions experienced by populations. \ud The second part of this thesis investigates the effect of two types of anthropogenic stressors – endocrine disrupting chemicals and temperature change as an outcome of global climate change – on disease progression in the stickleback-Schistocephalus system. The results indicated that the natural steroid 17β estradiol (E2) had a significant impact on disease progression in a sex and dose dependent manner, with males exposed to the high 100ngLˉ¹ E2 treatment harbouring significantly larger parasites compared to females in this treatment and fish from the lower E2 and solvent control treatment. Elevated temperatures were also found to significantly increase parasite growth and reduce host growth. In addition, a behavioural study showed that fish harbouring infective parasites seek out high temperatures which could be adaptive on the part of the parasite as it would allow them to grow faster and potentially increase their reproductive output. \ud The clear outcome of this thesis is that anthropogenic stressors increase disease progression in the stickleback-Schistocephalus system and this is likely to lead to reduced host reproduction and increased parasite transmission and reproduction, potentially leading to the evolution of higher virulence in this host-parasite interaction

Publisher: University of Leicester
Year: 2012
OAI identifier: oai:lra.le.ac.uk:2381/10178

Suggested articles

Citations

  1. (1984). A Functional Biology of Sticklebacks,
  2. (1997). A non-invasive morphometric technique for estimating cestode plerocercoid burden in small freshwater fish.
  3. (1980). Abnormal expression of secondary sex characters in a population of mosquitofish, Gambusia affinis holbrooki: Evidence for environmentally-induced masculinisation.
  4. (2005). Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals.
  5. (1995). Adaptive'' changes in the behaviour of parasitized animals: A critical review.
  6. (2000). Alligators and endocrine disrupting contaminants: A current perspective.
  7. (2001). Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants.
  8. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts.
  9. (1999). An 11-ketotestosterone induced kidney-secreted protein: the nest building glue from male three-spined stickleback, Gasterosteus aculeatus.
  10. (1953). An analysis of the parental behaviour of the male threespined stickleback (Gasterosteus aculeatus L.). Behaviour, Suppplement III.
  11. (2002). An assessment of in vitro androgenic activity and the identification of environmental androgens in United Kingdom estuaries.
  12. (2004). An endocrine disrupter increases growth and risky behavior in threespined stickleback (Gasterosteus aculeatus).
  13. (2007). An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks.
  14. (2002). Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus I. - Changes in 11-ketotestosterone levels during the nesting cycle.
  15. (2002). Androgen and Behavior in the male three-spined stickleback, Gasterosteus aculeatus II. Castration and 11-ketoandrostenedione effects on courtship and parental care during the nesting cycle.
  16. (2004). Androgen levels and energy metabolism in Oreochromis mossambicus.
  17. (1994). Androgens in teleost fishes.
  18. (2007). Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas).
  19. (2002). Bateman's principle and immunity.
  20. (1983). Behavioral effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the 3-spined stickleback, Gasterosteus aculeatus L.
  21. (1997). Behavioural defence. IN
  22. (1994). Behavioural defense against parasites: interaction with parasite invasiveness.
  23. (2010). Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit?
  24. (2010). Behavioural thermoregulation in two freshwater fish species.
  25. (2004). Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus.
  26. (1996). Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection.
  27. (2009). Can Myxosporean parasites compromise fish and amphibian reproduction?
  28. (2010). Castration of Female Ninespine Stickleback by the Pseudophyllidean Cestode Schistocephalus pungitii: Evolutionary Significance and Underlying Mechanism.
  29. Chemical fractionation and in vitro biological screening.
  30. (2009). Chronic Dietary Exposure to a Low-Dose Mixture of Genistein and Vinclozolin Modifies the Reproductive Axis, Testis Transcriptome, and Fertility. Environmental Health Perspectives,
  31. (2001). Climate Change
  32. (2003). Climate change and decreasing herbicide persistence.
  33. (2010). Climate change and freshwater ecosystems: impacts across multiple levels of organization.
  34. (2006). Climate change and human health: present and future risks.
  35. (2003). Climate Change and Human Health. Risks and Responses. Geneva, World Health Organization.
  36. (2005). Climate change and the recent emergence of bluetongue in Europe.
  37. (2001). Clonal variation and covariation in aphid resistance to parasitoids and a pathogen.
  38. (1982). Coevolution of hosts and parasites.
  39. (2007). Collapse of a fish population after exposure to a synthetic estrogen.
  40. (2007). Combined effects of herbicides on biomarkers reflecting immune-endocrine interactions in goldfish immune and antioxidant effects.
