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Micromammals and Macroparasites From Evolutionary Ecology to Management
Abstract
The idea for a book reviewing current knowledge on mammals and their parasites emerged during a visit by one of us (SM) to the laboratory of another of us (BK) at the Jacob Blaustein Institutes for Desert Research, Ben-
Gurion University of the Negev (Israel) in December 2004, with RP becoming associated with the project from its very beginning.
Frankly, we decided to restrict our focus to macroparasites, i.e., metazoan parasites such as helminths and arthropods. A second volume at least would be necessary to cover microparasites, i.e., viruses, bacteria, and protozoans. We also decided to restrict our scope to small (=micro) mammals, because they are the most abundant and diversified species in the order Mammalia. Moreover, most of our knowledge on the interactions between mammals and their macroparasites concerns small mammalian species, mainly rodents, but also insectivores, lagomorphs, and bats.
Our idea was to associate disciplinary fields (taxonomy, phylogenetics, physiology, genetics, ecology, evolution, conservation biology, mathematical epidemiology) that may not have enough opportunities to exchange and debate ideas. What better opportunity can there be than a book on the evolution and ecology of host–parasite interactions, and moreover, a book that focuses on and emphasizes a particular group of hosts and their parasites? A symposium on “Parasites and mammals: A macroecological perspective” (organized by BK and SM) at the 9th International Mammalogical Congress in Sapporo (Japan), held in August 2005, allowed us to
finalize the project with Springer Japan.
The book is conceived for a broad audience. Students will find up-todate reviews and state-of-the-art syntheses in several domains. We hope that they will find ideas and opportunities for new research and new applications. Senior researchers, who try to maintain themselves at the forefront of their discipline, will also be interested readers. They are forced to specialize, leaving them little time for exploring other fields, even those
closely related to their interest. This volume is organized in order that they will easily find reviews, summaries, data and references. Environmental managers, veterinarians, and conservationists have to use the results of
fundamental science for their daily tasks: evaluating different options to manage natural populations and habitats. They have to deal with and/or know that parasitism and diseases are important emerging problems. They need to have a clear picture of current knowledge, and the contributions in this book will prove invaluable.
The volume is divided into six parts, including a brief opening introduction explaining what micromammals and macroparasites are. The second part presents the major taxa that parasitize small mammals: helminths
(trematodes, cestodes, nematodes, acanthocephalans) and arthropods (ticks, mites, lice, fleas and bat flies). We did not include dipterans that are not normally considered as parasites but as blood feeders. Besides, the
main victims of dipterans are large rather than small mammals. In addition, we did not consider the chewing lice (Ischnocera, Amblycera) because they are generally understood to be commensals rather than parasites. A
review of the diversity of species, life traits and life cycles, and also of the known effects of these parasites on their hosts, is provided for each of these taxa. The third part deals with some ecological and evolutionary patterns of parasite associations: parasite species diversity, host specificity, co-speciation and co-phylogeography. The fourth part explores the processes that operate in parasite associations at both higher (populations and communities) and lower (individuals) levels of biological organization. Mathematical epidemiology, community ecology, physiology (with endocrinology, metabolism and immunology) and genetics are explored. The fifth part provides practical examples or applications of ecological concepts to management purposes: conservation biology, and the ecology of human and animal health. The volume ends with a conclusion that explores the future of host–parasite interactions in the face of global change.
... Interestingly, the observed pattern also concurs with the insular theory for small mammals (Lomolino, 1985; Laurance, 2008). In particular, the observed increase in body size that was recorded for R. pumilio supports Van Valen's rule in that smaller mammal species (< 100 g) grow larger on islands (Van Valen, 1973; Lomolino, 1985; Morand et al. 2006). Along the same lines, our study recorded higher rodent densities in some of the fragments compared to extensive natural areas. ...
... In addition, longer-lived hosts (which are generally larger in body size) favour delayed maturation to adult stages in parasites (Sorci et al. 1997). This in turn will result in a larger body size when the parasite reaches sexual maturity and higher fecundity (Sorci et al. 1997; Morand et al. 2006). In support of the latter, increased body size of adult female L. agrippinae fleas, in the present study, may be due to the production of larger eggs (Poulin and Morand, 1997), or larger egg batches (Khokhlova et al. 2009) and/or offspring (Khokhlova et al. 2010) which could all contribute to a longer body length during oviposition. ...
