George Nascimento, Mario-Helminth Community Structure of the Gray Four

Journal of Parasitology 2019 105(4) 624–629 Ó American Society of Parasitologists 2019

Published 16 August 2019 Contents and archives available through www.bioone.org or www.jstor.org Journal of Parasitology journal homepage: www.journalofparasitology.org DOI: 10.1645/18-195

HELMINTH COMMUNITY STRUCTURE OF THE GRAY FOUR-EYED OPOSSUM PHILANDER OPOSSUM (MAMMALIA: DIDELPHIDAE) IN THE NEOTROPICAL PORTION OF MEXICO

Sara Ange´lica Ramı´rez-Can˜ as1,2, Mario George-Nascimento3, Luis Garcıá-Prieto4, and Rosario Mata-Lo´ pez1 1 Departamento de Biologıá Evolutiva, Facultad de Ciencias, Universidad Nacional Autońoma de Me´xico. Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510; Mexico City, Mexico. 2 Posgrado en Ciencias Biolo´gicas, Universidad Nacional Autońoma de Me´xico, Apartado 70-153, C.P. 04510, Mexico City, Mexico. 3 Departamento de Ecologıá, Facultad de Ciencias, Universidad Cato´lica de la Santı´sima Concepcioń, C.P. 4090541, Concepcioń, Chile. 4 Coleccioń Nacional de Helmintos, Instituto de Biologıá, Universidad Nacional Autońoma de Me´xico. Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Mexico City, Mexico. Correspondence should be sent to Rosario Mata-Lo´pez at: [email protected]

KEY WORDS ABSTRACT Didelphidae Studies on helminth communities associated with didelphids are scarce; the majority of works have Didelphis marsupialis focused at taxonomic level. To increase the ecological knowledge of these host–parasite associations, Didelphis virginiana during March (dry season) of 3 consecutive years (2013–2015) a total of 49 adults of the gray four- Helminths eyed opossum (Philander opossum) was collected in the Neotropical portion of Mexico (Agua Frı´a, Infracommunity Chiapas State) and examined for helminths. The main objectives of this study were to describe the Nematoda infra- and component communities of helminths associated with P. opossum and to compare the

Philander opossum helminth fauna of the Mexican population of this host species with those studied in French Guiana Platyhelminthes and in other Mexican terrestrial didelphids. The helminthological record of this host consisted of 12 Trematoda species: 7 taxa of Nematoda, 3 of Trematoda, 1 Cestoda, and 1 Acanthocephala. Eight of the 12 taxa have been previously recorded in Didelphidae and 4 represent accidental infections (Glossocercus sp., Stomylotrema vicarium, Spirura mexicana and Acanthocephala gen. sp.). Diet of hosts is the main structuring factor of the communities (92% of the helminth species were recruited through ingestion). Forty-eight hosts were parasitized by at least 1 helminth species; Rhopalias coronatus was the most prevalent and abundant species in the hosts sampled. No significant differences were found in global prevalence among the helminth species present in all samplings, considering host sex and year. The dominance exerted by R. coronatus led to low values of evenness and diversity at both community levels. No significant differences were observed in composition of helminth species among the 3 sampling years regarding sex. The results of our study showed changes in helminth abundance at infracommunity level; during the first sampling these changes are explained by species with direct life cycle (Viannaia sp. and Cruzia tentaculata), whereas in last 2 surveys the explanation can be attributed to species with heteroxenous life cycles (particularly R. coronatus, Duboisiella proloba, and Turgida turgida). Thirty-three percent of the helminth species recorded in P. opossum in Agua Frıá is shared with the other 2 terrestrial species of didelphids sampled in different sites of Mexico: Didelphis marsupialis and Didelphis virginiana. In contrast, samples from French Guiana and Agua Frıá, differ in terms of helminth fauna, confirming that the helminth communities of opossum species inhabiting the same locality show higher levels of taxonomic similarity than communities of conspecific marsupials allopatrically distributed.

Studies on helminth communities associated with wild mammals helminth communities of mammals with respect to other vertebrates are scarce at the global level when compared with those conducted (particularly cold-blooded vertebrates). Notwithstanding, studies on other host groups (e.g., ﬁshes). This could be attributed mainly to carried out on rodents and other mammal hosts suggest that this the difﬁculty in obtaining representative samples of mammalian pattern is not always realized (see Pence, 1990; Poulin, 1997; Esteban hosts. However, despite the reduced number of studies conducted et al., 2001; Fuentes et al., 2005; Sainz-Elipe et al., 2007). with this group of hosts, Kennedy et al. (1986) established as a The helminthological surveys dealing particularly with didel- general pattern the high species richness and diversity found in the phid hosts have focused at taxonomic level (Alden, 1995; Monet-

