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DOI: 10.1515/ap-2015-0073

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Cidade Universitária Zeferino Vaz Barão Geraldo CEP 13083-970 – Campinas SP Fone: (19) 3521-6493 http://www.repositorio.unicamp.br DOI: 10.1515/ap-2015-0073 © W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2015, 60(3), 515–524; ISSN 1230-2821 Effect of body size on the abundance of ectoparasitic on the wild rodent Oligoryzomys nigripes

Fernanda Rodrigues Fernandes1*, Leonardo Dominici Cruz1, Arício Xavier Linhares2 and Claudio José Von Zuben3 1Universidade Federal do Maranhão, Campus de São Bernardo. Rua Projetada, s/n, Perímetro Urbano, CEP 65550-000, São Bernardo, MA, Brasil; 2Universidade Estadual de Campinas, Instituto de Biologia, Departamento de Biologia . Caixa Postal 6109, Cidade Universitária, CEP 13083-970, Campinas, São Paulo, Brasil; 3Universidade Estadual Paulista Júlio de Mesquita Filho, Instituto de Biociências de Rio Claro, Departamento de Zoologia. Avenida 24A, 1515, Caixa Postal 199, Bela Vista. CEP 13506-900, Rio Claro, São Paulo, Brasil

Abstract The abundance of parasites on a host can be affected by several factors; in this study, we investigated the influence of sex and body size of the host rodent Oligoryzomys nigripes on the abundance of ectoparasitic mites (: ). The gen- eralized linear model indicated that body size (indicative of age) of the host rodent O. nigripes significantly contributed to the variation in the abundance of mites on host rodents at the Experimental Station of Itirapina. This trend of increased parasitism on hosts with larger body sizes may be linked to the fact that larger individuals are able to support the coexistence of a larger number of parasites, and being more mobile, are more exposed to infection by parasites.

Keywords Abundance, age, body mass, mites, small mammal

Introduction (McNab 1963), and consequently are more heavily exposed to parasites (Bordes et al. 2009). Parasites use their hosts for shelter, nutrition, and dispersal, If the males and females of a host species differ in their causing some degree of damage to the hosts. The abundance morphology, physiology, and behavior, parasite abundance can of parasitic species on a given host species is not a product of also be influenced by the sex of the host (Fernandes et al. random processes but rather a consequence of the morpho- 2012). Many mammalian species exhibit sexual dimorphism logical and ecological characteristics of the host, such as body in terms of size, with males being bigger than females in more size (Ezenwa et al. 2006), population density (Nunn et al. than 45% of species (Lindenfors et al. 2007b). This intersex- 2003), and geographic distribution (Lindenfors et al. 2007a). ual difference in physiology is based on the negative relation- The parasites can also play a role in determining the parasite ship between the male hormone, testosterone, and immune abundance on a given host, since some parasite species can function, making males more susceptible to the majority of act as a facilitators. Parasites of unrelated taxa can facilitate parasite infections (Klein 2004). Behavioral differences be- the acquisition of other species of parasite, by lowering the tween genders are related to the greater mobility of males in immune defenses of the host (Krasnov et al. 2005; Pilosof systems with promiscuous mating, as the range of a female is et al. 2013). generally associated with habitat quality, while the range of a The abundance of parasites on a given host species can male is associated with an improved probability of finding vary according to body size, as individuals with larger bodies sexual partners (Püttker et al. 2006; Fernandes et al. 2010; can aggregate more parasites due to their higher mobility, Perdue et al. 2011). larger total mass (i.e., more potential nutrients for parasites) The differences in the density and diversity of species of and larger surface area (Moore and Wilson 2002; Poulin 2007; rodent hosts among localities can influence the abundance and Bordes et al. 2009). Larger individuals have a higher meta- diversity of parasites. A higher density of a given host species bolic requirement, travel greater distances in search of food increases the chances of ectoparasite transmission between in-

*Corresponding author: [email protected]

