Sex and season explain spleen weight variation in the Egyptian mongoose

Sex and season explain spleen weight variation in the Egyptian mongoose The Egyptian mongoose (Herpestes ichneumon Linnaeus, 1758) is a medium-sized carnivore that experienced remarkable geographic expansion over the last 3 decades in the Iberian Peninsula. In this study, we investigated the association of species-related and abiotic factors with spleen weight (as a proxy for immunocompetence) in the species. We assessed the relationship of body condition, sex, age, season, and environmental conditions with spleen weight established for 508 hunted speci- mens. Our results indicate that the effects of sex and season outweigh those of all other variables, including body condition. Spleen weight is higher in males than in females, and heavier spleens are more likely to be found in spring, coinciding with the highest period of investment in reproduction due to mating, gestation, birth, and lactation. Coupled with the absence of an effect of body condi- tion, our findings suggest that spleen weight variation in this species is mostly influenced by life- history traits linked to reproduction, rather than overall energy availability, winter immunoenhance- ment, or energy partitioning effects, and prompt further research focusing on this topic. Key words: body condition, carnivore, Herpestes ichneumon, Iberian Peninsula, mongoose, spleen weight. The vertebrate immune system must respond to antigenic challenges environmental scenarios (Vicente et al. 2007). Immunocompetence that irreversibly affect life-history traits and energy allocation trade- can be affected by seasonal variations or by sex or indeed by interac- offs (Schulte-Hostedde and Gooderham 2011). Since it directly tions between these 2 factors. Despite this fact, to date, studies influences survival, indicators of immunocompetence may help to focusing on immune competence that use spleen weight as an indica- disentangle the factors underlying species success under different tor lack samples covering all seasons of the year (e.g., Corbin et al. V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 2008; Schulte-Hostedde and Elsasser 2011) or from both sexes 1995), stress (Young and Monfort 2009), ectoparasitism (Perez- (e.g., Schulte-Hostedde and Elsasser 2011). In order to investigate Orella and Schulte-Hostedde 2005), and prey selection (Pierce et al. the factors that influence variance in immunocompetence within a 2000). Regarding its relationship with immunocompetence, body species, samples covering a broad range of environmental condi- condition has been proposed to influence spleen weight through tions, demographic groups, and all periods of the life-cycle are ne- overall energy availability (Ponlet et al. 2011; Schulte-Hostedde and cessary. The Egyptian mongoose Herpestes ichneumon is an Elsasser 2011) and energy partitioning effects (Vicente et al. 2007). appropriate model for such a study because it has colonized main- Therefore, body condition can be used as an indicator controlling land Portugal over the past 30 years (Barros and Fonseca 2011), cur- for energetic state and overall health when studying spleen weight as rently inhabiting a diverse array of habitats representing all a proxy of immune competence. environmental conditions available to the species. Furthermore, In this work, we set out to understand spleen weight variation in legal hunting generates a large number of specimens year-round of a sample of free-ranging Egyptian mongoose. If increased spleen both sexes and all ages from the entire distributional range. weight is simply a result of the availability of energy to invest in im- The spleen is the primordial secondary lymphoid organ in mam- munity, we expected it to be primarily associated with higher body mals, playing a key role in immune defense (Corbin et al. 2008). It is condition scores. Alternatively, spleen weight variation may result functionally and histologically divided into red pulp and white pulp from energy partitioning effects and trade-offs between key biologic- (Mebius and Kraal 2005). The red pulp ensures blood filtration, re- al functions, in which case we expected to find decreased spleen moval of effete erythrocytes, regeneration of free ferrous iron, and weight during periods of maximum investment in reproduction or pathogen clearance (Mebius and Kraal 2005). The white pulp growth. However, if spleen weight variation results from more spe- houses lymphoid components under resting conditions, such as cific or complex interactions, we might find it associated with one T cells, B cells, and antigen-presenting cells (Mebius and Kraal or more demographic, environmental, or life-history variables. 2005). Maintaining the immune system is energetically costly, and Finally, if increased spleen weight is the result of an immune re- individuals with better body condition are likely to have a greater sponse to parasitism, the cost of that response might be reflected in capacity for the production and storage of lymphocytes (Ponlet et al. body condition, with higher spleen weight values associated with 2011; Schulte-Hostedde and Elsasser 2011), which may translate poorer body condition scores. into heavier spleens. Spleen weight is considered a reliable proxy of individual immunocompetence, notwithstanding its other functions (Hosken and O’Shea 2001; Corbin et al. 2008; Hadidi et al. 2008; Materials and Methods Navarro-Gonzalez et al. 2011; Manjerovic and Waterman 2012). Study area At the intraspecific level, larger spleens may reflect greater invest- Wild Egyptian mongoose specimens were collected from 13 of the ment in immunity by healthy individuals with better body condition 18 districts of continental Portugal. Geographic origin of the speci- (Møller et al. 1998b), whereas smaller spleens suggest the opposite mens was attributed to either north or south of the Tagus River, (Dı ´ez-Leo ´ n et al. 2013). However, the use of spleen weight to evalu- given the marked differences in bioclimatic, biogeographic, and an- ate within-species immunocompetence has limitations. Sudden thropogenic pressures previously observed between both regions increases in spleen weight due to intense physical exertion and stress (Bandeira et al. 2016, 2018). The Tagus River was previously con- (Corbin et al. 2008) or ongoing infection might bias estimates relat- sidered a geographical barrier for the species, since the distribution ing to immune capacity (Gou ¨ y de Bellocq et al. 2007). The relative of the Egyptian mongoose was more concentrated in the south until amount of red blood cells stored in the mammalian spleen is known 3 decades ago (Borralho et al. 1996; Barros and Fonseca 2011). to vary depending on stress, exercise, or hemorrhagic trauma The vegetation of the southern region is mainly characterized by (Brendolan et al. 2007). Alternatively, enlargement of the spleen evergreen Quercus, whereas in the north monoculture plantations of may reflect an immune response to parasitism (Nunn 2002; Gou ¨y de Eucalyptus sp. have largely replaced Pinus pinaster and native de- Bellocq et al. 2007; Corbin et al. 2008), or inflammation due to ciduous trees (Alves et al. 2009). The northern region generally pathological changes (Møller et al. 1998a). Finally, in addition to a presents lower temperatures and higher levels of rainfall compared dependence on body condition, spleen weight may also be influ- with the southern region (Hijmans et al. 2005). Furthermore, human enced by energy partitioning and trade-offs between reproduction pressure is lower in the south, having fewer urbanized areas, a lower and growth (Vicente et al. 2007). Therefore, simultaneous consider- population density, a less extensive road network, and fewer frag- ation of indicators of overall health and energetic state (e.g., body mented habitats (Alves et al. 2009; European Commission 2015; condition), as well as information on season, sex, age, and environ- IGP 2015). Also, there are fewer mountainous ridges and a less ex- mental conditions can help overcome these limitations, facilitating tensive hydrographic network south of the Tagus River (SNIRH use of spleen weight as a proxy of immunocompetence. 2015). Body condition also can be altered by environmental conditions or individual traits such as sex or age (Toı¨go et al. 2006). Body con- Sampling procedures dition refers to the amount of energy reserves (such as fat and pro- Sampling took place between January 2008 and December 2014. tein) that an animal possesses (Perez-Orella and Schulte-Hostedde Capture date was classified as winter (January–March), spring 2005; Schulte-Hostedde et al. 2005), and it represents the energetic (April–June), summer (July–September), or autumn (October– state of an animal (Schulte-Hostedde et al. 2001). Body condition December). Specimens were obtained from hunting activities (box- scores have been developed as bioindicators of overall health or the trapped under legal game management actions aimed at controlling physical quality of individual specimens (Peig and Green 2009). predator densities), according to legal requirements and under li- Several studies have assessed the relationship between body condi- tion of mammals and a range of ecological parameters (Green cense from competent authorities [Instituto da Conservac¸ao da 2001), including animal density and fecundity (Stewart et al. 2005), Natureza e das Florestas (ICNF)]. A total of 508 Egyptian mon- the effect of parturition and weight of litter (Dobson and Michener gooses were included in this study, 266 females and 242 males. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Bandeira et al.  Sex, season, and spleen weight variation 3 Table 1. Numbers of Egyptian mongoose samples obtained for each region, North and South of the Tagus River, together with in- formation on age cohort and sex Age Sex Region North South Adult Female 41 107 Male 35 80 Sub-adult Female 12 33 Male 16 23 Juvenile II Female 4 34 Male 9 47 Juvenile I Female 4 31 Male 9 23 Total Female 61 205 Male 69 173 There were 263 adults, 84 sub-adults, 94 type II juveniles, and 67 type I juveniles (Table 1, see definitions below). Age was deter- mined by dentition according to Bandeira et al. (2016). Each speci- men was assigned to 1 of 4 age cohorts: adults over 1 year of age, sub-adults between 9 and 12 months, type II juveniles between 5.5 and 9 months, and type I juveniles between 2.5 and 5.5 months of age. Regarding geographic origin, 130 specimens came from north of the Tagus River and 378 from the south (Figure 1 and Table 1). Carcasses were labeled with collection date and location and stored at 20 C until processed. In the laboratory, samples were thawed, sexed, weighed, measured, and dissected. Spleens were collected and weighed separately. Six biometric measurements (Bandeira et al. 2016) were taken: snout–tail length (terminal hairs not included); Figure 1. Locations and sample sizes of Egyptian mongoose studied from dis- right hind leg length; right hind foot length; shoulder height; neck tricts in Portugal. perimeter; and head width. Only specimens for which age determin- ation was possible and that possessed an intact spleen were assessed. areas) representing habitat structure were retrieved from a Corine Pregnant females were excluded to avoid bias from body weight and Land Cover (2006) dataset with a spatial resolution of 250 m and body condition variables. converted in a single categorical variable represented by the most abundant habitat type in each grid cell. Hydrographic data were Environmental variables obtained from the Sistema Nacional de Informac¸~ ao de Recursos Based on ecological requirements and physiological characteristics Hı ´dricos (SNIRH 2015). The degree of anthropogenic pressure was of Egyptian mongoose, we selected 5 environmental variables that represented by 2 variables: population density [derived from the could directly or indirectly influence body condition and spleen European Commission (2015)] and extent of the road network weight for modeling (e.g., Ben-Yaacov and Yom-Tov 1983; Delibes (IGP 2015). Geographic position of collected samples was reported et al. 1984; Palomares and Delibes 1990, 1991a; Palomares 1993b; in terms of latitude and longitude. Abundances of Egyptian mon- Barros et al. 2015; Bandeira et al. 2016, 2018). Landscape structure goose (number of animals/400 ha) based on the number of animals can influence physical condition due to differences in the amount of hunted in each area and during the month, where and when each suitable habitat, prey availability, and its impact on the movement Egyptian mongoose sampled was collected, were established accord- ing to annual hunting yields (ICNF, unpublished data). and dispersal of mongooses (Palomares and Delibes 1993a; Palomares 1994; Bandeira et al. 2018). Habitat change in recent decades seems to have favored the expansion of mongoose popula- Statistical procedures tions into new territories (Barros et al. 2015). Anthropogenic factors All variables were tested for normality with Kolmogorov–Smirnov are a ubiquitous influence on ecosystems and, together with natural tests (with Lilliefors correction for the significance level) (Zar 1999). barriers, act as constraints on mongoose expansion, thereby shaping The principal component analysis (PCA) enables a single esti- this species’ distribution (Barros et al. 2015). We included anthropo- mate of body size on the first component, based on the covariance genic factors in our study to assess possible associations with physic- matrix of various measures. Body size was calculated by combining al condition and immunocompetence, which we expected to be specimen weight and the 6 biometric measurements into a single better in areas with low human pressure. value through a PCA, using all variables with loadings >0.70. Each variable was represented by mean values in 2 2 km grid The PCA was performed in STATISTICA version 7.1 (Stat Soft Inc., cells, considering the critical home area of the Egyptian mongoose 2005). Spleen weight was corrected for body weight and is reported (Palomares and Delibes 1991b). Nine variables (urban, rice fields, as spleen weight (in grams) per 100 g of total specimen mass agro-forestry, shrubs, inland water bodies, vineyards and orchards, (adjusted spleen weight). Body condition was scored according to coniferous forest, broadleaved and mixed forests, and agricultural the Scaled Mass Index (Peig and Green 2009, 2010). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Table 2. Model selection, using AICc, for the effect of age, season, sex, and their interactions, together with region, Egyptian mongoose abundance, habitat, extent of river network, and body condition (Scaled Mass Index), on adjusted spleen weight (expressed as g/100 g body weight) of the Egyptian mongoose in Portugal Models df AICc DAICc AICc weight R Season1 sex 7 2142.27 0.00 0.67 0.28 Season þ region þ sex 8 139.89 2.38 0.21 0.20 Egyptian mongoose abundance þ sex 5 135.78 6.49 0.03 0.26 Season 6 135.69 6.58 0.03 0.25 Sex 4 135.12 7.15 0.02 0.17 Season þ Egyptian mongoose abundance þ sex 8 135.01 7.26 0.02 0.31 Season þ region 7 134.16 8.11 0.01 0.17 Region þ sex 5 133.48 8.79 0.01 0.06 Season þ region þ Egyptian mongoose abundance þ sex 9 132.08 10.20 0.00 0.24 Region þ Egyptian mongoose abundance þ sex 6 131.99 10.28 0.00 0.20 Season þ Egyptian mongoose abundance 7 129.10 13.17 0.00 0.28 Egyptian mongoose abundance 4 128.95 13.32 0.00 0.23 Season þ region þ Egyptian mongoose abundance 8 126.91 15.36 0.00 0.21 (Null) 3 126.76 15.51 0.00 0.13 Region 4 126.32 15.95 0.00 0.03 Season þ sex þ season * sex 10 126.27 16.00 0.00 0.28 Region þ Egyptian mongoose abundance 5 125.76 16.51 0.00 0.17 Season þ sex þ scaled mass index 8 125.50 16.77 0.00 0.25 Season þ region þ sex þ season * sex 11 124.32 17.95 0.00 0.21 Season þ region þ sex þ scaled mass index 9 124.21 18.06 0.00 0.13 Season þ age þ sex 10 122.46 19.81 0.00 0.29 Ageþ sex 7 122.44 19.83 0.00 0.22 Notes: Models considered as explanatory are in bold. DAICc is the difference between the AIC yielded by each model and the lowest AICc (considered the best model); df, degrees of freedom. All explanatory variables were checked for collinearity using Results variance inflation factors (VIFs) (Zuur et al. 2009). A cut-off value The PCA of specimen body size explained 74.6% of the variance in of 2.5 was used to drop collinear variables. The predictor with the this parameter, with an eigenvalue of 5.220. highest VIF value was removed in a stepwise procedure, removing Two variables of anthropogenic factors (population density and one variable at a time, recalculating the VIF values, until all the extent of road network) and the variable body size were excluded remaining predictors had a VIF 2.5 (Zuur et al. 2009). Only from the initial set of predictors for adjusted spleen weight, as well those that presented VIF 2.5 were retained for model construc- as for body condition model construction, to avoid multicollinearity tion. Models explaining variation in spleen weight or body (Tables A1 and A2). Only one model (seasonþ sex) with DAICc< 2 condition included the discrete variables region, habitat, sex, age (AICc¼142.27, df¼ 507) could be considered explanatory and season and the interactions seasonsex, seasonage, and (Tables 2 and 3). Overall, males presented higher adjusted spleen sex age, as well as the continuous variables Egyptian mongoose weight than females, and spleens were heaviest in spring, followed abundance, population density, extents of the road and river net- by winter and autumn, and they were lightest in summer (Table 3, work, and body size, that were not excluded by VIF analysis. Body see details in Figures A1 and A2). Despite the fact that the inter- condition score was used as an explanatory variable in our model action sex  season was not explanatory in our model, an analysis of construction for spleen weight, and vice versa. For mixed the means of spleen weight for each sex-season group revealed dif- modeling, we used Gaussian distribution, identity link function, ferent seasonal trends between males and females (Figure A3). In and district (first-level