Abstract This article reviews patterns, causes and consequences of gender-biased infestation of small mammalian hosts by macroparasites. We start with a description of gender biases in parasite infestation and discuss variation in these patterns among host and parasite taxa. We also look at temporal and spatial variations in gender-biased parasitism and demonstrate that they can vary seasonally and be mediated by environmental conditions. Then, we present main hypotheses that examine mechanisms of gender-biased parasitism. One group of these hypotheses focuses on differences between male and female hosts in their probability to be attacked by parasites, while another group links gender-biased parasitism with differences in parasite performance in male vs. female hosts. Finally, we discuss possible consequences of male-biased parasitism for individual parasites, their populations and communities.

Gender-biased parasitism in small mammals: patterns, mechanisms, consequences

In the present study, two abundant sympatric rodent species (27 Apodemus flavicollis and 33 A. sylvaticus) were studied for their endo- and ectoparasite fauna. The rodents were trapped in Dormagen, a city in North Rhine-Westphalia, Germany. A total of 20 different parasites species were identified, 13 endoparasite (2 Digenea, 5 Cestoda and 7 Nematoda) and 7 ectoparasite (5 Insecta and 2 Arachnida) species. Thirteen parasite species were found inhabiting both rodent species. The predominant endoparasite species in both rodents was the nematode Pelodera strongyloides, followed by the nematode Heligmosomoides polygyrus and a Syphacia species. The flea Ctenophthalmus agyrtes was the dominant ectoparasite in both rodent species. A. flavicollis usually carried 1-7 ecto-/endoparasite species (mean 4.0), whereas A. sylvaticus were mostly infested with 1-9 (mean 4.4). The parasite diversity of A. flavicollis (H' = 0.268, J = 0.097) was marginal lower in comparison to A. sylvaticus (H' = 0.319, J = 0.110). The two rodent species examined show remarkable similarities in the composition of their endo- and ectoparasite fauna being directly related to their similar pattern of living in the investigated area.

Parasites of two abundant sympatric rodent species in relation to host phylogeny and ecology.

Wild mustelids and canids are definitive hosts of Taenia and Versteria spp. while rodents act as natural intermediate hosts. Rarely, larval stages of these parasites can cause serious zoonoses. In Europe, four cases of Taenia martis cysticercosis have been diagnosed in immunocompetent women, and two cases in zoo primates since 2013. In North America, a zoonotic genotype related but distinct from Versteria mustelae has been identified in 2014, which had caused a fatal infection in an orangutan and liver- and disseminated cysticercoses in two severely immune deficient human patients in 2018, respectively. Additionally, we could attribute a historic human case from the USA to this Versteria sp. by reanalysing a published nucleotide sequence. In the last decades, sporadic zoonotic infections by cysticerci of the canid tapeworm Taenia crassiceps have been described (4 in North America, 8 in Europe). Besides, 3 ocular cases from North America and one neural infection from Europe, all in immunocompetent patients, 6 cutaneous infections were described in severely immunocompromised European patients. Correspondingly, besides oral infections with taeniid eggs, accidental subcutaneous oncosphere establishment after egg-contamination of open wounds was suggested, especially in cases with a history of cutaneous injuries at the infection site. Taenia multiceps is mainly transmitted in a domestic cycle. Only five human coenurosis cases are published since 2000. In contrast, T. serialis coenurosis (1 human case since 2000) is primarily transmitted by wild canids. The etiological diagnosis of exotic cysticercoses is challenging. Usually, clinical material does not allow for a morphological identification, and serological tests are not available. These limitations have partly been overcome by molecular tools. Without claiming any dramatic emergence of cysticercoses and coenuroses transmitted by wild carnivores, further sporadic cases of such 'exotic' infections have to be expected.

https://www.zora.uzh.ch/id/eprint/179589/1/Deplazes_et_al.%2C_Parasites_and_Wildlife_9%282019%29_1333.pdf

Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates.