SUMMARY Habitat fragmentation can adversely impact biodiversity, although where remnant fragments of natural vegetation provide favourable conditions the negative effects of fragmentation may be mitigated. Host-parasite systems in fragmented areas have only recently been examined, with parasites generally showing higher prevalence and richness in fragments, mediated by changes in host density. However, the effect of fragmentation on parasite body size and fecundity remains poorly investigated. Thus, here we compared the body size and condition of a generalist rodent host, Rhabdomys pumilio and the body size of 2 common flea species between pristine natural areas and remnant fragments within agriculture areas. Host body length, weight and body condition values were significantly larger in fragments than in pristine natural vegetation. Listropsylla agrippinae fleas showed the same pattern, being significantly larger in fragments, while Chiastopsylla rossi fleas did not differ in size between fragments and natural areas. The differential response of the 2 flea species may reflect the strength of association between the host and parasite, with the former spending a greater proportion of its lifespan on the host. Therefore, in this study agriculture fragments provide better conditions for both an opportunistic rodent and a closely associated flea species.
... Metastrongylid larvae are expected to be found mostly in liver tissue in paratenic hosts and, to a lesser extent, in muscles and connective tissues [10,20,31]. Based on a field study on Varanus bengalensis infected with A. cantonensis (Radomyos et al. 1994), we decided to use liver tissue for our search of metastrongylids using a refined molecular method, as the concentration of larvae and the probability of detection is believed to be the highest in this tissue. ...
Background
Endemic lizards of the genus Gallotia are of high ecological value to the terrestrial ecosystem of the archipelago of the Canary Islands, being potent seed spreaders as well as an important component of the diet of other vertebrates. The endemic lizard Gallotiagalloti in Tenerife has recently been reported to be a paratenic host of Angiostrongyluscantonensis, an invasive metastrongylid with zoonotic potential that is associated with rats as definitive hosts. However, microscopic examination of G.galloti tissue samples also revealed the presence of other metastrongylid larvae inside granulomas on the liver of this reptile. The aim of this study was to investigate the presence of helminths other than A.cantonensis in tissues of G.galloti from Tenerife.
Methods
A multiplex-nested PCR targeting the internal transcribed spacer 1 was designed that enabled the species-specific detection of A.cantonensis, Angiostrongylusvasorum, Aelurostrongylusabstrusus, Crenosomastriatum and Crenosomavulpis. Liver samples from 39 G.galloti were analysed.
Results
Five metastrongylids were detected: A.cantonensis (15.4% of samples analysed), A.vasorum (5.1%), Ae.abstrusus (30.8%), C.striatum (30.8%) and undetermined metastrongylid sequences (12.8%). Co-infection was highly prevalent among the lizards which tested positive.
Conclusions
The study provides a new specific tool for the simultaneous detection of a range of metastrongylids of veterinary importance as well as new data on the circulation of metastrongylids in an ecosystem dominated by lizards.
Graphical Abstract
... The forested areas of the Pantanal are colonised by a rich community of small mammals, which use a wide variety of habitats, from land areas to arboreal strata (Rademaker et al., 2009;Andreazzi et al., 2011). These animals comprise the diet of mesocarnivores and perform essential ecosystem services, such as seed dispersal, as well as act as hosts and reservoirs for parasite species that affect humans and domestic animals (Janzen, 1971;Morand et al., 2006). ...
Despite the great diversity of coccidians, to our knowledge, no coccidian infections have been described in Oecomys spp. In this context, we examined Oecomys mamorae Thomas (Rodentia: Cricetidae) from the Brazilian Pantanal for infections with enteric coccidia. Nine individuals were sampled, and one was found to be infected. The oöcysts were recovered through centrifugal flotation in sugar solution. Using morphological and morphometric features, we described a new species of Cystoisospora Frenkel, 1977. Sporulated oöcysts were ovoidal 20.0–29.1 × 16.4–23.2 (26.7 × 21.2) µm and contained two sporocysts, 12.9–19.1 × 9.4–13.9 (16.4 × 12.4) µm, each with four banana-shaped sporozoites. Polar granule and oöcyst residuum were both absent. We documented the developmental forms in the small intestine and described the histopathological lesions in the enteric tract. Our results indicate that the prevalence of Cystoisospora mamorae n. sp. in O. mamorae is low, and tissue damage in the enteric tract is mild, even in the presence of coccidian developmental stages.
