Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: An example with fleas on prairie dogs

Eads, David A.; Biggins, Dean E.; Doherty, Paul F.; Gage, Kenneth L.; Huyvaert, Kathryn P.; Long, Dustin H.; Antolin, Michael F.

doi:10.1016/j.ijppaw.2013.09.002

Cited by 31 publications

(29 citation statements)

References 40 publications

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“…If an epizootic does not erupt in a dry year, and if precipitation returns, fleas might already be abundant because of the preceding drought, and the returning precipitation and accompanying mild temperatures might propel an epizootic vortex (Ray and Collinge ). Increased primary production facilitates reproductive output for prairie dogs (Knowles , Facka et al , Eads ), which might provide context for behavioral interactions among prairie dogs due to proximity, allowing for exchanges of fleas among hosts (Tripp et al , Eads et al ). Mild temperatures in wet years might favor plague transmission by fleas (Williams et al ), for example, while they attempt to feed on blood from hosts above ground.…”

Section: Discussionmentioning

confidence: 99%

Paltry past‐precipitation: Predisposing prairie dogs to plague?

Eads

Biggins

2017

J Wildl Manag

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The plague bacterium Yersinia pestis was introduced to California in 1900 and spread rapidly as a sylvatic disease of mammalian hosts and flea vectors, invading the Great Plains in the United States by the 1930s to 1940s. In grassland ecosystems, plague causes periodic, devastating epizootics in colonies of black‐tailed prairie dogs (Cynomys ludovicianus), sciurid rodents that create and maintain subterranean burrows. In doing so, plague inhibits prairie dogs from functioning as keystone species of grassland communities. The rate at which fleas transmit Y. pestis is thought to increase when fleas are abundant. Flea densities can increase during droughts when vegetative production is reduced and herbivorous prairie dogs are malnourished and have weakened defenses against fleas. Epizootics of plague have erupted frequently in prairie dogs during years in which precipitation was plentiful, and the accompanying cool temperatures might have facilitated the rate at which fleas transmitted Y. pestis. Together these observations evoke the hypothesis that transitions from dry‐to‐wet years provide conditions for plague epizootics in prairie dogs. Using generalized linear models, we analyzed a 24‐year dataset on the occurrence of plague epizootics in 42 colonies of prairie dogs from Colorado, USA, 1982–2005. Of the 33 epizootics observed, 52% erupted during years with increased precipitation in summer. For the years with increased summer precipitation, if precipitation in the prior growing season declined from the maximum of 502 mm to the minimum of 200 mm, the prevalence of plague epizootics was predicted to increase 3‐fold. Thus, reduced precipitation may have predisposed prairie dogs to plague epizootics when moisture returned. Biologists sometimes assume dry conditions are detrimental for plague. However, 48% of epizootics occurred during years in which precipitation was scarce in summer. In some cases, an increased abundance of fleas during dry years might compensate for other conditions that become less favorable for plague transmission. Global warming is forecasted to amplify the hydrological cycle in the Great Plains, causing an increased occurrence of prolonged droughts interceded by brief periods of intense precipitation. Results herein suggest these changes might affect plague cycles in prairie dogs. Both negative and positive consequences of dry conditions should be considered when managing plague. © 2017 The Wildlife Society.

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Section: Discussionmentioning

confidence: 99%

Paltry past‐precipitation: Predisposing prairie dogs to plague?