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traspecific individuals (Krasnov et al. 2006; Ryder et al. 2007) were performed using 80 Sherman traps (dimensions 7.5 cm and a higher diversity of host species increases the chances of × 9.0 cm × 23.5 cm) placed on the ground (Jones et al. 1996), ectoparasitic exchange between interspecific individuals if with four traps per point of capture, each using a sweet potato different species share the same parasites (Dobson 2004; and peanut butter as bait. The total capture effort consisted of Lareschi and Krasnov 2010; Fernandes et al. 2012). The trans- 6,800 trap nights. Rodents were each tagged with a numbered mission of ectoparasites can occur through direct contact earring (Rudran 1996), their body mass measured with a (Darolova et al. 2001; Valera et al. 2003) or rarely by phoresy, Pesola® (accuracy = 1 g), and their sex was determined. The when parasites attach themselves to other more mobile indi- rodents were brushed with a toothbrush while in a white plas- vidual parasites, in order to increase their dispersal distance tic tray. The ectoparasites were collected from the plastic tray (Houck and O’Connor 1991; Harbison et al. 2009). using a disposable pipette, and placed in glass flasks with 70% The Mesostigmata mites (Acari) are very diverse, includ- alcohol. Each flask contained the parasites collected from a ing groups of free-living predators, as well as both facultative single host, and received an outer and inner label containing and obligatory parasites (Dowling and O’Connor 2010); how- the following information: host species, sex, earring number, ever, all of them morphologically preadapted for parasitism collection date, and collection place (Bergallo 1994). After (Radovsky 1985). In mammals, parasitism by mites is fre- being used, the tray was carefully cleaned and inspected be- quent, and the mammal-associated mites coexist in the same fore being reused. The collected mesostigmatid mites were nest with free-living nidicolous to obligate hematophagous slide mounted in Hoyer’s medium, and identified by Prof. mites (Radovsky 1985). Some mesostigmatid mites are found Gilberto Salles Gazeta and his team from the Oswaldo Cruz on wild rodents, and can survive in the environment for long Foundation (FIOCRUZ-RJ) using taxonomic keys (e.g. Fur- periods travelling considerable distances in search of new man 1972, Krantz and Walter 2009) and by direct comparison hosts. The life cycle of a mesostigmatid consists of an with specimens from the Collection of Apterous egg, one six-legged larval stage, two eight-legged nymph sta- Vector of Community Health Importance (CAVAISC- ges, and adulthood, but only the first nymphal and adult sta- FIOCRUZ). All collected mesostigmatid specimens were de- ges feed on blood (Watson 2008). posited in CAVAISC-FIOCRUZ. This research was authorized In this study, data were collected from mites (Acari: by the System of Authorization and Information in Biodiver- Mesostigmata) parasitizing the rodent species Oligoryzomys sity (SISBio number 17669). nigripes (Mammalia: Rodentia) in two cerrado (a Brazilian tropical savanna ecoregion) areas of southeast Brazil, in order Data analysis to determine whether the total abundance (Bush et al. 1997) of mites is influenced by the sex and body size of the host. The prevalence of mesostigmatid mite species in each study area was estimated according to the concept described by Bush et al. (1997). The effect of host body mass and sex on Materials and methods prevalence was assessed using logistic regression models, with α = 0.05 significance level (Sokal and Rohlf 2012). The dis- Study area tributions of total mesostigmatid mite abundance showed data overdispersion for two study areas (ESMG variance-mean The study was conducted in two cerrado areas in the state of ratio = 20.52; ESI variance-mean ratio = 6.58) and the nega- São Paulo in southeast Brazil: the Experimental Station of tive binomial distribution was fitted to the abundance data Mogi Guaçu (hereafter ESMG) (22°24´S; 47°15´W) and the (ESMG: = 2.76; d.f. = 3; P value = 0.43; ESI: = 4.08; d.f. = 4; Experimental Station of Itirapina (hereafter ESI) (22°24´S; P value = 0.39). Thus, the generalized linear model (GLM) of 47°82´W). The ESI comprises 3,212 ha and altitudes range negative binominal regression was used in this study to ac- between 700 – 827 m, while the ESMG comprises 3,050 ha count for overdispersion of the mite abundance data (Zeileis and altitudes of 600 – 730 m (data from the São Paulo Forestry et al. 2008); the response variable representing the total abun- Institute). Both areas consist of remnants of cerrado and ri- dance of mesostigmatid mites per host and the explanatory parian forest, and they are 70 km apart from each other. The variables being the host body size (‘host body mass’) and host Cerrado is a Neotropical savannah formation with different sex (‘sex’), with α = 0.05 significance level. In cases when vegetation physiognomies forming a continuum from open GLM negative binominal regression detected that the ex- and dry grasslands to dense forests (Goodland 1971). planatory variable had a significant effect on the total abun- dance of mesostigmatid mites per host, the abundances of each mesostigmatid mite species with highest prevalence estimates Data collection ( 0.5) were modeled using GLM negative binominal regres- sion to access the effects of explanatory host variables (α = The fieldwork was conducted from February 2009 to June 0.05). For model validation analyses, Pearson standardized 2010. Data were obtained from rodents captured during five residuals were used through the graphic residuals analysis of consecutive nights per month in each study area. Captures normal probability. In this method, simulated 95% confidence