... Greater abundances of Neoheligmonella sp. were found in the mesic site compared to the arid site. Increased levels of moisture in the soil could be beneficial to the survival of the parasite itself as most trichostrongyloid L1 and L2 stages are free-living (Morand et al., 2006). Alternatively, greater population densities of C. h. ...
The spread of parasites through a host population is based on the variation in behavior and immune function between individuals and is rarely uniform. We studied the gastrointestinal parasites of common mole-rats (Cryptomys hottentotus hottentotus, Lesson 1826) from 2 sites and assessed the levels of infection based on host sex, breeding status and season. Only nematode species were found; Neoheligmonella sp. and Mammalakis macrospiculum, (Ortlepp, 1939) and a single specimen of Trichuris sp., all of which have direct life cycles. Parasite burden and species richness was greater in the mesic habitat. The abundance of Neoheligmonella sp. differed significantly between seasons and the season of peak abundance differed between sites, perhaps due to differences in host densities between sites. In addition, parasite burden did not differ between the sexes but breeding animals had higher infections of Neoheligmonella sp. and M. macrospiculum than non-breeding animals. This and previous studies thus suggest that the subterranean environment is beneficial in reducing parasite diversity, although the restrictions on movement may lead to certain individuals suffering higher parasite burdens.
... Studies on the life cycles of the helminths of mammals are relatively few (Georgiev, Bray, & Littlewood, 2006;Morand, Bouamer, & Hugot, 2006). We present information of congener species or species of the same family or order and extrapolate them to the present infections only when they are constant at the relevant taxonomic level. ...
Eighty-six specimens representing 7 species of rodents from 9 localities in the state Zacatecas were examined for helminths. Only 5 host species were found to harbor at least 1 species: Chaetodipus sp., Dipodomys merriami atronasus, Neotoma mexicana, Otospermophilus variegatus, and Peromyscus sp.; in contrast Mus musculus and Reithrodontomys sp., were not parasitized. Three species of cestodes (Catenotaeniidae gen. sp., Hymenolepis sp., and Raillietina sp.) and 7 nematodes (Gongylonema sp., Heteromyoxyuris longejector, Lamotheoxyuris cf. ackerti, Mastophorus dipodomis, Rauschtineria sp., Pterygodermatites dipodomis, and Trichuris dipodomis) were recorded. The intestine is the most parasitized (7 taxa) and trematodes were not found. The highest species richness was recorded in D. merriami atronasus from Rancho La Barranca (6 taxa), which also had the most sampling effort. H. longejector in Chaetodipus sp. from El Gordillo, showed the greatest mean abundance, and mean intensity values, followed by Rauschtineria sp. in O. variegatus from Morelos-Zacatecas Road. All species are new locality records, 14 new host records, and 2 taxa recorded for the first time in Mexico: Rauschtineria sp. and M. dipodomis. This is the first study of helminth parasites of rodents from Zacatecas.
Parasites are an integral part of all ecosystems and have gained wide acceptance as biological tags since they can provide important information about their hosts, including biology, diet, feeding behaviour, population structure, movements, geographical ranges and phylogenies. The plains vizcacha is a good model for studies on parasites since it has a particular behaviour (gregarious, coprophagic and allogrooming habits), a wide geographical distribution occurring in diverse ecoregions, economic importance for causing damage on the fields and for having meat for consumption and a sanitary interest as a potential host for zoonotic or enzootic parasites. Different populations of this rodent have been studied from economic, biological and ecological aspects in Argentina; however, studies on the diversity of parasites or their implications for human and animal health are very scarce. This chapter aims to explore the available information on plains vizcacha endoparasites considering their diversity, sanitary aspects, ecological data and distribution from host and environment. In this chapter, we present the following five sections: (1)—Diversity of Parasitic Species, Geographical Records and Ecological Data; (2)—Animal and Human Health Considerations; (3)—Structure of Parasitic Populations and Communities; (4)—Potential Use of the Parasitic Species as Biotags; and (5)—Conclusions.