  41. (2011). Combined effects of parasites and contaminants on animal health: parasites do matter.
  42. (1968). Comparative fine structure of outer tegument of Ligula intestinalis and Schistocephalus solidus.
  43. (2006). Comparison of response to 17 beta-estradiol and 17 beta-trenbolone among three small fish species.
  44. (2005). Concentrationdependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata).
  45. (2000). Concentrations of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometra ovata (Nematoda) compared to some their hosts (Osteichthyes).
  46. (1995). Condition factor and hepatosomatic index as estimates of energy status
  47. (1999). Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome hostparasite system.
  48. (1995). Costs of allogrooming in impala: distraction from vigilance.
  49. (1997). Current evidence for self-medication in primates: A multidisciplinary perspective.
  50. (2004). Cytokines and steroidogenesis.
  51. (2003). Cytokines and the immune-testicular axis.
  52. (2001). Decrease of psychomotor performance in subjects with latent 'asymptomatic' toxoplasmosis.
  53. (2006). Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect?
  54. (2006). Dehydroepiandrosterone decreases while cortisol increases in vitro growth and viability of Entamoeba histolytica.
  55. (2002). Detection of environmental androgens: A novel method based on enzyme-linked immunosorbent assay of spiggin, the stickleback (Gasterosteus aculeatus) glue protein.
  56. (1993). Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental Health Perspectives,
  57. (2004). Diclofenac residues as the cause of vulture population decline in Pakistan.
  58. (2007). Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks.
  59. (1998). Different carotenoids and potential information content of red coloration of male three-spined stickleback.
  60. (1999). Direct manipulation of insect reproduction by agents of parasite origin.
  61. (2002). Disruption of male reproductive behavior in threespine stickleback Gasterosteus aculeatus exposed to 17 beta-estradiol.
  62. (2010). Disruption of the Steroid Metabolome in Fish Caused by Exposure to the Environmental Estrogen 17 alpha-Ethinylestradiol.
  63. (2011). Distinct Lineages of Schistocephalus Parasites in Threespine and Ninespine Stickleback Hosts Revealed by DNA Sequence Analysis. Plos One,
  64. (2000). DNA sex identification in the three-spined stickleback.
  65. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?
  66. (1996). Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? An experimental analysis of behavioural resistance.
  67. (2002). Ecology - Climate warming and disease risks for terrestrial and marine biota.
  68. (2008). Ecosystem consequences of fish parasites.
  69. (1994). Ectoparasite affects choice and use of roost sites in the great tit, Parus major
  70. (2001). Effect of 17 beta-estradiol, o,p '-DDT, octylphenol and p,p '-DDE on gonadal development and liver and kidney pathology in juvenile male summer flounder (Paralichthys dentatus).
  71. (2009). Effect of 17-beta-estradiol on the immunocompetence of Japanese sea bass (Lateolabrax japonicus).
  72. (2004). Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity.
  73. (1977). Effect of parasitism on toxicity of cadmium to 3-spined stickleback, Gasterosteus-aculeatus L.
  74. (2004). Effect of the cestode macroparasite Schistocephalus pungitii on the reproductive success of ninespine stickleback, Pungitius pungitius.
  75. (1994). Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus.
  76. (1993). Effectiveness of several androgens in stimulating kidney hypertrophy, a secondary sexual character, in castrated male 3-spined sticklebacks, Gasterosteus aculeatus.
  77. (1987). Effects of a cestode (Schistocephalus sp.) on the response of ninespine sticklebacks (Pungitius pungitius) to aquatic hypoxia
  78. (2001). Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus.
  79. (2004). Effects of high doses of cortisol on innate cellular immune response of seabream (Sparus aurata L.). General and Comparative Endocrinology,
  80. (2000). Effects of parasites on fish behaviour: a review and evolutionary perspective.
  81. (2007). Effects of pollution and parasites on biomarkers of fish health in spottail shiners Notropis hudsonius (Clinton).
  82. (2001). Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus.
  83. (2001). Effects of stress on fish reproduction, gamete quality, and progeny.
  84. (1968). Effects of the plerocercoid larva of a pseudophyllidean cestode, Ligula intestinalis, on the pituitary gland and gonads of its host.
  85. (1986). Electrophoretic polymorphism and sexual dimorphism in the freshwater and anadromous threespine sticklebacks (Gasterosteus aculeatus) of the Little Cambell River, British Columbia.
  86. (2005). Endocrine disrupters in the aquatic environment: An overview.