624 RAMI´REZ-CAN˜AS ET AL.—PHILANDER OPOSSUM HELMINTH COMMUNITIES 625

Mendoza et al., 2005; Acosta-Virgen et al., 2015; Chero et al., variation of helminth species abundance in a 2-dimensional space 2017). From an ecological perspective, only 2 studies at at infracommunity level. The correlation between the abundance community level have been conducted (Jimeńez et al., 2011; of each parasitic taxon with the first 2 axes of the PCo was also Costa-Neto et al., 2018). These authors compared the component represented, for which the Spearman coefficient was used, communities of 4 opossum species in the Neotropical region, including in the figure those with values greater than 0.4 (Clarke establishing that Didelphinae marsupials offer the same resources and Gorley, 2006). to their parasites by sharing similar morphologic, behavioral, and Representativeness of the sample in the analysis of the physiologic traits. This determines that the marsupials would component community was defined through a curve of species acquire parasites of the same set of species present in a given area, accumulation and using the bootstrap nonparametric richness resulting in high taxonomic similarity among sympatric commu- estimator (Poulin, 1998). On the basis of the above analysis, the nities. On the basis of the studies mentioned above, the objectives following descriptors were obtained for the 49 sampled opossum of the present study are: (1) to describe the infracommunity and at infra- and component community levels: species richness, component community of helminths found in Philander opossum number of helminths, diversity (using Brillouin index for infra- in a locality in the Neotropical portion of Mexico, and (2) to and Shannon–Wiener index at component community level), discuss if the qualitative data obtained in this work have evenness (for Brillouin and Shannon–Wiener indexes, respective- similarities to prior community-based studies. ly), and numeric dominance (Berger–Parker index) (Magurran, 2004). MATERIALS AND METHODS RESULTS During March (dry season) of 3 consecutive years a total of 49 adults of the gray four-eyed opossum (2013: n ¼ 10 individuals; Helminthological record 2014: n 28, and 2015: n 11) was collected. Hosts were caught ¼ ¼ A total of 7,535 individual helminths from 49 P. opossum with Tomahawkt traps (Wildlife Control Supplies, Simsbury, reviewed between 2013 and 2015 (27 females and 22 males) was Connecticut) baited with a mixture of sardine, vanilla, and oats at collected in Agua Frıá, Chiapas, Mexico. The helminthological Agua Frıá, Chiapas (16811048.0800 N, 93854057.0300 W), Mexico. record found in the opossums consisted of 12 taxa (Table I). The Opossums were handled and killed according to Sikes and group of helminths most represented was Nematoda, with 7 taxa, Gannon (2011) under permission FAUT-0170 issued by Secre- followed by Trematoda with 3 taxa, and finally, Cestoda and tarıá de Medio Ambiente y Recursos Naturales of Mexico. Sex of Acanthocephala with 1 taxon each. The helminths were mainly the hosts was determined visually. Host identification follows found in adult stage (83.3%) predominantly inhabiting the Reid (2006). Some skulls of the hosts were deposited in the Museo digestive tract of hosts (7 of the 12 species). Eight of the 12 taxa de Zoologıá Alfonso L. Herrera, Facultad de Ciencias, Uni- recorded have been found in terrestrial Didelphidae and 4 represent versidad Nacional Autońoma de Me´xico (UNAM) and at accidental infections (Glossocercus sp., Stomylotrema vicarium, Coleccioń Nacional de Mamı´feros, Instituto de Biologıá, UNAM, Spirura mexicana, and Acanthocephala gen. sp.) (Table I). both in Mexico City. A complete helminthological examination was practiced on all host specimens under stereoscopic micro- Ecological analysis scope. Helminths were collected, washed in saline solution (0.85%), and fixed according to their taxonomic group: cestodes The cumulative curve species performed for total of opossums with hot 10% formaldehyde, and trematodes and nematodes with sampled reached the asymptote in host number 27; in the same hot 4% formaldehyde, except trichostrongylids, which were fixed way, the bootstrap estimator calculated value for the sample with acetic acid at room temperature. All specimens were (13.51) is almost in agreement with the observed species richness preserved in vials with 70% ethanol. Worms were processed (12), so the helminthological record of the host in this period can and studied following conventional techniques (see Lamothe- be considered complete. On the basis of the anterior tests, analysis Argumedo, 1997). Population descriptors are in accordance with at infra- and component community was conducted. Bush et al. (1997). A binary logistic regression obtained in R Forty-eight of the 49 gray four-eyed opossums collected were software (R Core Team, 2016) was used to examine the infected with at least 1 helminth taxon. Rhopalias coronatus was association between the global prevalence and year þ sex for the most prevalent and abundant species (global mean abun- each parasite species present in all 3 yr; the level of significance dance: 132.22 6 148.27; 2013: 10.20 6 6.14; 2014: 154.32 6 3.56; used was P , 0.05. To test the assumption of equal group and 2015:186.91 6 243.08), followed by Cruzia tentaculata (global dispersion related to abundance of all helminth species at mean abundance: 16.24 6 30; 2013: 29.50 6 37.24; 2014: 12.71 infracommunity level (considering host sex and sampling year), 61.11; and 2015: 13.18 6 15.34); the remaining taxa reached a PERMDISP analysis in the Primer-6 software was performed parameters of infection comparatively lower both globally and by with P , 0.05 (Anderson et al., 2008). A permutational year (Table I). No significant differences among the global multivariate analysis of variance (PERMANOVA) with 9,999 prevalence of the helminth taxa collected in the 3 samplings (R. permutations was conducted to test similarity in community coronatus, C. tentaculata, and Viannaia sp.) were found consid- composition among the explanatory variables. Abundance of ering host sex (P ¼ 0.998; P ¼ 0.344; P ¼ 0.982, respectively) and each taxon in the infracommunities was transformed to the fourth sampled years (P ¼ 0.909; P ¼ 0.461; P ¼ 0.872, respectively). root; then, the similarity of Bray–Curtis 6 1 was obtained to The results of the analysis of the infracommunities showed that analyze variations in composition through software PRIMER- species richness oscillated from 1 to 5; the high numerical PERMANOVA 6.1.16 (Clarke and Gorley, 2006). Finally, a dominance exerted by R. coronatus determined the low evenness principal coordinate (PCo) analysis was used to display the and diversity values recorded (Table II).