This chapter provided general information on parasitic helminths, including biology, taxonomic classification, a list of parasitic helminths of medical and public health importance globally, and their impacts on humans to address some fundamental questions on how many parasitic helminth species have ever been reported to infect humans and which parasite taxonomic groups are of scientific significance. Research interests in medical parasitology, molecular biology, health, and life science information were obtained mainly from the Host-Parasite Database of the Natural History Museum, London (NHM), and other published sources. This chapter also discussed the diversity of parasitic helminths and their relationships based on classical systematics and taxonomy.
Serra Calderona Natural Park, a Mediterranean ecosystem, has been in post-fire regeneration for 10 years. To elucidate which helminth community component species of the wood mouse, Apodemus sylvaticus, can be considered biological tags of this process, the influence of intrinsic (host density; host sex and age) and extrinsic factors (site, year, and period of capture; vegetation recovery) on their prevalence and abundance has been analysed, comparing a burned and an unburned area. A total of 564 wood mice (408 from the burned and 156 from the unburned area), from the 2nd to the10th post-fire year, was included in this helminthoecological study. The results suggest that the area in post-fire regeneration is still more vulnerable to periodic environmental changes than the unburned area as deduced from the analysis of the helminth populations of Pseudocatenotaenia matovi, Skrjabinotaenia lobata, Trichuris muris, Eucoleus bacillatus and Aonchotheca annulosa. The intermediate and definitive host populations presented a greater variability to these environmental changes in the burned area (Taenia parva, P. matovi, S. lobata, A. annulosa, Syphacia stroma and S. frederici). In the regenerating area, some behavioural changes in certain populations determined by the host sex are taking place (T. parva, Helgimosomoides polygyrus and S. frederici). During the last years studied, a greater similarity in the populational development of some component species between both areas can be appreciated (H. polygyrus and S. stroma). The role of the wood mouse and its helminth parasites as biological tags of the post-fire regeneration process in Mediterranean ecosystems has been confirmed.
The progressive anthropization of caves for food resources or economic purposes increases human exposure to pathogens that naturally infect cave-dwelling animals. The presence of wild or domestic animals in the immediate surroundings of caves also may contribute to increasing the risk of emergence of such pathogens. Some zoonotic pathogens are transmitted through direct contact, but many others require arthropod vectors, such as blood-feeding insects. In Africa, hematophagous insects often play a key role in the epidemiology of many pathogens; however, their ecology in cave habitats remains poorly known. During the last decades, several investigations carried out in Afrotropical caves suggested the medical and veterinary importance particularly of insect taxa of the Diptera order. Therefore, the role of some of these insects as vectors of pathogens that infect cave-dwelling vertebrates has been studied. The present review summarizes these findings, brings insights into the diversity of cave-dwelling hematophagous Diptera and their involvement in pathogen transmission, and finally discusses new challenges and future research directions.
Contrasting host and parasite population genetic structures can provide information about the population ecology of each species and the potential for local adaptation. Here, we examined the population genetic structure of the nematode Neoheligmonella granjoni at a regional scale in southeastern Senegal, using 11 microsatellite markers. Using the results previously obtained for the two main rodent species of the host community, Mastomys natalensis and Mastomys erythroleucus, we tested the hypothesis that the parasite population structure was mediated by dispersal levels of the most vagile host. The results showed similar genetic diversity levels between host and parasite populations, and consistently lower levels of genetic differentiation in N. granjoni, with the exception of one outlying locus with a high F(ST). The aberrant pattern at this locus was primarily due to two alleles occurring at markedly different frequencies in one locality, suggesting selection at this locus, or a closely linked one. Genetic differentiation levels and isolation by distance analyses suggested that gene flow was high and random in N. granjoni at the spatial scale examined. The correlation between pair-wise genetic differentiation levels in the parasite and its main host was consistent with the hypothesis tested. Models of local adaptation as a function of the dispersal rates of hosts and parasites suggest that opportunities for local adaptation would be low in this biological system.