  87. (2006). Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus L.
  88. (2010). Endocrine effects of the tapeworm Ligula intestinalis in its teleost host, the roach (Rutilus rutilus).
  89. (1997). Environmental antiandrogens: Developmental effects, molecular mechanisms, and clinical implications.
  90. (2010). Environmental causes of cancer: endocrine disruptors as carcinogens.
  91. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution.
  92. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment?
  93. (1994). Estradiol increases susceptibility of goldfish to Trypanosoma-danilewskyi. Developmental and Comparative Immunology,
  94. (2010). Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific.
  95. (2010). Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries.
  96. (1994). Estrogenic effects of effluents from sewage treatment works.
  97. (2008). Evidence of temperature-dependent effects on the estrogenic response of fish: implications with regard to climate change.
  98. (2007). Evolutionary Ecology of Parasites,
  99. (2005). Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle.
  100. (2010). Evolutionary significance of fecundity reduction in threespine stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus.
  101. (1993). Exploitation of cold temperature as defense against parasitoids in bumblebees.
  102. (2009). Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda).
  103. (2001). Family origin and the response of threespine stickleback, Gasterosteus aculeatus, to thermal acclimation.
  104. (2000). Fatal attraction in rats infected with Toxoplasma gondii.
  105. (2001). Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism.
  106. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitised males.
  107. (2001). Fifteen-spined stickleback (Spinachia spinachia) females prefer males with more secretional threads in their nests: an honestcondition display by males.
  108. (2011). Fish Sexual Development Test (FSDT), Test guideline no TG234, Guidelines for testing chemicals. OECD,
  109. (2004). Fishes: an introduction to ichthyology,
  110. (2006). Fitness consequences of selfing and outcrossing in the cestode Schistocephalus solidus.
  111. (1993). Further observations of the use of the medicinal plant, Veronia amygdalina (Del), by a wild chimpanzee, its possible effect on parasite load, and its phytochemistry.
  112. (2007). Gene expression responses of European flounder (Platichthys flesus) to 17-beta estradiol.
  113. (1996). Geochemistry and clay mineralogy of termite mound soil and the role of geophagy in chimpanzees of the Mahale Mountains,
  114. (1997). Haemolymph from female beetles infected with Hymenolepis diminuta metacestodes retards the development of ovarian follicles in recipient Tenebrio molitor (Coleoptera).
  115. (2007). Health impacts of estrogens in the environment, considering complex mixture effects. Environmental Health Perspectives,
  116. (1995). Hematocrit in oxygen transport and swimming in rainbow trout (Oncorhynchus mykiss).
  117. (1982). Heritable true fitness and bright birds - a role for parasites.
  118. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection.
  119. (2004). Hormonal control of male reproductive behaviour in fishes: A stickleback perspective.
  120. (2007). Hormonal Control of Reproductive Behaviour in the Stickleback.
  121. (1997). Host - parasite evolution.
  122. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in
  123. (1985). Host life history variation in response to parasitism.
  124. (2010). Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus.
  125. (2007). Host-parasite interactions from an ecotoxicological perspective.
  126. (2008). Host-parasite interactions in polluted environments.
  127. (2007). Host-Parasite Interactions of the Three-Spined Stickleback.
  128. (2002). Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness.
  129. (1999). How environmental stress affects the impacts of parasites.
  130. (2003). How should environmental stress affect the population dynamics of disease?
  131. (1994). Identification and partial characterization of the proteases from different developmental stages of Schistocephalus solidus
  132. (1998). Identification of estrogenic chemicals
  133. (1998). Identification of estrogenic chemicals in STW effluent.
  134. (2008). Immune activation suppresses plasma testosterone level: a meta-analysis.
  135. (2009). Immunity in a variable world.
  136. (2005). Immunobiology: the immune system in health and disease.
  137. (2005). Impact of regional climate change on human health.
  138. (2008). Impacts of climate warming on terrestrial ectotherms across latitude.
  139. (1992). Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs and mercury.
  140. (2007). Impaired reproduction in three-spined sticklebacks exposed to ethinyl estradiol as juveniles.
  141. (2007). Implications of research on endocrine disruption for the environmental risk assessment, regulation and monitoring of chemicals in the European Union. Environmental Pollution,
  142. (2002). In vitro and in vivo effects of 17 beta-trenbolone: A feedlot effluent contaminant.
  143. (2001). In vitro effects of hypothalamicpituitary-adrenal axis (HPA) hormones on Schistosoma mansoni.