Eads

Biggins

2017

J Wildl Manag

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“…We note that while multi-model inference has been used in a few studies similar to ours [32]–[34], the formal treatment of detection failures has hardly entered the vector ecology literature thus far [14], [28], [29], [35], [36]. Yet, as discussed below, standard approaches can yield biased effect-size estimates and SEs; site-occupancy models may provide a more reliable and realistic picture of key population parameters and their environmental correlates [15], [16].…”

Section: Discussionmentioning

confidence: 99%

Modeling Disease Vector Occurrence When Detection Is Imperfect II: Drivers of Site-Occupancy by Synanthropic Triatoma brasiliensis in the Brazilian Northeast

et al. 2014

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BackgroundUnderstanding the drivers of habitat selection by insect disease vectors is instrumental to the design and operation of rational control-surveillance systems. One pervasive yet often overlooked drawback of vector studies is that detection failures result in some sites being misclassified as uninfested; naïve infestation indices are therefore biased, and this can confound our view of vector habitat preferences. Here, we present an initial attempt at applying methods that explicitly account for imperfect detection to investigate the ecology of Chagas disease vectors in man-made environments.MethodologyWe combined triplicate-sampling of individual ecotopes (n = 203) and site-occupancy models (SOMs) to test a suite of pre-specified hypotheses about habitat selection by Triatoma brasiliensis. SOM results were compared with those of standard generalized linear models (GLMs) that assume perfect detection even with single bug-searches.Principal Findings Triatoma brasiliensis was strongly associated with key hosts (native rodents, goats/sheep and, to a lesser extent, fowl) in peridomestic environments; ecotope structure had, in comparison, small to negligible effects, although wooden ecotopes were slightly preferred. We found evidence of dwelling-level aggregation of infestation foci; when there was one such focus, same-dwelling ecotopes, whether houses or peridomestic structures, were more likely to become infested too. GLMs yielded negatively-biased covariate effect estimates and standard errors; both were, on average, about four times smaller than those derived from SOMs.Conclusions/SignificanceOur results confirm substantial population-level ecological heterogeneity in T. brasiliensis. They also suggest that, at least in some sites, control of this species may benefit from peridomestic rodent control and changes in goat/sheep husbandry practices. Finally, our comparative analyses highlight the importance of accounting for the various sources of uncertainty inherent to vector studies, including imperfect detection. We anticipate that future research on infectious disease ecology will increasingly rely on approaches akin to those described here.

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“…, Eads et al. , ). Some studies have suggested that high precipitation enhances growth in populations of fleas (Stapp et al.…”

Section: Introductionmentioning

confidence: 99%

Factors that affect parasitism of black‐tailed prairie dogs by fleas

Eads

Hoogland

2016

Ecosphere

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Fleas (Insecta: Siphonaptera) are hematophagous ectoparasites that feed on vertebrate hosts. Fleas can reduce the fitness of hosts by interfering with immune responses, disrupting adaptive behaviors, and transmitting pathogens. The negative effects of fleas on hosts are usually most pronounced when fleas attain high densities. In lab studies, fleas desiccate and die under dry conditions, suggesting that populations of fleas will tend to decline when precipitation is scarce under natural conditions. To test this hypothesis, we compared precipitation vs. parasitism of black‐tailed prairie dogs (Cynomys ludovicianus) by fleas at a single colony during May and June of 13 consecutive years (1976–1988) at Wind Cave National Park, South Dakota, USA. The number of fleas on prairie dogs decreased with increasing precipitation during both the prior growing season (April through August of the prior year) and the just‐completed winter–spring (January through April of current year). Due to the reduction in available moisture and palatable forage in dry years, herbivorous prairie dogs might have been food‐limited, with weakened behavioral and immunological defenses against fleas. In support of this hypothesis, adult prairie dogs of low mass harbored more fleas than heavier adults. Our results have implications for the spread of plague, an introduced bacterial disease, transmitted by fleas, that devastates prairie dog colonies and, in doing so, can transform grassland ecosystems.

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Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: An example with fleas on prairie dogs

Abstract: Graphical abstract

Cited by 31 publications

References 40 publications

Paltry past‐precipitation: Predisposing prairie dogs to plague?

Paltry past‐precipitation: Predisposing prairie dogs to plague?

Modeling Disease Vector Occurrence When Detection Is Imperfect II: Drivers of Site-Occupancy by Synanthropic Triatoma brasiliensis in the Brazilian Northeast

Factors that affect parasitism of black‐tailed prairie dogs by fleas

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