administrative subdivision of mainland males, adjusted spleen weight was highest in winter and decreased in Portugal, compartmentalized based on history, common land use, spring, reaching its lowest value in summer, before increasing again and related issues) as a random factor to control for non- in autumn. However, in females, adjusted spleen weight reached its independence of samples from the same area. highest values in spring and remained low in the other 3 seasons of Selection of models explaining either spleen weight or body con- the year. dition variation was performed separately according to the proced- For body condition analyses, only one model with DAICc< 2 ure described in Zuur et al. (2009), whereby a ranking was made of (AICc¼ 7089.62, df¼ 507) was considered explanatory (Table 4). all possible models using the Akaike Information Criterion (AICc) It included the variables: spleen weightþ seasonþ ageþ sex þ (Burnham and Anderson 2002) and only those with DAICc values season ageþ seasonsex þ agesexþ habitatþ regionþ Egyptian <2 were considered explanatory. The residual patterns were mongoose abundance (Tables 4 and 5). Males presented higher checked. body condition scores than females (Table 5). Juvenile type I All statistical analyses were performed in R (version 2.13.2) Egyptian mongooses had higher body condition scores compared using the packages lme4 (Bates et al. 2014)and MuMIn for with adults, sub-adults, and juveniles type II, in descending order, multimodel selection and model averaging approaches (Barton respectively (Table 5). Animals collected in autumn presented the 2012). highest body condition scores, followed by those collected in winter, Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Bandeira et al.  Sex, season, and spleen weight variation 5 spring, and summer (Table 5). Specimens with heavier spleens pre- immunity, larger spleens may indicate more competent immune sys- sented higher body condition scores (Table 5). Mongooses captured tems, allowing animals to attain better body condition scores. In general, the adjusted spleen weight of male mongooses is sig- from places with lower abundances of conspecifics had higher body nificantly higher than that of females, contrasting with results for condition, as well as those from the south (Table 5). Specimens col- red deer Cervus elaphus in which spleen weight adjusted for body lected from vineyards and orchards, rice fields, and urban habitats size does not differ between sexes (Corbin et al. 2008). Our data had the highest body condition scores (Table 5). Some selected fac- also show that adjusted spleen weight varies across seasons. In tors are graphically presented in Figures A4–A6. spring, our Egyptian mongoose specimens presented the highest spleen weights, with a slight decrease in values during winter, and Discussion an abrupt decrease in summer, followed by a rise again in autumn. To our knowledge, this is the first time that year-round spleen Based on a large sample of free-ranging Egyptian mongoose of both weight measurements have been presented for a wild carnivore spe- sexes and all ages, sampled from throughout Portugal and year- cies. A study on wild male American mink Neovison vison (Persson round, our study shows that sex and season explain the variation in et al. 2011) and a report focusing on wild boar Sus scrofa adjusted spleen weight. We found no evidence for an effect of body (Ferna ´ ndez-Llario et al. 2004) showed that animal spleens were condition score on spleen weight in the explanatory model, contra- heaviest during winter, but these studies only compared data from 3 dicting the hypothesis that spleen weight depends primarily on the and 2 seasons, respectively. Two hypotheses are offered in previous availability of energy to invest in immune function (Ponlet et al. studies to explain seasonal variation in indicators of immunity in 2011; Schulte-Hostedde and Elsasser 2011). In fact, our results sug- vertebrates (Martin et al. 2008). The first is the winter immunoen- gest the opposite causal relationship, with spleen weight appearing hancement hypothesis, whereby animals up-regulate their immune as one of the factors in the model explaining the variation in body activity as a response to changes in photoperiod, to compensate for condition score. The directionality apparent from these results sug- the immunosuppressive effects of winter temperatures and resource gests that even though higher body condition scores may not neces- scarcity (Sinclair and Lochmiller 2000). The second is the trade-off sarily imply larger spleens and a greater ability to invest energy in hypothesis according to which the high cost of immune activity is in- compatible with other costly physiological activities that occur at Table 3. Effects of the model considered as explanatory for certain times of the year, such as reproduction (Vicente et al. 2007). adjusted spleen weight (expressed as g/100 g body weight) of the Deeper analysis is necessary to determine which mechanism under- Egyptian mongoose in Portugal lies the influence of sex and season on spleen weight in this Egyptian mongoose population. Since an increase in spleen weight in spring is Variables Estimate Standard error t-Value apparently incompatible with the winter immunoenhancement hy- Intercept 0.328 0.023 14.197 pothesis for seasonal variation in immunity (Martin et al. 2008), we Sex Male 0.054 0.015 3.712 speculate that different reproductive strategies, sex-specific behav- Season Spring 0.081 0.020 4.079 ior, and physiological variations may also be linked to spleen weight Summer 0.026 0.020 1.285 variation, especially since the Egyptian mongoose is a polygynic Winter 0.071 0.023 3.142 species (Palomares 1993a), exhibiting differential investment in Table 4. Model selection, using AICc, for the effect of age, season, sex, and their interactions, together with region, Egyptian mongoose abundance, habitat, extent of river network, and adjusted spleen weight (expressed as g/100 g body weight), on body condition (Scaled Mass Index) of the Egyptian mongoose in Portugal Models df AICc DAICc AICc weight R Spleen weight1 season1 habitat1 age1 region1 Egyptian mongoose abundance1 sex 34 7,089.62 0.00 0.88 0.11 1 season3age1 season3sex1 age3sex Spleen weight þ season þ habitat þ age þ region þ sex þ season3age þ season3sex þ age3sex 33 7,094.83 5.21 0.07 0.11 Spleen weight þ season þ habitat þ age þ region þ river network þ Egyptian mongoose abundance 35 7,096.02 6.40 0.04 0.11 þ sex þ season3age þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ Egyptian mongoose abundance þ sex þ season3age 33 7,097.90 8.28 0.01 0.12 þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ region þ river network þ sex þ season3age þ season3sex 34 7,101.54 11.92 0.00 0.11 þ age3sex Season þ habitat þ age þ region þ Egyptian mongoose abundance þ sex þ season3age þ season3sex 33 7,103.01 13.39 0.00 0.12 þ age3sex Spleen weight þ season þ habitat þ age þ sex þ season3ageþ season3sex þ age3sex 32 7,103.15 13.53 0.00 0.12 Spleen weight þ season þ habitat þ age þ river network þ Egyptian mongoose abundance þ sex 34 7,104.00 14.39 0.00 0.11 þ season3age þ season3sex þ age3sex Season þ habitat þ age þ region þ sex þ season3age þ season3sex þ age3sex 32 7,108.72 19.10 0.00 0.12 Season þ habitat þ age þ region þ river network þ Egyptian mongoose abundance þ sex 34 7,109.47 19.85 0.00 0.11 þ season3age þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ river network þ sex þ season3age þ season3sex þ age3sex 33 7,109.59 19.97 0.00 0.11 Notes: Models considered as explanatory are in bold. DAICc is the difference between the AIC yielded by each model and the lowest AICc (considered the best model); df, degrees of freedom. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Table 5. Effects of the model considered as explanatory for body showed a peak in spring, thus again contradicting the reproductive condition (Scaled Mass Index) of the Egyptian mongoose in trade-off scenario. Portugal Animals are expected to have larger spleens during active infec- tion due to increased lymphocyte production and/or pathological in- Variables Estimate Standard error t-Value flammation (Møller et al. 1998a) or parasitism (Nunn 2002; Gou ¨y Intercept 1,878.46 80.44 23.351 de Bellocq et al. 2007; Corbin et al. 2008), so we must consider a Sex Male 59.80 76.10 0.786 third hypothesis, whereby these seasonal differences in spleen weight Age Juvenile 1 3.96 128.17 0.031 can be influenced by parasitism. Additionally, pathogen infection Juvenile 2 226.44 86.41 2.621 and parasite burden may be more pronounced in males of polygyn- Sub-adult 70.07 91.39 0.767 ous species (Moore and Wilson 2002; Perez-Orella and Schulte- Season Spring 113.97 74.15 1.537 Summer 187.89 76.52 2.455 Hostedde 2005), which has been attributed to sexual selection, com- Winter 111.04 81.22 1.367 petition, and larger home ranges (Zuk 1990). Unfortunately, the Region South 53.18 57.99 0.917 lack of measures of diversity and abundance of parasites in our Spleen weight 181.37 79.61 2.278 study is a major limitation to investigate this