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Table I. Prevalence estimates (P%) and abundance (n) of the mesostigmatid mite species collected on rodents of the species O. nigripes at the Experimental Station of Mogi Guaçu (ESMG) and the Experimental Station of Itirapina (ESI), São Paulo, Brazil

P% Mite species n Females Males Total ESMG Family Androlaelaps fahrenholzi 15 13.33 31.25 22.58 Gigantolaelaps oudemansi 32 6.67 6.25 6.45 Gigantolaelaps peruviana 23 20 37.5 29.03 Gigantolaelaps tiphoni 1 6.67 0 3.23 Gigantolaelaps vitzthumi 29 33.33 12.5 22.58 Laelaps paulistanensis 198 73.33 87.5 80.65 Mysolaelaps parvispinosus 182 66.67 87.5 77.42 Family Macronyssidae Ornithonyssus sp. 61 0 6.25 3.23 ESI Family Laelapidae Androlaelaps farenholzi 64 57.14 31.03 42 Androlaelaps rotundus 33 14.29 3.45 8 Gigantolaelaps peruviana 98 52.38 58.62 56 Gigantolaelaps vitzthumi 14 14.29 10.34 12 Laelaps differens 4 0 6.90 4 Laelaps manguinhosi 11 0 3.45 2 Laelaps paulistanensis 306 80.95 82.76 82 Laelaps thori 9 0 3.45 2 Mysolaelaps parvispinosus 292 76.19 86.21 82 Family Macronyssidae Ornithonyssus brasiliensis 1 0 3.45 2 Ornithonyssus monteroi 2 4.76 0 2 Ornithonyssus sp. 18 19.05 24.14 22 bands (envelopes) were constructed using 1,000 simulations to on the prevalence of mesostigmatid species (Table II). The provide a better plot interpretation; if the model is well fitted, total mean abundance was 17.45 (sd = 18.92) mesostigmatid the majority of the points representing the residuals should be mites per individual host, with L. paulistanensis and M. distributed within those bands (Atkinson 1987). All statistical parvispinosus being the most abundant mites (Table I). The procedures were performed using R version 3.1.2 (R Devel- GLM negative binomial regression did not detect the effects opment Core Team 2014). The analysis methodology applied of host body mass and sex on the total abundance of mesostig- used in this study is similar to that described by Fernandes matid mites (Table III). et al. (2012). In ESI, a total of 852 specimens belonging to twelve species of mesostigmatid mites were found on O. nigripes (Table I). L. paulistanensis, M. parvispinosus and Giganto- Results laelaps peruviana were the mesostigmatid species with the highest prevalence estimates (Table I). As in ESMG, the lo- A total of 31 Oligoryzomys nigripes individuals rodents were gistic regression models did not detect any effect of host body captured in ESMG (males = 16 and females = 15), and 50 in- mass and sex on the prevalence of mesostigmatid species in dividuals in ESI (males = 29 and females = 21) during data ESI (Table IV). The total mean abundance was 17.04 (sd = collection. In ESMG, a total of 541 specimens belonging to 10.6) mesostigmatid mites per individual host, with L. paulis- eight species of mesostigmatid mites were found on O. ni- tanensis and M. parvispinosus again being the most abundant gripes (Table I). Laelaps paulistanensis and Mysolaelaps mites (Table I). Unlike ESMG, in ESI the GLM negative bi- parvispinosus were the mesostigmatid species with the high- nomial regression detected the significant effect of the host est prevalence estimates (Table I). The logistic regression body mass on the total abundance of mesostigmatid mites models did not detect the effect of the host body mass and sex (Table V), and the total abundance of mites increased propor-