  144. (2001). In vivo testing system for determining the estrogenic activity of endocrine-disrupting chemicals (EDCs) in goldfish (Carassius auratus).
  145. (2001). Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections.
  146. (1967). Infections of the three spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects.
  147. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda, Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus.
  148. (1994). Influence of chronic toxoplasmosis on some human personality factors.
  149. (1993). Influence of oral-administration of estradiol-17β and testosterone on growth, digestion, food conversion and metabolism in the underyearling red sea bream,
  150. (1971). Influence of Schistocephalus plerocercoids on respiration of Gasterosteus and a possible resulting effect on behaviour of fish.
  151. (2010). Influence of simulated climate change and eutrophication on three-spined stickleback populations: a large scale mesocosm experiment.
  152. (2011). Inhibition of gametogenesis by the cestode Ligula intestinalis in roach (Rutilus rutilus) is attenuated under laboratory conditions.
  153. (1979). Integrating thermal physiology and ecology of ectotherms - discussion of approaches.
  154. (2010). Interactions between effects of environmental chemicals and natural stressors: A review.
  155. (2010). Interactions between parasites and pollutants in yellow perch (Perca flavescens) in the St. Lawrence River, Canada: implications for resistance and tolerance to parasites.
  156. (1999). Interactions between the immune system and the hypothalamo-pituitaryinterrenal axis in fish.
  157. (2008). Intercalibration exercise using a stickleback endocrine disrupter screening assay.
  158. (1994). Introduction to Animal Parasitology, London,
  159. (1989). Investigations on the occurence of pinocytosis in the tegument of Schistocephalus solidus.
  160. (1996). Leaf-swallowing by chimpanzees: A behavioral adaptation for the control of strongyle nematode infections.
  161. (2010). Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model?
  162. (1997). Ligula intestinalis: Interactions with the pituitary-gonadal axis of its fish host.
  163. (2006). Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum.
  164. (2004). Longterm exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environmental Health Perspectives,
  165. (2004). Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks.
  166. (1998). Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.).
  167. (1996). Male reproductive health and environmental xenoestrogens. Environmental Health Perspectives,
  168. (2008). Male three-spined sticklebacks Gasterosteus aculeatus make antibiotic nests: a novel form of parental protection?
  169. (2001). Masculinization of female mosquitofish in kraft mill effluent-contaminated Fenholloway River water is associated with androgen receptor agonist activity.
  170. (1975). Mate selection - selection for a handicap.
  171. (1975). Membrane-transport in helminth parasites -review.
  172. (2009). Metabolic depression and spleen and liver enlargement in juvenile Arctic charr Salvelinus alpinus exposed to chronic parasite infection.
  173. (2002). Modulation of goldfish testicular testosterone production in vitro by tumor necrosis factor alpha, interleukin-1 beta, and macrophage conditioned media.
  174. (2004). Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus.
  175. (2004). Molecular mechanisms involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps.
  176. (2006). Multiple anthropogenic stressors cause ecological surprises in boreal lakes.
  177. (2000). Natural selection and parallel speciation in sympatric sticklebacks.
  178. (2010). Naturally-induced endocrine disruption by the parasite Ligula intestinalis (Cestoda) in roach (Rutilus rutilus).
  179. (2006). Nesting, courtship and kidney hypertrophy in Schistocephalus-infected male three-spined stickleback from an upland lake.
  180. (2002). Next remarks to the knowledge of heavy metal concentrations in gravid tapeworm species parasitizing aquatic birds.
  181. (2001). No effect of a parasite on reproduction in stickleback males: a laboratory artefact?
  182. (1989). Observations on the iIlness and consumption of a possibly medicinal plant Veronia amygdalina (DEL.), by a Wild Chimpanzee in the Mahale Mountains National Park,
  183. (2010). Occurrence, fate, and biodegradation of estrogens in sewage and manure.
  184. (2002). P=0.031; Figure 3.4.e), but this 3.3.3. Comparison of lab bred and wild caught Carsington Reservoir
  185. (2011). Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes.
  186. (2005). Parasite regulation by host hormones: an old mechanism of host exploitation? Trends in Parasitology,
  187. (2003). Parasite selection for immunogenetic optimality.
  188. (1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific.
  189. (1996). Parasite-induced changes in the behaviour of cestodeinfected beetles: Adaptation or simple pathology?
  190. (2010). Parasites and global warming: net effects of temperature on an intertidal host-parasite system.
  191. (2002). Parasites and the Behavior of Animals,
  192. (2006). Parasites dominate food web links.