effect. However, costly Egyptian mongoose abundance 10.09 8.44 1.195 immune responses to parasitism and high parasite burdens are often Habitat Agro-forestry 41.35 61.20 0.676 negatively correlated with body condition (e.g., Irvine et al. 2006; Broadleaved and 5.81 42.05 0.138 mixed forests Davidson et al. 2015; Taylor et al. 2018). Therefore, the fact that in Rice fields 80.84 254.03 0.318 our sample the peak in spleen weight coincides with peaks in body Shrubs 9.47 82.46 0.115 condition for both sexes apparently conflicts with a parasite-driven Urban 61.44 122.44 0.502 variation in spleen weight, and highlights the need for further Vineyards and orchards 115.56 170.09 0.679 research. Sexage MaleJuvenile I 3.28 104.63 0.031 In summary, body condition does not predict spleen weight vari- MaleJuvenile II 49.27 94.62 0.521 ation in this Egyptian mongoose population, which instead is pri- MaleSub-adult 96.32 93.66 1.028 Sexseason MaleSpring 93.12 91.93 1.013 marily explained by sex and season. Moreover, spleen weight peaks MaleSummer 109.86 90.44 1.215 in spring and coincides with the period of maximum reproductive MaleWinter 71.71 99.91 0.718 investment for the species, thus contradicting the winter immunoen- Seasonage SpringJuvenile I 30.38 158.76 0.191 hancement and reproductive trade-off hypotheses. Nevertheless, the SpringJuvenile II 304.12 133.21 2.283 coincidence of the peaks in spleen weight trends with the period of SpringSub-adult 156.35 126.01 1.241 maximum investment in reproduction for each sex suggests that SummerJuvenile I 115.86 137.33 0.844 spleen weight variation is closely related to the species’ reproductive SummerJuvenile II 261.95 107.34 2.440 SummerSub-adult 129.61 172.67 0.751 biology. This relationship warrants further research to establish if it WinterJuvenile I 320.24 276.42 1.159 is a consequence of reproductive behavior, a biologically timed in- WinterJuvenile II 236.69 198.20 1.194 vestment to prepare for a challenging period in terms of immunity WinterSub-adult 32.04 112.64 0.284 or simply a result of seasonal host–pathogen dynamics. Author Contributions reproduction and sex-skewed survival (Palomares 1993a; Palomares and Delibes 1993b). V.B., E.V., and C.F. conceived and designed the experiments. V.B. According to a study on the reproductive parameters of the and A.A. performed the experiments. V.B. and E.V. analyzed the Egyptian mongoose in Spain, courtship and mating begin in winter data and performed the statistical analyses. J.C. generated maps and and extend almost to the end of spring (Palomares and Delibes provided ecological, habitat, and climatic data. V.B., E.V., A.A., 1992). During the breeding season, males engage in physical aggres- M.V.C., and C.F. wrote the manuscript. All authors contributed to sion to defend their territory, to gain access to females, to mate, and the development of ideas and approved the final version of the to compete for prey (Palomares 1991, 1993a). Therefore, male in- manuscript. vestment in immune function may decrease during the reproductive period, since energetic resources should be directed primarily toward reproduction and less toward immune responses (Zuk and Acknowledgments Stoehr 2002; Stoehr and Kokko 2006). However, our results do not Thanks are due to collectors, hunters, entities managing hunting areas and support this trade-off hypothesis because spleen weight in our sam- their representatives (namely FENCAC¸A, ANPC, and CNCP), to Tapada ple of males actually tends toward its highest levels in winter. In Nacional de Mafra, and to all that contributed to animal sampling, as well as Spain, pregnant Egyptian mongooses are observed mostly in March ICNF for the capture permits. We thank Carlos Pimenta (DGPC-Laborato ´ rio and April (Palomares and Delibes 1992). We also observed this pat- de Arqueocie ˆ ncias, SEC—Direc¸~ ao Geral do Patrimo ´ nio Cultural) for instruc- tern in our sample, with 80% of pregnancies detected in the 3 spring tions on a method for cleaning skulls. We would also like to thank Madalena months (Bandeira et al., unpublished data). The energetic cost of Monteiro, Paulo Carvalho, and Paula Mendonc¸a (veterinarians of Instituto gestation, birth, and lactation (Gittleman and Thompson 1988; Nacional de Investigac¸~ ao Agra ´ ria e Veterina ´ ria, I.P., INIAV) for some of the Speakman 2008), coupled with the increased difficulty in obtaining samples harvest. We appreciate the support of the Doctoral Program in food and decreased foraging time (Bandeira et al. 2018), is expected Biology and Ecology of Global Changes of University of Aveiro and to result in a trade-off between reproduction and immunity that is University of Lisbon. V.B. and J.C. were supported by FCT doctoral grants more pronounced in spring for Egyptian mongoose females. (SFRH/BD/51540/2011 and SFRH/BD/98387/2013, respectively). We thank However, trends in spleen weight data from our female specimens 2 anonymous reviewers and the editor for their helpful comments. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Bandeira et al.  Sex, season, and spleen weight variation 7 Gittleman JL, Thompson SD, 1988. Energy allocation in mammalian repro- Funding duction. Amer Zool 28:863–875. This project was funded by National (through FCT) and European funds Gou ¨ y de Bellocq J, Ribas A, Casanova JC, Morand S, 2007. (through COMPETE and FEDER, co-funding through the project “Genetic Immunocompetence and helminth community of the white-toothed shrew assessment of a successful invasion: Population genetics of the Egyptian mon- Crocidura russula from the Montseny Natural Park, Spain. Eur J Wildl Res goose H. ichneumon in Portugal,” reference PTDC/BIA-BEC/104401/2008). 53:315–320. We acknowledge University of Aveiro (Department of Biology) and FCT/ Green AJ, 2001. 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VIFs for the full set of explanatory variables for adjusted spleen weight model construction 1 2 3 4 Variable VIF VIF VIF VIF Season Spring 1.84 1.84 1.83 1.82 Summer 1.82 1.82 1.82 1.81 Winter 1.63 1.63 1.61 1.60 Sex 1.11 1.11 1.11 1.06 Age Juvenile 1 3.32 3.32 3.32 1.26 Juvenile 2 1.78 1.77 1.77 1.31 Sub-adult 1.31 1.31 1.29 1.19 Region 1.97 1.80 1.75 1.76 Egyptian mongoose abundance 1.44 1.44 1.43 1.42 Habitat Agro-forestry 1.57 1.55 1.53 1.51 Broadleaved and mixed forests 1.87 1.82 1.65 1.65 Rice fields 1.04 1.03 1.03 1.03 Shrubs 1.15 1.13 1.12 1.13 Urban 5.07 3.12 1.17 1.17 Vineyards and orchards 1.13 1.12 1.11 1.11 Population density 14.66 — — — Road network 12.07 4.57 — — River network 1.92 1.92 1.62 1.63 Body size 3.26 3.24 3.24 — Body condition 1.10 1.09 1.09 1.08 Note: Variables removed are in bold. Table A2. VIFs for the full set of explanatory variables for body condition model construction 1 2 3 4 Variable VIF VIF VIF VIF Season Spring 1.85 1.84 1.83 1.82 Summer 1.78 1.78 1.78 1.77 Winter 1.65 1.65 1.63 1.62 Sex 1.14 1.13 1.13 1.09 Age Juvenile 1 3.30 3.29 3.29 1.25 Juvenile 2 1.78 1.77 1.77 1.30 Sub-adult 1.31 1.31 1.29 1.19 Region 2.00 1.83 1.78 1.79 Egyptian mongoose abundance 1.46 1.45 1.44 1.44 Habitat Agro-forestry 1.57 1.56 1.54 1.52 Broadleaved and mixed forests 1.87 1.82 1.65 1.65 Rice fields 1.04 1.03 1.03 1.03 Shrubs 1.17 1.15 1.14 1.15 Urban 5.06 3.12 1.18 1.17 Vineyards and orchards 1.14 1.12 1.11 1.11 Population density 14.57 — — — Road network 12.04 4.57 — — River network 1.90 1.90 1.60 1.61 Body size 3.25 3.23 3.22 — Adjusted spleen weight 1.18 1.18 1.18 1.17 Note: Variables removed are in bold. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 10 Current Zoology, 2018, Vol. 0, No. 0 0.48 1940 0.46 0.44 0.42 0.40 0.38 0.36 1800 Male Female Male Female Sex Sex Figure A1. Means of Egyptian mongoose adjusted spleen weight (expressed Figure A4. Means of Egyptian mongoose body condition [Scaled Mass as g/100 g body weight) observed for both sexes. Vertical bars denote 95% Index—predicted body mass (in grams) for an individual standardized to lin- confidence intervals. ear body measurement] observed for both sexes. Vertical bars denote 95% confidence intervals. 0.52 0.50 0.48 0.46 0.44 0.42 0.40 0.38 0.36 0.34 0.32 Winter Spring Summer Autumn Season Juvenile 1 Juvenile 2 Sub-adult Adult Age Figure A2. Means of Egyptian mongoose adjusted spleen weight (expressed as g/100 g body weight) observed for each season. Vertical bars denote 95% Figure A5. Means of Egyptian mongoose body condition [Scaled Mass confidence intervals. Index—predicted body mass (in grams) for an individual standardized to lin- ear body measurement] observed for each age cohort. Vertical bars denote 95% confidence intervals. 0.60 0.55 0.50 0.45 1950 0.40 0.35 0.30 0.25 Male Winter Spring Summer Autumn Female Male Season Winter Spring Summer Autumn Female Season Figure A3. Means of Egyptian mongoose adjusted spleen weight (expressed as g/100 g body weight) observed for each sex and season. Vertical bars de- Figure A6. Means of Egyptian mongoose body condition [Scaled Mass note 95% confidence intervals. Index—predicted body mass (in grams) for an individual standardized to lin- ear body measurement] observed for each sex and season. Vertical bars de- note 95% confidence intervals. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Spleen weight (g/100 g body weight) Spleen weight (g/100 g body weight) Spleen weight (g/100 g body weight) Body condition (g - Scaled Mass Index) Body condition (g - Scaled Mass Index) Body condition (g - Scaled Mass Index) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Sex and season explain spleen weight variation in the Egyptian mongoose