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Table II. Coefficient estimates of the logistic regression models for mesostigmatid mite species prevalence, as a function of the body mass and sex of the O. nigripes rodent host in ESMG, São Paulo, Brazil

Species Estimate S.E. Z p-value A. farenholzi Intercept –1.904 1.741 –1.093 0.274 Host body mass 0.002 0.101 0.02 0.984 Sex 0.934 2.581 0.362 0.717 Host body 0.006 0.132 0.048 0.962 G. oudemansi Intercept –95.239 29380.570 –0.003 0.997 Host body mass 3.187 1037.161 0.003 0.998 Sex 78.934 29380.573 0.003 0.998 Host body –2.676 1037.161 –0.003 0.998 G. peruviana Intercept –1.700 1.475 –1.152 0.249 Host body mass 0.02 0.083 0.242 0.809 Sex –1.937 2.927 –0.662 0.508 Host body 0.12 0.135 0.888 0.374 G. tiphoni Intercept –2.518 2.393 –1.052 0.293 Host body mass –0.008 0.144 –0.056 0.956 Sex –18.05 15460 –0.001 0.999 Host body 0.008 687.100 0 1 G. vitzthumi Intercept –0.525 1.264 –0.415 0.678 Host body mass –0.011 0.075 –0.147 0.883 Sex –2.749 3.4 –0.809 0.419 Host body 0.07 0.152 0.463 0.643 L. paulistanensis Intercept –1.31 1.826 –0.717 0.473 Host body mass 0.172 0.141 1.22 0.222 Sex 10.251 6.087 1.684 0.092 Host body –0.456 0.258 –1.764 0.078 M. parvispinosus Intercept 1.103 1.263 0.873 0.383 Host body mass –0.026 0.072 –0.365 0.715 Sex 7.839 5.942 1.319 0.187 Host body –0.257 0.228 –1.128 0.259 Ornithonyssus sp. Intercept –20.57 10510 –0.002 0.998 Host body mass 0 614.1 0 1 Sex 16.22 10510 0.002 0.999 Host body 0.072 614.1 0 1

Table III. Coefficient estimates of the GLM negative binomial regression for the total abundance of the mesostigmatid mites, as a function of the body mass and sex of the O. nigripes rodent host in ESMG, São Paulo, Brazil

Coefficients Estimate S.E. Z p–value Intercept 1.962 0.542 3.618 < 0.001 Host body mass 0.035 0.031 1.104 0.27 Sex 1.079 0.95 1.135 0.256 Host body mass*Sex –0.032 0.047 –0.691 0.49

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Table IV. Coefficient estimates of the logistic regression models for mesostigmatid mite species prevalence, as a function of the body mass and sex of the O. nigripes rodent host in ESI, São Paulo, Brazil

