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Patterns of host specificity and transmission among parasites of wild ...

Patterns of host specificity and transmission among parasites of wild ...

A.B. Pedersen et al. /

A.B. Pedersen et al. / International Journal for Parasitology 35 (2005) 647–657 649infections from wild populations only (i.e. excludingrecords of parasites from captive animals or infectionexperiments), and considered only vertebrate host species inassigning specificity scores, ignoring invertebrates thatmight serve as intermediate hosts or vectors.To each specificity score, we added a confidence scorebased on the quality and quantity of published records thatprovided information on affected host species. Highestconfidence scores (3) were assigned to records based ondirect isolation of pathogens or their DNA, in combinationwith a sufficient number of published records (usually 5 ormore); intermediate confidence (2) was assigned to scoresbased on indirect measures of pathogen presence (e.g.serology) or a limited number of published records, and lowconfidence (1) was assigned to specificity scores based onunpublished knowledge, strong inference, or informationderived solely from our primate parasite database. Confidencescores were used to evaluate the sensitivity of patternsby analyzing the data once with all available records, andsecond by excluding data with low confidence. All viralspecificity scores were assigned high or moderate confidence;thus, for this group we did not repeat analysesexcluding low confidence data.As a second measure of confidence, we examined thesampling effort associated with each parasite species usingcitation counts from three common bibliographic databases:ISI Web of Science (WOS; www.isiwebofknowledge.com),Biosis Previews (www.biosis.org), and Pubmed (www.pubmed.org). We searched each database for correctedparasite Latin binomials or ICTVdb virus names. For eachparasite species we computed average sampling effort as thelog-transformed arithmetic mean of all three citation counts(adding one to each count first to avoid taking the log ofzero). Analysis of variance showed that categoricalmeasures of confidence were highly associated with theaverage of citation counts (F 2,409 Z132.9; P!0.0001) sothat specificity scores assigned high confidence were alsogenerally from the best studied parasites in the scientificliterature (mean log-referencesZ2.18). Parasites withmoderate confidence scores had intermediate numbers ofcitations (mean log-referencesZ1.04), and those with thelowest confidence were generally not well represented in thescientific literature (mean log-references 0.29).Not surprisingly, specificity scores were associated withboth categorical and continuous measures of confidence. Inparticular, the least specific parasites were associated withthe highest confidence scores, whereas genus or speciesspecific parasites were more likely to be assigned intermediateor low confidence scores. This association washighly significant when examined across all parasite groups(c 2 Z193.6, d.f.Z8, P!0.0001), as well as within each ofthe three major parasite groups: viruses (c 2 Z15.3, d.f.Z4,PZ0.004), protozoa (c 2 Z33.3, d.f.Z8, P!0.0001), andhelminths (c 2 Z61.5, d.f.Z8, P!0.0001). A similar patternwas found when we examined the association betweenspecificity and average citation counts (F 4,407 Z83.04;P!0.0001). In this case, mean citation counts were lowestamong parasites assigned genus- or species-specific status(mean log-referencesZ0.25 and 0.34, respectively). Citationcounts were intermediate for parasites assigned familyspecific status (meanZ0.90) and were greatest for parasitesin the order-specific and multi-order categories (meanZ1.83 and 2.24, respectively).2.3. Parasite transmission modeThe transmission strategy of each parasite species wasrecorded as one or more of the following four categories:close contact, non-close contact, biting arthropod vectors, orintermediate hosts. Parasites spread by close contact werethose that were highly contagious and communicable byclose proximity or direct contact such as biting, scratching,mating contact, or other touching. Close contact transmissionwas further subdivided into three routes—sexual,vertical (parent to offspring), or close non-sexual contact.Non-close contact involved transmission via fomites orcontact with contaminated soil or water. Vector-borneparasites were those spread via biting arthropods (ticks,mites, fleas, flies, and other invertebrates), and parasiteswith intermediate hosts were those characterised by thepresence of complex life cycles and/or trophic transmission.Transmission strategies were assigned by multiple websearches using parasite Latin binomials or ICTV virusnames. If direct information was not available for aparticular parasite species, transmission strategies wereassigned based on information from closely related parasites(if similar transmission strategies were highly likely) orremained unassigned.2.4. Data analysisWe first examined the occurrence of host specificity andmajor transmission strategies across all parasites from wildprimates, and then within each of the three best-representedgroups: viruses, helminths, and protozoa. Second, we testedwhether the predicted associations between transmissionand host specificity were consistent with observed patternswithin each of the major parasite groups. Finally, thetaxonomic distribution of parasites from wild primates(arthropods, bacteria, fungi, helminths, protozoa, andviruses) was compared with reports from earlier studies ofhumans and domesticated animals (e.g. Cleaveland et al.,2001; Taylor et al., 2001) to investigate whether the typesand characteristics of parasites from wild hosts were similarto those reported for economically important species, and toexamine characteristics of parasites from wild primates thatwere also reported as emerging in human populations.Unless otherwise stated, we used Pearson Chi squareanalysis or logistic regression (general linear model withbinomial errors) to examine associations between hostspecificity, parasite taxonomy, and transmission strategy.

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