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Abstract

The Egyptian mongoose (Herpestes ichneumon Linnaeus, 1758) is a medium-sized carnivore that experienced remarkable geographic expansion over the last 3 decades in the Iberian Peninsula. In this study, we investigated the association of species-related and abiotic factors with spleen weight (as a proxy for immunocompetence) in the species. We assessed the relationship of body condition, sex, age, season, and environmental conditions with spleen weight established for 508 hunted speci- mens. Our results indicate that the effects of sex and season outweigh those of all other variables, including body condition. Spleen weight is higher in males than in females, and heavier spleens are more likely to be found in spring, coinciding with the highest period of investment in reproduction due to mating, gestation, birth, and lactation. Coupled with the absence of an effect of body condi- tion, our findings suggest that spleen weight variation in this species is mostly influenced by life- history traits linked to reproduction, rather than overall energy availability, winter immunoenhance- ment, or energy partitioning effects, and prompt further research focusing on this topic. Key words: body condition, carnivore, Herpestes ichneumon, Iberian Peninsula, mongoose, spleen weight. The vertebrate immune system must respond to antigenic challenges environmental scenarios (Vicente et al. 2007). Immunocompetence that irreversibly affect life-history traits and energy allocation trade- can be affected by seasonal variations or by sex or indeed by interac- offs (Schulte-Hostedde and Gooderham 2011). Since it directly tions between these 2 factors. Despite this fact, to date, studies influences survival, indicators of immunocompetence may help to focusing on immune competence that use spleen weight as an indica- disentangle the factors underlying species success under different tor lack samples covering all seasons of the year (e.g., Corbin et al. V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 2008; Schulte-Hostedde and Elsasser 2011) or from both sexes 1995), stress (Young and Monfort 2009), ectoparasitism (Perez- (e.g., Schulte-Hostedde and Elsasser 2011). In order to investigate Orella and Schulte-Hostedde 2005), and prey selection (Pierce et al. the factors that influence variance in immunocompetence within a 2000). Regarding its relationship with immunocompetence, body species, samples covering a broad range of environmental condi- condition has been proposed to influence spleen weight through tions, demographic groups, and all periods of the life-cycle are ne- overall energy availability (Ponlet et al. 2011; Schulte-Hostedde and cessary. The Egyptian mongoose Herpestes ichneumon is an Elsasser 2011) and energy partitioning effects (Vicente et al. 2007). appropriate model for such a study because it has colonized main- Therefore, body condition can be used as an indicator controlling land Portugal over the past 30 years (Barros and Fonseca 2011), cur- for energetic state and overall health when studying spleen weight as rently inhabiting a diverse array of habitats representing all a proxy of immune competence. environmental conditions available to the species. Furthermore, In this work, we set out to understand spleen weight variation in legal hunting generates a large number of specimens year-round of a sample of free-ranging Egyptian mongoose. If increased spleen both sexes and all ages from the entire distributional range. weight is simply a result of the availability of energy to invest in im- The spleen is the primordial secondary lymphoid organ in mam- munity, we expected it to be primarily associated with higher body mals, playing a key role in immune defense (Corbin et al. 2008). It is condition scores. Alternatively, spleen weight variation may result functionally and histologically divided into red pulp and white pulp from energy partitioning effects and trade-offs between key biologic- (Mebius and Kraal 2005). The red pulp ensures blood filtration, re- al functions, in which case we expected to find decreased spleen moval of effete erythrocytes, regeneration of free ferrous iron, and weight during periods of maximum investment in reproduction or pathogen clearance (Mebius and Kraal 2005). The white pulp growth. However, if spleen weight variation results from more spe- houses lymphoid components under resting conditions, such as cific or complex interactions, we might find it associated with one T cells, B cells, and antigen-presenting cells (Mebius and Kraal or more demographic, environmental, or life-history variables. 2005). Maintaining the immune system is energetically costly, and Finally, if increased spleen weight is the result of an immune re- individuals with better body condition are likely to have a greater sponse to parasitism, the cost of that response might be reflected in capacity for the production and storage of lymphocytes (Ponlet et al. body condition, with higher spleen weight values associated with 2011; Schulte-Hostedde and Elsasser 2011), which may translate poorer body condition scores. into heavier spleens. Spleen weight is considered a reliable proxy of individual immunocompetence, notwithstanding its other functions (Hosken and O’Shea 2001; Corbin et al. 2008; Hadidi et al. 2008; Materials and Methods Navarro-Gonzalez et al. 2011; Manjerovic and Waterman 2012). Study area At the intraspecific level, larger spleens may reflect greater invest- Wild Egyptian mongoose specimens were collected from 13 of the ment in immunity by healthy individuals with better body condition 18 districts of continental Portugal. Geographic origin of the speci- (Møller et al. 1998b), whereas smaller spleens suggest the opposite mens was attributed to either north or south of the Tagus River, (Dı ´ez-Leo ´ n et al. 2013). However, the use of spleen weight to evalu- given the marked differences in bioclimatic, biogeographic, and an- ate within-species immunocompetence has limitations. Sudden thropogenic pressures previously observed between both regions increases in spleen weight due to intense physical exertion and stress (Bandeira et al. 2016, 2018). The Tagus River was previously con- (Corbin et al. 2008) or ongoing infection might bias estimates relat- sidered a geographical barrier for the species, since the distribution ing to immune capacity (Gou ¨ y de Bellocq et al. 2007). The relative of the Egyptian mongoose was more concentrated in the south until amount of red blood cells stored in the mammalian spleen is known 3 decades ago (Borralho et al. 1996; Barros and Fonseca 2011). to vary depending on stress, exercise, or hemorrhagic trauma The vegetation of the southern region is mainly characterized by (Brendolan et al. 2007). Alternatively, enlargement of the spleen evergreen Quercus, whereas in the north monoculture plantations of may reflect an immune response to parasitism (Nunn 2002; Gou ¨y de Eucalyptus sp. have largely replaced Pinus pinaster and native de- Bellocq et al. 2007; Corbin et al. 2008), or inflammation due to ciduous trees (Alves et al. 2009). The northern region generally pathological changes (Møller et al. 1998a). Finally, in addition to a presents lower temperatures and higher levels of rainfall compared dependence on body condition, spleen weight may also be influ- with the southern region (Hijmans et al. 2005). Furthermore, human enced by energy partitioning and trade-offs between reproduction pressure is lower in the south, having fewer urbanized areas, a lower and growth (Vicente et al. 2007). Therefore, simultaneous consider- population density, a less extensive road network, and fewer frag- ation of indicators of overall health and energetic state (e.g., body mented habitats (Alves et al. 2009; European Commission 2015; condition), as well as information on season, sex, age, and environ- IGP 2015). Also, there are fewer mountainous ridges and a less ex- mental conditions can help overcome these limitations, facilitating tensive hydrographic network south of the Tagus River (SNIRH use of spleen weight as a proxy of immunocompetence. 