Linking parasitism to network centrality and the impact of sampling bias in its interpretation
Group living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission because increased numbers or frequencies of social contacts are often associated with increased parasite abundance or diversity. The social structure of a group...
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PeerJ Inc.
2022-11-01
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author | Zhihong Xu Andrew J.J. MacIntosh Alba Castellano-Navarro Emilio Macanás-Martínez Takafumi Suzumura Julie Duboscq |
author_facet | Zhihong Xu Andrew J.J. MacIntosh Alba Castellano-Navarro Emilio Macanás-Martínez Takafumi Suzumura Julie Duboscq |
author_sort | Zhihong Xu |
collection | DOAJ |
description | Group living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission because increased numbers or frequencies of social contacts are often associated with increased parasite abundance or diversity. The social structure of a group or population is paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the links between sociality and parasitism in animals, especially in primates, have only accounted for parts of the group (e.g., only adults), which is likely to impact the interpretation of results. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a whole group of Japanese macaques (Macaca fuscata). We then tested the impact of omitting parts of the group on this relationship. We aimed to test: (1) whether social network centrality –in terms of the number of partners (degree), frequency of interactions (strength), and level of social integration (eigenvector) –was linked to parasite infection intensity (estimated by eggs per gram of faeces, EPG); and, (2) to what extent excluding portions of individuals within the group might influence the observed relationship. We conducted social network analysis on data collected from one group of Japanese macaques over three months on Koshima Island, Japan. We then ran a series of knock-out simulations. General linear mixed models showed that, at the whole-group level, network centrality was positively associated with geohelminth infection intensity. However, in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still generally positive - lost statistical significance. Furthermore, knock-out simulations where individuals were removed but network metrics were retained from the original whole-group network showed that these changes are partly a power issue and partly an effect of sampling the incomplete network. Our study indicates that sampling bias can thus hamper our ability to detect real network effects involving social interaction and parasitism. In addition to supporting earlier results linking geohelminth infection to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with implications for infectious disease epidemiology, population management, and health interventions. |
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publishDate | 2022-11-01 |
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spelling | doaj.art-a95fbc17cee14047b9aa83a8d0bb5b152023-12-02T21:55:49ZengPeerJ Inc.PeerJ2167-83592022-11-0110e1430510.7717/peerj.14305Linking parasitism to network centrality and the impact of sampling bias in its interpretationZhihong Xu0Andrew J.J. MacIntosh1Alba Castellano-Navarro2Emilio Macanás-Martínez3Takafumi Suzumura4Julie Duboscq5Wildlife Research Center, Kyoto University, Kyoto, Kyoto, JapanWildlife Research Center, Kyoto University, Kyoto, Kyoto, JapanEthology and Animal Welfare Section, Universidad CEU Cardenal Herrera, Valencia, Valencia, SpainEthology and Animal Welfare Section, Universidad CEU Cardenal Herrera, Valencia, Valencia, SpainWildlife Research Center, Kyoto University, Kyoto, Kyoto, JapanUMR7206 Eco-Anthropologie, CNRS-MNHN-Université de Paris, Paris, Île-de-France, FranceGroup living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission because increased numbers or frequencies of social contacts are often associated with increased parasite abundance or diversity. The social structure of a group or population is paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the links between sociality and parasitism in animals, especially in primates, have only accounted for parts of the group (e.g., only adults), which is likely to impact the interpretation of results. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a whole group of Japanese macaques (Macaca fuscata). We then tested the impact of omitting parts of the group on this relationship. We aimed to test: (1) whether social network centrality –in terms of the number of partners (degree), frequency of interactions (strength), and level of social integration (eigenvector) –was linked to parasite infection intensity (estimated by eggs per gram of faeces, EPG); and, (2) to what extent excluding portions of individuals within the group might influence the observed relationship. We conducted social network analysis on data collected from one group of Japanese macaques over three months on Koshima Island, Japan. We then ran a series of knock-out simulations. General linear mixed models showed that, at the whole-group level, network centrality was positively associated with geohelminth infection intensity. However, in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still generally positive - lost statistical significance. Furthermore, knock-out simulations where individuals were removed but network metrics were retained from the original whole-group network showed that these changes are partly a power issue and partly an effect of sampling the incomplete network. Our study indicates that sampling bias can thus hamper our ability to detect real network effects involving social interaction and parasitism. In addition to supporting earlier results linking geohelminth infection to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with implications for infectious disease epidemiology, population management, and health interventions.https://peerj.com/articles/14305.pdfSocialitySocial networkGeohelminthKnock-out simulationParasite transmission |
spellingShingle | Zhihong Xu Andrew J.J. MacIntosh Alba Castellano-Navarro Emilio Macanás-Martínez Takafumi Suzumura Julie Duboscq Linking parasitism to network centrality and the impact of sampling bias in its interpretation PeerJ Sociality Social network Geohelminth Knock-out simulation Parasite transmission |
title | Linking parasitism to network centrality and the impact of sampling bias in its interpretation |
title_full | Linking parasitism to network centrality and the impact of sampling bias in its interpretation |
title_fullStr | Linking parasitism to network centrality and the impact of sampling bias in its interpretation |
title_full_unstemmed | Linking parasitism to network centrality and the impact of sampling bias in its interpretation |
title_short | Linking parasitism to network centrality and the impact of sampling bias in its interpretation |
title_sort | linking parasitism to network centrality and the impact of sampling bias in its interpretation |
topic | Sociality Social network Geohelminth Knock-out simulation Parasite transmission |
url | https://peerj.com/articles/14305.pdf |
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