One hundred and eighty specimens of sigmodontine rodents living in sympatric conditions were collected in the Atlantic Forest in the state of Rio de Janeiro, Brazil (25 Akodon cursor, 98 Akodon montensis and 57 Oligoryzomys nigripes) to examine whether the helminth structure and component communities can be characterized among these three closely related rodents. The parasite species richness was 9 in A. cursor, 12 in A. montensis and 12 in O. nigripes. Five species were common to the three rodent species, and eight were common to A. cursor and A. montensis. The trichostrongylids - Stilestrongylus eta in A. cursor, S. aculeata in A. montensis and S. lanfrediae in O. nigripes - were the species with highest dominance frequency and determined the characterization of individual community structures. The prevalence and abundance of concurrent helminth species among rodents were significantly different. Canonical multivariate analysis demonstrated a similar helminth community structure between A. cursor and A. montensis but a high discrepancy between Akodon spp. and O. nigripes. Thus, the data indicated that small rodents such as A. cursor, A. montenis and O. nigripes that are sympatric and phylogenetically related have a different community structure, but similar component community, suggesting the role of helminth specificity and the hosts' habitats as determinants in structuring their helminth communities.

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Variation in the helminth community structure of three sympatric sigmodontine rodents from the coastal Atlantic Forest of Rio de Janeiro, Brazil

Sex-biased parasitism is rarely investigated in relation to host tolerance and resistance, which are two defense strategies hosts can adopt when challenged by parasites. Health or fitness deteriorations in less tolerant individuals with increasing parasite burden would be faster than those in more tolerant ones. Hence, the body condition and reproductive potential of an infected individual host can be considered proxies for tolerance to parasitism. We studied Mediterranean populations of the wood mouse (Apodemus sylvaticus) and its helminth parasites. We assessed their resistance using the phytohemagglutinin test and spleen size, and their tolerance using body condition in males and females and testes mass in males. In order to avoid spurious correlations, we took into account the phylogeographic structure of the Mediterranean wood mouse populations. We used a mixed model adapted from the animal model used in quantitative genetics. While helminth infection did not differ between the two sexes, females and males differed in their measured defenses. Females seem to invest more in immune defense with increasing risk of parasite diversity, but also appear to be potentially more tolerant of parasitic diversity. These results suggest the existence of sexual differences in resistance and tolerance, and that measurements of parasitic loads alone could be insufficient to detect any underlying sexual differences in the two strategies that have evolved in response to multiple parasitic attacks.

Is there sex-biased resistance and tolerance in Mediterranean wood mouse ( Apodemus sylvaticus ) populations facing multiple helminth infections?

The helminth community of the wood mouse, Apodemus sylvaticus, in the Sierra Espuna was characterized after a complete analysis of its helminth community component and infracommunity structure relative to host age, sex and year of capture. The helminth community comprised 13 species: one trematode, four cestodes and eight nematodes. The cestode Pseudocatenotaenia matovi and the nematode Syphacia frederici were the most prevalent and abundant helminth species, respectively. Sixty four percent of mice analysed presented helminths with a direct cycle and 42% presented helminths with an indirect cycle. The helminth community presents a low diversity with infracommunities usually made up of only one or two helminth species. Host age and year of capture seem to play a major role in determining species richness and helminth diversity, but not in determining the abundance of helminths. Host sex does not seem to affect the infection rate nor the diversity. Further studies on more samples of wood mice and other small mammal species in this regional park are needed to explore any possible interactions between helminth communities in the host populations.

The helminth community of the wood mouse, Apodemus sylvaticus, in the Sierra Espuna, Murcia, Spain.

The Spanish mountain range of Gredos was included in the studies conducted on the Iberian peninsula to investigate helminth fauna of small mammals. The helminth community of the wood mouse, Apodemus sylvaticus (Rodentia, Muridae), was analysed. Qualitatively, 13 helminth species were detected: Plagiorchis sp. I and Plagiorchis sp. II (Trematoda); Taenia parva larvae, T. martis larvae, T. taeniaeformis larvae, Rodentolepis straminea and R. fraterna (Cestoda); and Trichuris muris, Heligmosomoides polygyrus, Syphacia stroma, S. frederici, Aspiculuris tetraptera and Rictularia proni (Nematoda). Quantitatively, the highest prevalence (65.0%) and the mean abundance (36.9%) of H. polygyrus stand out. In comparison with the other mountain ranges studied, analysis of the global results demonstrates that the helminth fauna of the host species studied is diverse despite the adverse climatic conditions. This could be related to both the particular ecological characteristics and the appropriate state of preservation of this ecosystem.

S. Sáez

Papers

The helminth community of the wood mouse, Apodemus sylvaticus, in the Sierra Espuna, Murcia, Spain.

The helminth community of Apodemus sylvaticus (Rodentia, Muridae) in the Sierra de Gredos (Spain)