2015). Body condition also can be altered by environmental conditions or individual traits such as sex or age (Toı¨go et al. 2006). Body con- Sampling procedures dition refers to the amount of energy reserves (such as fat and pro- Sampling took place between January 2008 and December 2014. tein) that an animal possesses (Perez-Orella and Schulte-Hostedde Capture date was classified as winter (January–March), spring 2005; Schulte-Hostedde et al. 2005), and it represents the energetic (April–June), summer (July–September), or autumn (October– state of an animal (Schulte-Hostedde et al. 2001). Body condition December). Specimens were obtained from hunting activities (box- scores have been developed as bioindicators of overall health or the trapped under legal game management actions aimed at controlling physical quality of individual specimens (Peig and Green 2009). predator densities), according to legal requirements and under li- Several studies have assessed the relationship between body condi- tion of mammals and a range of ecological parameters (Green cense from competent authorities [Instituto da Conservac¸ao da 2001), including animal density and fecundity (Stewart et al. 2005), Natureza e das Florestas (ICNF)]. A total of 508 Egyptian mon- the effect of parturition and weight of litter (Dobson and Michener gooses were included in this study, 266 females and 242 males. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Bandeira et al.  Sex, season, and spleen weight variation 3 Table 1. Numbers of Egyptian mongoose samples obtained for each region, North and South of the Tagus River, together with in- formation on age cohort and sex Age Sex Region North South Adult Female 41 107 Male 35 80 Sub-adult Female 12 33 Male 16 23 Juvenile II Female 4 34 Male 9 47 Juvenile I Female 4 31 Male 9 23 Total Female 61 205 Male 69 173 There were 263 adults, 84 sub-adults, 94 type II juveniles, and 67 type I juveniles (Table 1, see definitions below). Age was deter- mined by dentition according to Bandeira et al. (2016). Each speci- men was assigned to 1 of 4 age cohorts: adults over 1 year of age, sub-adults between 9 and 12 months, type II juveniles between 5.5 and 9 months, and type I juveniles between 2.5 and 5.5 months of age. Regarding geographic origin, 130 specimens came from north of the Tagus River and 378 from the south (Figure 1 and Table 1). Carcasses were labeled with collection date and location and stored at 20 C until processed. In the laboratory, samples were thawed, sexed, weighed, measured, and dissected. Spleens were collected and weighed separately. Six biometric measurements (Bandeira et al. 2016) were taken: snout–tail length (terminal hairs not included); Figure 1. Locations and sample sizes of Egyptian mongoose studied from dis- right hind leg length; right hind foot length; shoulder height; neck tricts in Portugal. perimeter; and head width. Only specimens for which age determin- ation was possible and that possessed an intact spleen were assessed. areas) representing habitat structure were retrieved from a Corine Pregnant females were excluded to avoid bias from body weight and Land Cover (2006) dataset with a spatial resolution of 250 m and body condition variables. converted in a single categorical variable represented by the most abundant habitat type in each grid cell. Hydrographic data were Environmental variables obtained from the Sistema Nacional de Informac¸~ ao de Recursos Based on ecological requirements and physiological characteristics Hı ´dricos (SNIRH 2015). The degree of anthropogenic pressure was of Egyptian mongoose, we selected 5 environmental variables that represented by 2 variables: population density [derived from the could directly or indirectly influence body condition and spleen European Commission (2015)] and extent of the road network weight for modeling (e.g., Ben-Yaacov and Yom-Tov 1983; Delibes (IGP 2015). Geographic position of collected samples was reported et al. 1984; Palomares and Delibes 1990, 1991a; Palomares 1993b; in terms of latitude and longitude. Abundances of Egyptian mon- Barros et al. 2015; Bandeira et al. 2016, 2018). Landscape structure goose (number of animals/400 ha) based on the number of animals can influence physical condition due to differences in the amount of hunted in each area and during the month, where and when each suitable habitat, prey availability, and its impact on the movement Egyptian mongoose sampled was collected, were established accord- ing to annual hunting yields (ICNF, unpublished data). and dispersal of mongooses (Palomares and Delibes 1993a; Palomares 1994; Bandeira et al. 2018). Habitat change in recent decades seems to have favored the expansion of mongoose popula- Statistical procedures tions into new territories (Barros et al. 2015). Anthropogenic factors All variables were tested for normality with Kolmogorov–Smirnov are a ubiquitous influence on ecosystems and, together with natural tests (with Lilliefors correction for the significance level) (Zar 1999). barriers, act as constraints on mongoose expansion, thereby shaping The principal component analysis (PCA) enables a single esti- this species’ distribution (Barros et al. 2015). We included anthropo- mate of body size on the first component, based on the covariance genic factors in our study to assess possible associations with physic- matrix of various measures. Body size was calculated by combining al condition and immunocompetence, which we expected to be specimen weight and the 6 biometric measurements into a single better in areas with low human pressure. value through a PCA, using all variables with loadings >0.70. Each variable was represented by mean values in 2 2 km grid The PCA was performed in STATISTICA version 7.1 (Stat Soft Inc., cells, considering the critical home area of the Egyptian mongoose 2005). Spleen weight was corrected for body weight and is reported (Palomares and Delibes 1991b). Nine variables (urban, rice fields, as spleen weight (in grams) per 100 g of total specimen mass agro-forestry, shrubs, inland water bodies, vineyards and orchards, (adjusted spleen weight). Body condition was scored according to coniferous forest, broadleaved and mixed forests, and agricultural the Scaled Mass Index (Peig and Green 2009, 2010). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Table 2. Model selection, using AICc, for the effect of age, season, sex, and their interactions, together with region, Egyptian mongoose abundance, habitat, extent of river network, and body condition (Scaled Mass Index), on adjusted spleen weight (expressed as g/100 g body weight) of the Egyptian mongoose in Portugal Models df AICc DAICc AICc weight R Season1 sex 7 2142.27 0.00 0.67 0.28 Season þ region þ sex 8 139.89 2.38 0.21 0.20 Egyptian mongoose abundance þ sex 5 135.78 6.49 0.03 0.26 Season 6 135.69 6.58 0.03 0.25 Sex 4 135.12 7.15 0.02 0.17 Season þ Egyptian mongoose abundance þ sex 8 135.01 7.26 0.02 0.31 Season þ region 7 134.16 8.11 0.01 0.17 Region þ sex 5 133.48 8.79 0.01 0.06 Season þ region þ Egyptian mongoose abundance þ sex 9 132.08 10.20 0.00 0.24 Region þ Egyptian mongoose abundance þ sex 6 131.99 10.28 0.00 0.20 Season þ Egyptian mongoose abundance 7 129.10 13.17 0.00 0.28 Egyptian mongoose abundance 4 128.95 13.32 0.00 0.23 Season þ region þ Egyptian mongoose abundance 8 126.91 15.36 0.00 0.21 (Null) 3 126.76 15.51 0.00 0.13 Region 4 126.32 15.95 0.00 0.03 Season þ sex þ season * sex 10 126.27 16.00 0.00 0.28 Region þ Egyptian mongoose abundance 5 125.76 16.51 0.00 0.17 Season þ sex þ scaled mass index 8 125.50 16.77 0.00 0.25 Season þ region þ sex þ season * sex 11 124.32 17.95 0.00 0.21 Season þ region þ sex þ scaled mass index 9 124.21 18.06 0.00 0.13 Season þ age þ sex 10 122.46 19.81 0.00 0.29 Ageþ sex 7 122.44 19.83 0.00 0.22 Notes: Models considered as explanatory are in bold. DAICc is the difference between the AIC yielded by each model and the lowest AICc (considered the best model); df, degrees of freedom. All explanatory variables were checked for collinearity using Results variance inflation factors (VIFs) (Zuur et al. 2009). A cut-off value The PCA of specimen body size explained 74.6% of the variance in of 2.5 was used to drop collinear variables. The predictor with the this parameter, with an eigenvalue of 5.220. highest VIF value was removed in a stepwise procedure, removing Two variables of anthropogenic factors (population density and one variable at a time, recalculating the VIF values, until all the extent of road network) and the variable body size were excluded remaining predictors had a VIF 2.5 (Zuur et al. 2009). Only from the initial set of predictors for adjusted spleen weight, as well those that presented VIF 2.5 were retained for model construc- as for body condition model construction, to avoid multicollinearity tion. Models explaining variation in spleen weight or body (Tables A1 and A2). Only one model (seasonþ sex) with DAICc< 2 condition included the discrete variables region, habitat, sex, age (AICc¼142.27, df¼ 507) could be considered explanatory and season and the interactions seasonsex, seasonage, and (Tables 2 and 3). Overall, males presented higher adjusted spleen sex age, as well as the continuous variables Egyptian mongoose weight than females, and spleens were heaviest in spring, followed abundance, population density, extents of the road and river net- by winter and autumn, and they were lightest in summer (Table 3, work, and body size, that were not excluded by VIF analysis. Body see details in Figures A1 and A2). Despite the fact that the inter- condition score was used as an explanatory variable in our model