  193. (2005). Parasites grow larger in faster growing fish hosts.
  194. (1992). Parasites, bright males, and the immunocompetence handicap.
  195. (2009). Parasitic castration: the evolution and ecology of body snatchers.
  196. (2005). Parasitic manipulation: where are we and where should we go?
  197. (2005). Parasitism in fish - an endocrine modulator of ecological relevance?
  198. (1990). Parasitism in marine fish after chronic exposure to petroleumhydrocarbons in the laboratory and to the exxon valdez oil-spill.
  199. (2011). Parasitized snails take the heat: a case of host manipulation? Oecologia, Published online ahead of press.
  200. (1999). Parental energy expenditure of the male threespined stickleback.
  201. (2006). Perchlorate induces hermaphroditism in threespine sticklebacks.
  202. (1994). Physiological bases for parasiteinduced alterations of host behaviour.
  203. (1994). Physiological ecology and evolution of the threespine stickleback. IN
  204. (2006). Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission.
  205. (1987). Pollution and parasitism in the aqautic environment.
  206. (1999). Pomphorhynchus laevis: The intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus).
  207. (2009). Protecting aquatic organisms from chemicals: the harsh realities.
  208. (1971). Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus.
  209. (2007). Rapid bioconcentration of steroids in the plasma of three-spined stickleback Gasterosteus aculeatus exposed to waterborne testosterone and 17 beta-oestradiol.
  210. (2003). Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite.
  211. (2007). Reproductive Behaviour in the Three-Spined Stickleback.
  212. (2007). Reproductive Physiology of Sticklebacks.
  213. (1997). Review: Are the classical hematological variables acceptable indicators of fish health?
  214. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food
  215. (2011). Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex.
  216. (1978). Schistocephalus solidus - Pinocytosis by plercocercoid tegument.
  217. (1981). Schistocephalus solidus and Ligula intestinalis - Pinocytosis by the tegument.
  218. (2007). Schistocephalus solidus: Establishment of tapeworms in sticklebacks - fast food or fast lane? Experimental Parasitology,
  219. (2006). Seasonal changes in expression of LH-beta and FSH-beta in male and female three-spined stickleback, Gasterosteus aculeatus.
  220. (1980). Seasonal variations in plasma concentrations of 11 Ketotestosterone and testosterone in male rainbow trout, Salmo gairdnerii Richardson.
  221. (2001). Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees.
  222. (2010). Self-Medication: Passive Prevention and Active Treatment.
  223. (2003). Sequencing the genome of threespine sticklebacks (Gasterosteus aculeatus).
  224. (1996). Sex differences in parasite infections: Patterns and processes.
  225. (1990). Sexual reproduction as an adaptation to resist parasites (a review).
  226. (1989). Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.).
  227. (1983). Some effects of the cestode (Schistocephalus-solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus), evolutionary aspects of a host-parasite interaction.
  228. (2007). Spiggin levels are reduced in male sticklebacks infected with Schistocephalus solidus.
  229. (2000). Split-clutch IVF: A technique to examine indirect fitness consequences of mate preferences in sticklebacks.
  230. (2003). Steroid estrogens profiles along river stretches arising from sewage treatment works discharges.
  231. (1987). Stimulation of reproductive behaviour by aromatizable and nonaromatizable androgens in the male three-spined stickleback, Gasterosteus aculeatus L.
  232. (1989). Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus-tshawytscha).
  233. (1967). Studies on Schistocephalus solidus. 4. The effect of temperature on growth and maturation in vitro.
  234. (1946). Studies on tapeworm physiology. I. The cultivation of Schistocephalus solidus in vitro.
  235. (1954). Studies on tapeworm physiology. VII. Fertilization of Schistocephalus solidus in vitro.
  236. (2007). Summary for policymakers. IN
  237. (2011). Suppressed monocyte gene expression profile in men versus women with PTSD.
  238. (2002). Suppression in function of phagocytic cells in common carp Cyprinus carpio L. injected with estradiol, progesterone or 11-ketotestosterone.
  239. (2007). Suppression of aromatase activity in populations of bream (Abramis brama) from the river Elbe,
  240. (2005). Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: Individual variation and fitness consequences.
  241. (2000). Survival for immunity: The price of immune system activation for bumblebee workers.
  242. (2007). Sympatric and allopatric combinations of sticklebacks and the tapeworm Schistocephalus solidus -mutual adaptations of hosts and parasites.
  243. (2002). Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature?
  244. (2008). Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna.