Domestication of the dog some 14 000 years ago has enabled this species to become the most abundant carnivore in the world today with an estimated population of 500 million. Dogs perform a wide range of roles from working as guides for the blind and deaf, guarding, protecting and driving sheep and cattle, and in hunting. Most, however, are companion animals, and the benefits of contact with animals to human health and psychological well-being is now well recognised. As well as the advantages, the close relationship between dogs and humans brings its problems. Zoonotic diseases such as rabies and a wide range of helminth and protozoal parasites represent a threat to public health. This threat of zoonotic infection is greatest for immunosuppressed people such as those with AIDS or malnutrition, or those under immunosuppressive medication for cancer and transplant therapy. This book aims to provide a comprehensive account of the interaction between dogs and humans in various social and cultural situations throughout the world. The chapters are written by 22 contributors from all over the world and the first two chapters cover the human-canine relationship (including the social and health benefits of dogs and their use in therapy) and dog ecology and population biology. Then follow chapters on rabies, bacterial zoonoses, protozoal zoonoses, trematodes, cestodes, nematodes and ectoparasites. The final three chapters cover zoonoses and immunosuppressed populations (immunosuppressed dogs as well as humans), management of dog populations (including legislation, education and costs), and control of zoonoses in dogs (using rabies, leishmaniasis and echinococcosis as examples). The chapters are supported by references and there is a subject index.
Mass mortalities due to disease outbreaks have recently affected major taxa in the oceans. For closely monitored groups like
corals and marine mammals, reports of the frequency of epidemics and the number of new diseases have increased recently. A
dramatic global increase in the severity of coral bleaching in 1997–98 is coincident with high El Niño temperatures. Such
climate-mediated, physiological stresses may compromise host resistance and increase frequency of opportunistic diseases.
Where documented, new diseases typically have emerged through host or range shifts of known pathogens. Both climate and human
activities may have also accelerated global transport of species, bringing together pathogens and previously unexposed host
populations.
The energetics of 11 species of New World hystricognath 'caviomorph' rodents are presented and compared with data from the literature on 19 additional species. Log body mass alone accounts for 94% of the variation in the log 10 10 basal rate of metabolism in caviomorphs. The residual variation in basal rate is correlated with the stratum on which species live: arboreal species have low basal rates; terrestrial and fossorial species have intermediate basal rates; and aquatic species have high basal rates. When stratum is not included in the analysis, folivores, especially those that are arboreal, have lower basal rates than species with other food habits when combined with log body mass. Small island 10 endemics, all of which are folivores, have basal rates that are 61% of continental species. Log basal rate correlates 10 with family affiliation when combined with log mass, but only if no other factor is included. Therefore, caviomorphs 10 with low basal rates are arboreal, folivorous, live on small islands and belong to the Capromyidae, whereas other character combinations are associated with higher basal rates. These observations demonstrate that the basal rates of caviomorphs reflect many factor interactions. No differences in basal rate were found to reflect climate. Log mass, the 10 only factor to correlate with conductance, accounts for 82% of the variation in log minimal thermal conductance. 10 Mean interspecific body temperature was 36.9C; it was lowest in aquatic and fossorial species.
Conservation medicine is an emerging discipline, focussing on the intersection of ecosystem health, animal health, and human health. Work in the biomedical and veterinary sciences is now being folded into conservation biology; to explore the connections between animal and human health; trace the environmental sources of pathogens and pollutants; develop an understanding of the ecological causes of changes in human and animal health; and understand the consequences of diseases to populations and ecological communities. Conservation Medicine defines this new discipline. It examines ecological health issues from various standpoints, including the emergence and resurgence of infectious disease agents; the increasing impacts of toxic chemicals and hazardous substances; and the health implications of habitat fragmentation and degradation and loss of biodiversity. It will provide a framework to examine the connections between the health of the planet and the health of all species and challenge practitioners and students in the health sciences and natural sciences to think about new, collaborative ways to address ecological health concerns.
This is a major synthesis of the theory and empirical knowledge about the ecology and epidemiology of infectious diseases in natural, unmanaged, animal and plant populations. Throughout the book a dialogue is developed between the patterns observed in empirical studies of disease in natural populations and the mathematical models used to dissect and examine the observed epidemiological patterns. The book arose from a symposium at the Newton Institute at Cambridge University. It is divided into a number of reviews by experts in various fields and four group reports: two of these synthesize important issues relating to the dynamics of microparasites and macroparasites, while the others discuss spatial patterns in disease dynamics and the evolutionary biology of parasites, pathogens and their hosts.