Species Estimate S.E. Z p–value A. farenholzi Intercept -0.775 2.012 –0.385 0.7 Host body mass 0.049 0.09 0.539 0.59 Sex –0.856 2.64 –0.324 0.746 Host body –0.015 0.113 –0.129 0.897 A. rotundus Intercept -5.587 3.325 –1.681 0.093 Host body mass 0.163 0.133 1.228 0.219 Sex 11.987 10.671 1.123 0.261 Host body –0.65 0.572 –1.135 0.256 G. peruviana Intercept -2.023 2.099 –0.964 0.335 Host body mass 0.097 0.094 1.028 0.304 Sex 1.563 2.645 0.591 0.555 Host body –0.063 0.115 –0.553 0.58 G. vitzthumi Intercept 1.906 3.056 0.624 0.533 Host body mass –0.181 0.155 –1.165 0.244 Sex –4.19 3.996 –1.049 0.294 Host body 0.186 0.186 0.998 0.318 L. differens Intercept -20.57 17410 –0.001 0.999 Host body mass 0 774.7 0 1 Sex 12.68 1741 0.001 0.999 Host body 0.195 774.7 0 1 L. manguinhosi Intercept –20.57 17410 –0.001 0.999 Host body mass 0 774.7 0 1 Sex 17.36 17410 0.001 0.999 Host body –0.005 774.7 0 1 L. paulistanensis Intercept 1.006 2.492 0.404 0.686 Host body mass 0.02 0.113 0.18 0.857 Sex –3.183 3.589 –0.887 0.375 Host body 0.146 0.165 0.889 0.374 L. thori Intercept -21.57 28700 –0.001 0.999 Host body mass 0 1277 0 1 Sex 27.97 28700 0.001 0.999 Host body –0.487 1277 0 1 M. parvispinosus Intercept –0.135 2.326 –0.058 0.954 Host body mass 0.06 0.107 0.562 0.574 Sex 2.231 3.254 0.686 0.493 Host body –0.071 0.14 –0.507 0.612 O. brasiliensis Intercept -21.57 28700 –0.001 0.999 Host body mass 0 1277 0 1

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Sex 14.67 28700 0.001 1 Host body 0.135 1277 0 1 O. monteroi Intercept –2.155 4.566 –0.472 0.637 Host body mass –0.039 0.211 –0.185 0.853 Sex –19.41 22930 –0.001 0.999 Host body 0.039 921.6 0 1 Ornithonyssus sp. Intercept –0.171 2.511 –0.068 0.946 Host body mass –0.059 0.117 –0.51 0.61 Sex –2.25 3.13 –0.719 0.472 Host body 0.111 0.137 0.811 0.417

Table V. Coefficient estimates of the GLM negative binomial regression for the total abundance of the mesostigmatid mites, as a function of the body mass and sex of the O. nigripes rodent host in ESI, São Paulo, Brazil

Coefficients Estimate S.E. Z p–value Intercept 1.088 0.631 1.724 0.085 Host body mass 0.079 0.028 2.859 0.004 Sex 1.003 0.804 1.247 0.212 Host body mass*Sex –0.051 0.034 –1.495 0.135

Table VI. Coefficient estimates of the GLM negative binomial regression for the abundance of the mesostigmatid mite species with highest prevalence estimates, as a function of the body mass and sex of the O. nigripes rodent host in ESI, São Paulo, Brazil

Coefficients Estimate S.E. Z p-value G. peruviana Intercept –0,624 1,307 –0,477 0,633 Host body mass 0,065 0,057 1,14 0,254 Sex 0,419 1,691 0,248 0,804 Host body mass*Sex –0,036 0,071 –0,5 0,617 L. paulistanensis Intercept -0.540 1.064 –0.508 0.612 Host body mass 0.099 0.047 2.132 0.033 Sex 1.546 1.341 1.153 0.249 Host body mass*Sex –0.065 0.057 –1.136 0.256 M. parvispinosus Intercept 1.262 1.072 1.178 0.239 Host body mass 0.027 0.048 0.573 0.566 Sex –0.25 1.378 –0.182 0.856 Host body mass*Sex 0.0001 0.059 0.001 0.999

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Fig. 1. Variation in the total abundance of mesostigmatid mites as a function of the body mass of O. nigripes host individuals

Fig. 2. Normal probability plot of Pearson residuals, with a simulated envelope from the negative binomial regression model