  245. (2003). Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment.
  246. (2002). Temperature dependent activation of leucocyte populations of rainbow trout, Oncorhynchus mykiss, after intraperitoneal immunisation with Aeromonas salmonicida.
  247. (2005). Temperature effects on acute copper toxicity to juvenile channel catfish Ictalurus punctatus.
  248. (2004). Testicular dysgenesis syndrome: new epidemiological evidence.
  249. (1976). The Biology of the Sticklebacks,
  250. (1993). The breeding coloration of male 3 spined sticklebacks (Gasterosteus aculeatus) as and inidcator of energy investment in vigor.
  251. (2011). The cost of a bodyguard. Biology Letters, Published online ahead of press.
  252. (2009). The ecological significance of manipulative parasites.
  253. (1982). The effect of ration and temperature on the growth of the 3-spined stickleback, Gasterosteus-aculeatus L.
  254. (2011). The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review.
  255. (1997). The effects of pollutants on the immune response of fish: Implications for helminth parasites.
  256. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis.
  257. (1996). The evolution of parasitic diseases.
  258. (1999). The evolution of trophic transmission.
  259. (2004). The evolution of virulence when parasites cause host castration and gigantism.
  260. (1994). The Evolutionary Biology of the Threespine Stickleback,
  261. (1952). The food of the cormorant in the Netherlands.
  262. (2000). The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field.
  263. (1980). The immune-system of cyprinid fish. Kinetics and temperature dependence of antibody-producing cells in carp (Cyprinus carpio).
  264. (2011). The impact of environmental change on host-parasite coevolutionary dynamics.
  265. (2002). The impact of oestrogenic and androgenic contamination on marine organisms in the United Kingdom -summary of the EDMAR programme.
  266. (1997). The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus.
  267. (2004). The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption - II -kidney hypertrophy, vitellogenin and spiggin induction.
  268. (2004). The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome.
  269. (2008). The model anti-androgen flutamide suppresses the expression of typical male stickleback reproductive behaviour.
  270. (1999). The morphology of the immune system in teleost fishes.
  271. (2009). The organophosphorous pesticide, fenitrothion, acts as an anti-androgen and alters reproductive behavior of the male three-spined stickleback, Gasterosteus aculeatus.
  272. (1969). The physiology of cestodes,
  273. (2002). The potential of the threespined stickleback (Gasterosteus aculeatus L.) as a combined biomarker for oestrogens and androgens in European waters.
  274. (1974). The regulation of egg yolk protein synthesis by steroid hormones.
  275. (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behaviour of its intermediate host, the 3-spined stickleback, Gasterosteus aculeatus.
  276. (2008). The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction.
  277. (1997). The stress response in fish.
  278. (2005). The tapeworm Ligula intestinalis (Cestoda : Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus.
  279. (2009). The toxicology of climate change: Environmental contaminants in a warming world.
  280. (2007). The Use of the Stickleback as a Sentinel and Model Species in Ecotoxicology.
  281. (2000). The use of the threespined stickleback as a potential biomarker for androgenic xenobiotics.
  282. (2003). Thermal biology in insect-parasite interactions.
  283. (1995). Thermal ecology of a malarial parasite and its insect vector: consequences for the parasites transmission success.
  284. (2008). Thermal tolerance, acclimatory capacity and vulnerability to global climate change.
  285. (2007). Three-Spined Stickleback: an Emerging Model in Environmental Endocrine Disruption.
  286. (1992). Toxic pollution and parasitism in fresh-water fish.
  287. (1985). Use of nest material as insecticidal and antipathogenic agents by the European Starling.
  288. (2006). Use of the three-spined stickleback (Gasterosteus aculeatus) as a sensitive in vivo test for detection of environmental antiandrogens.
  289. (2003). Variation in immune defence as a question of evolutionary ecology.
  290. (1995). Vitellogenesis as a biomarker for estrogenic contamination of the aqautic environment. Environmental Health Perspectives,
  291. (2008). Vitellogenin Functions as a Multivalent Pattern Recognition Receptor with an Opsonic Activity. Plos One,
  292. (2001). Vitellogenininduced pathology in male summer flounder (Paralichthys dentatus).
  293. (2005). Water-seeking behavior in insects harboring hairworms: should the host collaborate?
  294. (2004). When synthetic chemicals degrade in the environment.
  295. (2007). Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host.
  296. (2006). Widespread amphibian extinctions from epidemic disease driven by global warming.
  297. (1998). Widespread sexual disruption in wild fish.

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.