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Effect of Host and Environment-Related Factors on Fleas of the Pichi, An An Acad Bras Cienc (2020) 92(2): e20180656 DOI 10.1590/0001-3765202020180656 Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences Printed ISSN 0001-3765 I Online ISSN 1678-2690 www.scielo.br/aabc | www.fb.com/aabcjournal BIOLOGICAL SCIENCES Effect of host and environment-related factors Running title: THE PICHI AND on fleas of the pichi, an armadillo from Argentina ITS FLEAS IN ARGENTINA Academy Section: BIOLOGICAL MARIA CECILIA EZQUIAGA, TATIANA A. RIOS, ESTEBAN A. ACTIS, GUILLERMO H. CASSINI, AGUSTÍN M. ABBA & MARIELLA SUPERINA SCIENCES Abstract: The pichi (Zaedyus pichiy; Cingulata: Chlamyphoridae) is an armadillo whose ectoparasite fauna is composed of ticks and fleas. Fleas were collected from 218 pichis in e20180656 southern Mendoza, Argentina, in summer and winter of 2015 and 2016. Prevalences were analyzed and differences in the intensities of the total number of fleas related to host (age, sex, weight, size and physical condition) and environment-related (seasonality and 92 year) factors evaluated. Phthiropsylla agenoris was the only species found. Intensities (2) 92(2) of fleas were higher in 2015, in juveniles, and in males. Individuals with poor physical condition were more parasitized than those with good or normal body condition. The main explanatory variable was sampling year. This factor was directly associated with precipitation. The extreme conditions and heavy rains during the El Niño event in 2015/2016 led to environmental changes that seem to have severely affected the life cycle of fleas. Key words: ENSO, Environmental conditions, Mendoza province, Phthiropsylla agenoris. INTRODUCTION extinctions (Cizauskas et al. 2017). In this sense, the habitat of an ectoparasite should not be There is ample evidence of the ecological impact just a particular host, but a particular host in of recent climate change, from polar terrestrial a particular habitat because of its sensitivity to to tropical marine environments (Walther et factors of the off-host environment. Flea species al. 2002). When parasites are considered in the composition in a habitat is not only determined climate change literature, most studies focus by host species composition, but also by the on virulent pathogens that could become environmental parameters of that habitat. dominant in a changing climate, raising human These parameters determine the conditions of health concerns. The majority of parasites have, the burrow or the nest of the host (temperature, however, no direct effect on human health, humidity, substrate, nest material) and thus and the potential negative impacts of climate affect flea assemblage (Krasnov 2008). change on most wildlife parasites are still The pichi (Zaedyus pichiy; Xenarthra: untested (Cizauskas et al. 2017 and references Chlamyphoridae) is a small (body mass herein). A changing climate alters the availability approximately 1 kg) armadillo endemic to arid of parasite niche space, driving a combination and semiarid lands with firm sandy soils of of habitat loss and range shifts, and potentially Argentina and Chile (Superina 2008). Its range decreasing population growth and reproductive covers the horizontal strip from the province rates, all of which may encourage primary of La Rioja to southern Buenos Aires province An Acad Bras Cienc (2020) 92(2) MARIA CECILIA EZQUIAGA et al. THE PICHI AND ITS FLEAS IN ARGENTINA in Argentina, as well as eastern Chile, south to belongs to the Andean biogeographic region, the Straits of Magellan (Superina & Abba 2014). Patagonian Subregion (Morrone 2006) and is These semi-fossorial, solitary and predominantly characterized by an arid climate, poor volcanic diurnal mammals are opportunistic omnivores soil, and scarce vegetation (Candia et al. 1993). that primarily feed on insects (Superina 2008, Pichis were captured by hand, sexed, Superina et al. 2009a). They are the only measured, weighed, aged (taking into account a xenarthrans known to hibernate during winter combination of weight, body length and external and to enter torpor in warmer seasons (Superina characteristics) and released. Forceps were used & Boily 2007). One tick and 4 flea species have to collect all visible ectoparasites. The field been found associated with this armadillo: study was carried out under permission issued Amblyomma pseudoconcolor (Ixodidae), by Dirección de Recursos Naturales Renovables, Malacopsylla grossiventris, Phthiropsylla Provincia de Mendoza, through Resolutions agenoris (both Malacopsyllidae), Tunga 41/2015 and 4/2016. All animals were cared in perforans, Hectopsylla (Hectopsylla) broscus accordance with the Guiding Principles in the (both Tungidae) (Mauri & Navone 1993, Superina Care and Use of Animals of the US National et