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tionally to host body mass (Fig. 1). The probability plot of in the environment. For ectoparasitic mites, in which only the Pearson standardized residuals shows that the majority of the dispersing stage (females) is harbored in the host, the size of points that represent the residuals are distributed within the the host individual seems to be indicative of the number of ec- confidence bands, indicating that the model is valid (Fig. 2). toparasites that it is capable of aggregating and transporting. The GLM negative binominal regression analysis of the mite Due to their larger metabolic requirements, larger individ- species with highest prevalence estimates in ESI, i.e. L. paulis- uals can have greater mobility, which increases their suscep- tanensis, M. parvispinosus and G. peruviana, detected that tibility to parasitic infection by contact with infective stage of host body mass had a significant effect on the abundance of L. the parasite, and by parasitic exchange with other individuals paulistanensis only (Table VI). (Bordes et al. 2009). The parasitic exchange can be influenced by the host density and the number of host species sharing the same parasites (Arneberg et al. 1998; Krasnov et al. 2002; Fer- Discussion nandes et al. 2012). Fernandes et al. 2012 showed that the abundance of lice parasitizing the host Oligoryzomys nigripes These results indicated the presence of an aggregate distribu- in ESI was significantly higher than in ESMG, probably as a tion of the ectoparasitic mite species, described by the nega- reflection of both a higher host density and a greater number tive binomial distribution. This distribution, with many host of host species occurring in ESI. individuals harboring few or no parasites and a few host indi- Lower quality habitats (e.g. higher anthropogenic influ- viduals having many parasites, is a usually pattern observed in ence, lower host density, fewer host species sharing the same host–parasite relationships (Shaw et al. 1998; Poulin 2007). parasites, lower species richness of parasites) may feature dif- The two most abundant species of mites, Laelaps paulis- ferent parasite-host dynamics because of a lack of the many in- tanensis and Mysolaelaps parvispinosus, belong to the family traspecific and interspecific relationships that occur in habitats Laelapidae. In many species of Laelapidae mite, the general of higher quality. During our fieldwork, five rodent species life cycle is reduced by the retention of the egg and sometimes and twelve mesostigmatid mite species were captured in ESI, the larvae by the parent mite, which protects the young from whereas three rodent species and eight mesostigmatid mite mortality factors that would affect the initial stages of devel- species were captured in ESMG. opment (Radovsky 1994). The predominance of females in In conclusion, we found that the body mass of the host the majority of the collected species of Laelapidae mites is species O. nigripes was the most important factor influencing consistent with the hypothesis that males and nymphs remain the abundance of ectoparasitic mites in ESI (a locality of in the host nest, while females disperse (Radovsky 1994; Mar- higher quality than ESMG), probably because bigger host in- tins-Hatano et al. 2002). Some laelapid mites are unable to re- dividuals are more mobile, and allow for a greater coexistence produce without the inclusion of vertebrate blood in their diet of parasitic individuals. Moreover, when the host moves to a (Downling 2006), which is a possible explanation for why fe- new nest, female mites are responsible for nest infestation and males are more commonly found on hosts. transmission to other host individuals. Mite abundance is influenced by host body mass in ESI. The hypothesis of the "well-fed host" states that parasites Acknowledgments. We want to thank the Experimental Station of choose bigger hosts because they are better fed, increasing the Mogi Guaçu and the Experimental Station of Itirapina for authoriz- ing this study and for providing the logistical support. We thank Dr. parasite’s ability to acquire food (Hawlena et al. 2005). Moore Gilberto Salles Gazeta and his team from the Oswaldo Cruz Foun- and Wilson (2002) observed the influence of mammalian dation (FIOCRUZ-RJ) for the identification of the collected mites. species body size on parasite load. In species where the male Fernanda Rodrigues Fernandes and Leonardo Dominici Cruz re- is the larger sex, they are the ones more frequently parasitized, ceived PhD fellowships from the Coordination for the Improvement whereas in species in which females are the larger sex, they are of Higher Education Personnel (CAPES). This research was funded by the Research Foundation of the State of São Paulo (FAPESP, the ones most affected. Brazil: 2008/56231-2). If a host represents a patch of parasite habitat with char- acteristics that vary both spatially and temporarily, the size of the patch can influence the amount of organisms that it is ca- References pable of supporting. 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Received: October 9, 2014 Revised: February 20, 2015 Accepted for publication: April 1, 2015

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