action sex  season was not explanatory in our model, an analysis of construction for spleen weight, and vice versa. For mixed the means of spleen weight for each sex-season group revealed dif- modeling, we used Gaussian distribution, identity link function, ferent seasonal trends between males and females (Figure A3). In and district (first-level administrative subdivision of mainland males, adjusted spleen weight was highest in winter and decreased in Portugal, compartmentalized based on history, common land use, spring, reaching its lowest value in summer, before increasing again and related issues) as a random factor to control for non- in autumn. However, in females, adjusted spleen weight reached its independence of samples from the same area. highest values in spring and remained low in the other 3 seasons of Selection of models explaining either spleen weight or body con- the year. dition variation was performed separately according to the proced- For body condition analyses, only one model with DAICc< 2 ure described in Zuur et al. (2009), whereby a ranking was made of (AICc¼ 7089.62, df¼ 507) was considered explanatory (Table 4). all possible models using the Akaike Information Criterion (AICc) It included the variables: spleen weightþ seasonþ ageþ sex þ (Burnham and Anderson 2002) and only those with DAICc values season ageþ seasonsex þ agesexþ habitatþ regionþ Egyptian <2 were considered explanatory. The residual patterns were mongoose abundance (Tables 4 and 5). Males presented higher checked. body condition scores than females (Table 5). Juvenile type I All statistical analyses were performed in R (version 2.13.2) Egyptian mongooses had higher body condition scores compared using the packages lme4 (Bates et al. 2014)and MuMIn for with adults, sub-adults, and juveniles type II, in descending order, multimodel selection and model averaging approaches (Barton respectively (Table 5). Animals collected in autumn presented the 2012). highest body condition scores, followed by those collected in winter, Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Bandeira et al.  Sex, season, and spleen weight variation 5 spring, and summer (Table 5). Specimens with heavier spleens pre- immunity, larger spleens may indicate more competent immune sys- sented higher body condition scores (Table 5). Mongooses captured tems, allowing animals to attain better body condition scores. In general, the adjusted spleen weight of male mongooses is sig- from places with lower abundances of conspecifics had higher body nificantly higher than that of females, contrasting with results for condition, as well as those from the south (Table 5). Specimens col- red deer Cervus elaphus in which spleen weight adjusted for body lected from vineyards and orchards, rice fields, and urban habitats size does not differ between sexes (Corbin et al. 2008). Our data had the highest body condition scores (Table 5). Some selected fac- also show that adjusted spleen weight varies across seasons. In tors are graphically presented in Figures A4–A6. spring, our Egyptian mongoose specimens presented the highest spleen weights, with a slight decrease in values during winter, and Discussion an abrupt decrease in summer, followed by a rise again in autumn. To our knowledge, this is the first time that year-round spleen Based on a large sample of free-ranging Egyptian mongoose of both weight measurements have been presented for a wild carnivore spe- sexes and all ages, sampled from throughout Portugal and year- cies. A study on wild male American mink Neovison vison (Persson round, our study shows that sex and season explain the variation in et al. 2011) and a report focusing on wild boar Sus scrofa adjusted spleen weight. We found no evidence for an effect of body (Ferna ´ ndez-Llario et al. 2004) showed that animal spleens were condition score on spleen weight in the explanatory model, contra- heaviest during winter, but these studies only compared data from 3 dicting the hypothesis that spleen weight depends primarily on the and 2 seasons, respectively. Two hypotheses are offered in previous availability of energy to invest in immune function (Ponlet et al. studies to explain seasonal variation in indicators of immunity in 2011; Schulte-Hostedde and Elsasser 2011). In fact, our results sug- vertebrates (Martin et al. 2008). The first is the winter immunoen- gest the opposite causal relationship, with spleen weight appearing hancement hypothesis, whereby animals up-regulate their immune as one of the factors in the model explaining the variation in body activity as a response to changes in photoperiod, to compensate for condition score. The directionality apparent from these results sug- the immunosuppressive effects of winter temperatures and resource gests that even though higher body condition scores may not neces- scarcity (Sinclair and Lochmiller 2000). The second is the trade-off sarily imply larger spleens and a greater ability to invest energy in hypothesis according to which the high cost of immune activity is in- compatible with other costly physiological activities that occur at Table 3. Effects of the model considered as explanatory for certain times of the year, such as reproduction (Vicente et al. 2007). adjusted spleen weight (expressed as g/100 g body weight) of the Deeper analysis is necessary to determine which mechanism under- Egyptian mongoose in Portugal lies the influence of sex and season on spleen weight in this Egyptian mongoose population. Since an increase in spleen weight in spring is Variables Estimate Standard error t-Value apparently incompatible with the winter immunoenhancement hy- Intercept 0.328 0.023 14.197 pothesis for seasonal variation in immunity (Martin et al. 2008), we Sex Male 0.054 0.015 3.712 speculate that different reproductive strategies, sex-specific behav- Season Spring 0.081 0.020 4.079 ior, and physiological variations may also be linked to spleen weight Summer 0.026 0.020 1.285 variation, especially since the Egyptian mongoose is a polygynic Winter 0.071 0.023 3.142 species (Palomares 1993a), exhibiting differential investment in Table 4. Model selection, using AICc, for the effect of age, season, sex, and their interactions, together with region, Egyptian mongoose abundance, habitat, extent of river network, and adjusted spleen weight (expressed as g/100 g body weight), on body condition (Scaled Mass Index) of the Egyptian mongoose in Portugal Models df AICc DAICc AICc weight R Spleen weight1 season1 habitat1 age1 region1 Egyptian mongoose abundance1 sex 34 7,089.62 0.00 0.88 0.11 1 season3age1 season3sex1 age3sex Spleen weight þ season þ habitat þ age þ region þ sex þ season3age þ season3sex þ age3sex 33 7,094.83 5.21 0.07 0.11 Spleen weight þ season þ habitat þ age þ region þ river network þ Egyptian mongoose abundance 35 7,096.02 6.40 0.04 0.11 þ sex þ season3age þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ Egyptian mongoose abundance þ sex þ season3age 33 7,097.90 8.28 0.01 0.12 þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ region þ river network þ sex þ season3age þ season3sex 34 7,101.54 11.92 0.00 0.11 þ age3sex Season þ habitat þ age þ region þ Egyptian mongoose abundance þ sex þ season3age þ season3sex 33 7,103.01 13.39 0.00 0.12 þ age3sex Spleen weight þ season þ habitat þ age þ sex þ season3ageþ season3sex þ age3sex 32 7,103.15 13.53 0.00 0.12 Spleen weight þ season þ habitat þ age þ river network þ Egyptian mongoose abundance þ sex 34 7,104.00 14.39 0.00 0.11 þ season3age þ season3sex þ age3sex Season þ habitat þ age þ region þ sex þ season3age þ season3sex þ age3sex 32 7,108.72 19.10 0.00 0.12 Season þ habitat þ age þ region þ river network þ Egyptian mongoose abundance þ sex 34 7,109.47 19.85 0.00 0.11 þ season3age þ season3sex þ age3sex Spleen weight þ season þ habitat þ age þ river network þ sex þ season3age þ season3sex þ age3sex 33 7,109.59 19.97 0.00 0.11 Notes: Models considered as explanatory are in bold. DAICc is the difference between the AIC yielded by each model and the lowest AICc (considered the best model); df, degrees of freedom. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Table 5. Effects of the model considered as explanatory for body showed a peak in spring, thus again contradicting the reproductive condition (Scaled Mass Index) of the Egyptian mongoose in trade-off scenario. Portugal Animals are expected to have larger spleens during active infec- tion due to increased lymphocyte production and/or pathological in- Variables Estimate Standard error t-Value flammation (Møller et al. 1998a) or parasitism (Nunn 2002; Gou ¨y Intercept 1,878.46 80.44 23.351 de Bellocq et al. 2007; Corbin et al. 2008), so we must consider a Sex Male 59.80 76.10 0.786 third hypothesis, whereby these seasonal differences in spleen weight Age Juvenile 1 3.96 128.17 0.031 can be influenced by parasitism. Additionally, pathogen infection Juvenile 2 226.44 86.41 2.621 and parasite burden may be more pronounced in males of polygyn- Sub-adult 70.07 91.39 0.767 ous species (Moore and Wilson 2002; Perez-Orella and Schulte- Season Spring 113.97 74.15 1.537 Summer 187.89 76.52 2.455 Hostedde 2005), which has been attributed to sexual selection, com- Winter 111.04 81.22 1.367 petition, and larger home ranges (Zuk 1990). Unfortunately, the Region South 53.18 57.99 0.917 lack of measures of diversity and abundance of parasites in our Spleen weight 181.37 79.61 2.278 study is a major limitation to investigate this effect. However, costly Egyptian mongoose abundance 10.09 8.44 1.195 immune responses to parasitism and high parasite burdens are often Habitat Agro-forestry 41.35 61.20 0.676 negatively correlated with body condition (e.g., Irvine et al. 2006; Broadleaved and 5.81 42.05 0.138 mixed forests Davidson et al. 2015; Taylor et al. 2018). Therefore, the fact that in Rice fields 80.84 254.03 0.318 our sample the peak in spleen weight coincides with peaks in body Shrubs 9.47 82.46 0.115 condition for both sexes apparently conflicts with a parasite-driven Urban 61.44 122.44 0.502 variation in spleen weight, and highlights the need for further Vineyards and orchards 115.56 170.09 0.679 research. Sexage MaleJuvenile I 3.28 104.63 0.031 In summary, body condition does not predict spleen weight vari- MaleJuvenile II 49.27 94.62 0.521 ation in this Egyptian mongoose population, which instead is pri- MaleSub-adult 96.32 93.66 1.028 Sexseason MaleSpring 93.12 91.93 1.013 marily explained by sex and season. Moreover, spleen weight peaks MaleSummer 109.86 90.44 1.215 in spring and coincides with the period of maximum reproductive MaleWinter 71.71 99.91 0.718 investment for the species, thus contradicting the winter immunoen- Seasonage SpringJuvenile I 30.38 158.76 0.191 hancement and reproductive trade-off hypotheses. Nevertheless, the SpringJuvenile II 304.12 133.21 2.283 coincidence of the peaks in spleen weight trends with the period of SpringSub-adult 156.35 126.01 1.241 maximum investment in reproduction for each sex suggests that SummerJuvenile I 115.86 137.33 0.844 spleen weight variation is closely related to the species’ reproductive SummerJuvenile II 261.95 107.34 2.440 SummerSub-adult 129.61 172.67 0.751 biology. This relationship warrants further research to establish if it WinterJuvenile I 320.24 276.42 1.159 is a consequence of reproductive behavior, a biologically timed in- WinterJuvenile II 236.69 198.20 1.194 vestment to prepare for a challenging period in terms of immunity WinterSub-adult 32.04 112.64 0.284 or simply a result of seasonal host–pathogen dynamics. Author Contributions reproduction and sex-skewed survival (Palomares 1993a; Palomares and Delibes 1993b). V.B., E.V., and C.F. conceived and designed the experiments. V.B. According to a study on the reproductive parameters of the and A.A. performed the experiments. V.B. and E.V. analyzed the Egyptian mongoose in Spain, courtship and mating begin in winter data and performed the statistical analyses. J.C. generated maps and and extend almost to the end of spring (Palomares and Delibes provided ecological, habitat, and climatic data. V.B., E.V., A.A., 1992). During the breeding season, males engage in physical aggres- M.V.C., and C.F. wrote the manuscript. All authors contributed to sion to defend their territory, to gain access to females, to mate, and the development of ideas and approved the final version of the to compete for prey (Palomares 1991, 1993a). Therefore, male in- manuscript. vestment in immune function may decrease during the reproductive period, since energetic resources should be directed primarily toward reproduction and less toward immune responses (Zuk and Acknowledgments Stoehr 2002; Stoehr and Kokko 2006). However, our results do not Thanks are due to collectors, hunters, entities managing hunting areas and support this trade-off hypothesis because spleen weight in our sam- their representatives (namely FENCAC¸A, ANPC, and CNCP), to Tapada ple of males actually tends toward its highest levels in winter. In Nacional de Mafra, and to all that contributed to animal sampling, as well as Spain, pregnant Egyptian mongooses are observed mostly in March ICNF for the capture permits. We thank Carlos Pimenta (DGPC-Laborato ´ rio and April (Palomares and Delibes 1992). We also observed this pat- de Arqueocie ˆ ncias, SEC—Direc¸~ ao Geral do Patrimo ´ nio Cultural) for instruc- tern in our sample, with 80% of pregnancies detected in the 3 spring tions on a method for cleaning skulls. We would also like to thank Madalena months (Bandeira et al., unpublished data). The energetic cost of Monteiro, Paulo Carvalho, and Paula Mendonc¸a (veterinarians of Instituto gestation, birth, and lactation (Gittleman and Thompson 1988; Nacional de Investigac¸~ ao Agra ´ ria e Veterina ´ ria, I.P., INIAV) for some of the Speakman 2008), coupled with the increased difficulty in obtaining samples harvest. We appreciate the support of the Doctoral Program in food and decreased foraging time (Bandeira et al. 2018), is expected Biology and Ecology of Global Changes of University of Aveiro and to result in a trade-off between reproduction and immunity that is University of Lisbon. V.B. and J.C. were supported by FCT doctoral grants more pronounced in spring for Egyptian mongoose females. (SFRH/BD/51540/2011 and SFRH/BD/98387/2013, respectively). We thank However, trends in spleen weight data from our female specimens 2 anonymous reviewers and the editor for their helpful comments. 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VIFs for the full set of explanatory variables for adjusted spleen weight model construction 1 2 3 4 Variable VIF VIF VIF VIF Season Spring 1.84 1.84 1.83 1.82 Summer 1.82 1.82 1.82 1.81 Winter 1.63 1.63 1.61 1.60 Sex 1.11 1.11 1.11 1.06 Age Juvenile 1 3.32 3.32 3.32 1.26 Juvenile 2 1.78 1.77 1.77 1.31 Sub-adult 1.31 1.31 1.29 1.19 Region 1.97 1.80 1.75 1.76 Egyptian mongoose abundance 1.44 1.44 1.43 1.42 Habitat Agro-forestry 1.57 1.55 1.53 1.51 Broadleaved and mixed forests 1.87 1.82 1.65 1.65 Rice fields 1.04 1.03 1.03 1.03 Shrubs 1.15 1.13 1.12 1.13 Urban 5.07 3.12 1.17 1.17 Vineyards and orchards 1.13 1.12 1.11 1.11 Population density 14.66 — — — Road network 12.07 4.57 — — River network 1.92 1.92 1.62 1.63 Body size 3.26 3.24 3.24 — Body condition 1.10 1.09 1.09 1.08 Note: Variables removed are in bold. Table A2. VIFs for the full set of explanatory variables for body condition model construction 1 2 3 4 Variable VIF VIF VIF VIF Season Spring 1.85 1.84 1.83 1.82 Summer 1.78 1.78 1.78 1.77 Winter 1.65 1.65 1.63 1.62 Sex 1.14 1.13 1.13 1.09 Age Juvenile 1 3.30 3.29 3.29 1.25 Juvenile 2 1.78 1.77 1.77 1.30 Sub-adult 1.31 1.31 1.29 1.19 Region 2.00 1.83 1.78 1.79 Egyptian mongoose abundance 1.46 1.45 1.44 1.44 Habitat Agro-forestry 1.57 1.56 1.54 1.52 Broadleaved and mixed forests 1.87 1.82 1.65 1.65 Rice fields 1.04 1.03 1.03 1.03 Shrubs 1.17 1.15 1.14 1.15 Urban 5.06 3.12 1.18 1.17 Vineyards and orchards 1.14 1.12 1.11 1.11 Population density 14.57 — — — Road network 12.04 4.57 — — River network 1.90 1.90 1.60 1.61 Body size 3.25 3.23 3.22 — Adjusted spleen weight 1.18 1.18 1.18 1.17 Note: Variables removed are in bold. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 10 Current Zoology, 2018, Vol. 0, No. 0 0.48 1940 0.46 0.44 0.42 0.40 0.38 0.36 1800 Male Female Male Female Sex Sex Figure A1. Means of Egyptian mongoose adjusted spleen weight (expressed Figure A4. Means of Egyptian mongoose body condition [Scaled Mass as g/100 g body weight) observed for both sexes. Vertical bars denote 95% Index—predicted body mass (in grams) for an individual standardized to lin- confidence intervals. ear body measurement] observed for both sexes. Vertical bars denote 95% confidence intervals. 0.52 0.50 0.48 0.46 0.44 0.42 0.40 0.38 0.36 0.34 0.32 Winter Spring Summer Autumn Season Juvenile 1 Juvenile 2 Sub-adult Adult Age Figure A2. Means of Egyptian mongoose adjusted spleen weight (expressed as g/100 g body weight) observed for each season. Vertical bars denote 95% Figure A5. Means of Egyptian mongoose body condition [Scaled Mass confidence intervals. Index—predicted body mass (in grams) for an individual standardized to lin- ear body measurement] observed for each age cohort. Vertical bars denote 95% confidence intervals. 0.60 0.55 0.50 0.45 1950 0.40 0.35 0.30 0.25 Male Winter Spring Summer Autumn Female Male Season Winter Spring Summer Autumn Female Season Figure A3. Means of Egyptian mongoose adjusted spleen weight (expressed as g/100 g body weight) observed for each sex and season. Vertical bars de- Figure A6. Means of Egyptian mongoose body condition [Scaled Mass note 95% confidence intervals. Index—predicted body mass (in grams) for an individual standardized to lin- ear body measurement] observed for each sex and season. Vertical bars de- note 95% confidence intervals. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy031/4969522 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Spleen weight (g/100 g body weight) Spleen weight (g/100 g body weight) Spleen weight (g/100 g body weight) Body condition (g - Scaled Mass Index) Body condition (g - Scaled Mass Index) Body condition (g - Scaled Mass Index)

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