al. 2004, Ezquiaga et al. 2015). Future climate Institute of Health and ASM guidelines (Sikes scenarios for the pichi’s range include projected et al. 2016). Procedures were approved by the temperature increases that are, in general, Institutional Animal Care and Use Committee more intense during the summer months. of the School of Medical Science, Universidad Precipitation levels are expected to decline Nacional de Cuyo (Protocol approval No. especially in winter (Barros et al. 2015). These 23/2014). changes in environmental conditions could lead The collected ectoparasites, all of them fleas, to a modification of species assemblages, range were stored in 96% ethanol. In the laboratory, shifts, and local extinctions of fleas parasitizing they were cleared in KOH 10%, dehydrated in pichis. an increasing series of ethanol dilutions (80% The aim of this work was to study the flea to 100%), diaphanized in eugenol, and mounted community of a population of Zaedyus pichiy in Canada balsam for later identification with from Malargüe (southern Mendoza province) an optic microscope following Smit (1987). The and associate their presence and parasitism studied material is deposited in the Centro de rates with the factors that influence them, such Estudios Parasitológicos y de Vectores (CEPAVE) as host-related factors (age, sex, weight, size and and holds the field number (ZP50-54, 60-65, 67- physical condition) and environment-related 86, 89-111, 113-121, 123-126, 128-144, 146-165, 167- factors (seasonality and year). 169, 171-211, 213-226, 229-285). The physical condition of pichis was assessed by an iterative outlier test on an ordinary-least- MATERIALS AND METHODS squares (OLS) regression of log10-transformed Fieldwork was conducted near El Cortaderal weight and body length (Ezquiaga et al. 2014). (36°35.105’ S; 68°32.184’ W), Malargüe Department, Outliers in each iteration were discarded to fit Mendoza Province, Argentina in February 2015 the OLS regression in the next step. Outliers with and March 2016 (summer), and September 2015 positive externally studentized residuals were and September 2016 (winter). The study area assigned to a good condition, whereas those with negative externally studentized residuals were An Acad Bras Cienc (2020) 92(2) e20180656 2 | 10 MARIA CECILIA EZQUIAGA et al. THE PICHI AND ITS FLEAS IN ARGENTINA assigned to a poor condition. The procedures competing models had similar wAIC values, an finished when outliers were no longer detected. averaged model was computed using the MuMIn R The remaining observations were then assigned package (Barton 2016). Additionally, we computed to a normal condition. Flea prevalence, mean simple GLMs with the number of fleas per host abundance (MA) and mean intensity (MI) were (count data) as response variable and each of calculated as described by Bush et al. (1997). the 7 explanatory variables. To evaluate error Prevalences were analyzed by means of distribution (Poisson or negative binomial), as contingency tables using the log-likelihood ratio well as overdispersion on the count or zero data, Chi-square statistic (Zar 2009) and applying we visualized flea counts in Cleveland dot plots the loglm function of MASS 7.3-45 R package and histograms. Whenever graphical analyses (Venables & Ripley 2002). The first step was to were not conclusive, we obtained models using evaluate multidimensional contingency tables different error distribution (Poisson and negative for mutual independence (i.e., no interactions) binomial GLM) and accounting for zero inflated among the variables year, season, age, sex data (zero-inflated GLM) and later compared them and physical condition. Partial independence using the likelihood ratio test (LRT) (Zuur et al. was tested whenever mutual independence 2009). The measurement of ‘false zeros’ (absence was significant. Based on the results of the of fleas recorded when fleas are present) might multidimensional analyses, all variables were be random or related to sampling protocols, but tested by means of bidimensional contingency there are no biological reasons to believe that the tables. explanatory variables have an effect. A constant Generalized Linear Models (GLM) were used was therefore used in all zero-inflated GLM to to evaluate differences in the intensities of the model false-zero probability on the count data. total number of fleas related to host factors and All GLM and statistics analyses were performed temporal dynamics. The number of fleas per with the lmtest 0.9-33 R (Zeileis & Hothorn 2002), individual host (count data) was the response multcomp 1.4-6 R (Hothorn et al. 2008), pscl 1.04.4 variable, and year, age (categorical ordinal R (Zeileis et al. 2008) and lme4 1.1-12 packages sequential), season, sex, physical condition (Bates et al. 2015)
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