Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica

Durante las dos últimas décadas tanto en ecología como en epidemiología el poder entender que variables determinan la riqueza de parásitos en primates ha sido de gran interés. Se ha planteado que variables ambientales como la temperatura, la humedad relativa y la precipitación son factores que deter...

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Autores:
Galvis Ramírez, Nelson Fabián
Tipo de recurso:
Doctoral thesis
Fecha de publicación:
2024
Institución:
Universidad de los Andes
Repositorio:
Séneca: repositorio Uniandes
Idioma:
spa
OAI Identifier:
oai:repositorio.uniandes.edu.co:1992/75481
Acceso en línea:
https://hdl.handle.net/1992/75481
Palabra clave:
Primates neotropicales
Parásitos gastrointestinales
Análisis de redes sociales
Transmisión de parásitos
Estructura social
Patrones de agrupamiento
Cohesividad social
Centralidad
Modularidad
Dominancia social
Tamaño corporal
Cebus versicolor
Ateles hybridus
Sapajus apella
Biología
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openAccess
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Attribution-NonCommercial-NoDerivatives 4.0 International
id UNIANDES2_4e6771892433aeb2dbd3b883a9de15e2
oai_identifier_str oai:repositorio.uniandes.edu.co:1992/75481
network_acronym_str UNIANDES2
network_name_str Séneca: repositorio Uniandes
repository_id_str
dc.title.spa.fl_str_mv Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
title Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
spellingShingle Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
Primates neotropicales
Parásitos gastrointestinales
Análisis de redes sociales
Transmisión de parásitos
Estructura social
Patrones de agrupamiento
Cohesividad social
Centralidad
Modularidad
Dominancia social
Tamaño corporal
Cebus versicolor
Ateles hybridus
Sapajus apella
Biología
title_short Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
title_full Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
title_fullStr Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
title_full_unstemmed Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
title_sort Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológica
dc.creator.fl_str_mv Galvis Ramírez, Nelson Fabián
dc.contributor.advisor.none.fl_str_mv Stevenson Díaz, Pablo Roberto
Link Ospina, Andrés
dc.contributor.author.none.fl_str_mv Galvis Ramírez, Nelson Fabián
dc.contributor.jury.none.fl_str_mv Solórzano García, Brenda
Molina Escobar, Jorge Alberto
dc.contributor.researchgroup.none.fl_str_mv Facultad de Ciencias::Centro de Investigaciones Ecológicas la Macarena
dc.subject.keyword.spa.fl_str_mv Primates neotropicales
Parásitos gastrointestinales
Análisis de redes sociales
Transmisión de parásitos
Estructura social
Patrones de agrupamiento
Cohesividad social
Centralidad
Modularidad
Dominancia social
Tamaño corporal
topic Primates neotropicales
Parásitos gastrointestinales
Análisis de redes sociales
Transmisión de parásitos
Estructura social
Patrones de agrupamiento
Cohesividad social
Centralidad
Modularidad
Dominancia social
Tamaño corporal
Cebus versicolor
Ateles hybridus
Sapajus apella
Biología
dc.subject.keyword.none.fl_str_mv Cebus versicolor
Ateles hybridus
Sapajus apella
dc.subject.themes.spa.fl_str_mv Biología
description Durante las dos últimas décadas tanto en ecología como en epidemiología el poder entender que variables determinan la riqueza de parásitos en primates ha sido de gran interés. Se ha planteado que variables ambientales como la temperatura, la humedad relativa y la precipitación son factores que determinan la riqueza de parásitos en diferentes grupos de vertebrados. Sin embargo, los resultados de los diferentes estudios que han puesto a prueba estas variables han sido inconclusos, por consiguiente, se ha sugerido que existen otras fuerzas que tienen una mayor influencia como el tamaño del grupo, la densidad poblacional, dieta del hospedero y/o las dinámicas comportamentales. Teniendo en cuenta los diferentes supuestos asociados a las variables ambientales, poblacionales y comportamentales, en este estudio evaluamos la potencial relación entre la riqueza de parásitos gastrointestinales con el tamaño del grupo, la densidad poblacional, los patrones de agrupamiento, la estructura social, la dieta, el tamaño corporal y la dominancia social en primates, los cuales son detallados en tres capítulos distintos. En el primer capítulo, mediante un metaanálisis evaluamos si el tamaño poblacional, la densidad poblacional y la dieta explican la riqueza de las cargas parasitarias de 163 especies de primates. También, mediante un estudio de caso evaluamos si la temperatura, la humedad relativa y la pluviosidad explican la riqueza de especies en las cargas parasitarias de monos cariblancos (Cebus versicolor), monos maiceros (Sapajus apella) y monos araña café (Ateles hybridus). Los resultados de este capítulo sugieren que la riqueza de parásitos incrementa positivamente con el tamaño del grupo y la densidad poblacional, como una potencial consecuencia de un mayor riesgo de infección. Al igual que previos estudios, nuestros resultados no evidencian un patrón claro entre la dieta y la riqueza de parásitos en primates, rechazando la hipótesis de que el tipo de dieta puede determinar la comunidad de parásitos del hospedero. También, se encontró que ni la temperatura, la humedad y la precipitación explican la riqueza de parásitos en las tres especies de primates estudiadas. Sin embargo, existe una tendencia a observarse una mayor riqueza de parásitos durante la época seca en la tropa de monos araña café y de cariblancos. Los resultados de este trabajo son un aporte para el entendimiento de los factores que influencian las cargas parasitarias en primates neotropicales, evidenciando la complejidad de las dinámicas de transmisión de parásitos. En el segundo capítulo, implementando análisis de redes sociales describimos como la estructura social, los patrones de cohesividad, la jerarquía social, el tamaño corporal y las relaciones entre individuos medidas a través de métricas de centralidad, influencian las cargas parasitarias y las dinámicas de transmisión de parásitos en monos araña café (Ateles hybridus), monos maiceros (Sapajus apella) y (Cebus versicolor) que habitan en bosques de tierras bajas en Colombia. Los resultados de este estudio resaltan la fluidez en los patrones de agrupación y la estructura social altamente modular de la tropa de monos araña, aportando evidencia a la complejidad de la estructura social tipo fisión – fusión que ha sido reportada en otras especies de monos araña. Adicionalmente, se encontró que esta especie ajusta su patrón de agrupación a la disponibilidad de recursos observándose una menor cohesividad durante las épocas de escases. En contraste tanto en los monos maiceros y los monos cariblancos, se registró una mayor cohesividad y una estructura grupal compacta, la cual no es afectada por la productividad de frutos. Adicionalmente, se encontró que la estructura social no explica la riqueza de parásitos en ninguna de las tres especies de primates. En los monos maiceros y en los monos cariblancos no se encontró una relación entre la cohesividad de los grupos con la riqueza de especies de sus cargas parasitarias, mientras que en los monos araña se evidenció que el patrón de agrupamiento explica las cargas parasitarias, registrándose una mayor riqueza de parásitos durante los periodos de cohesividad social más altos. Al combinar estos resultados con la estructura social altamente modular observada en los monos araña, se evidencia que este estudio soporta la hipótesis del cuello de botella epidemiológico. En las tres especies de primates se determinó la importancia de los integrantes de las tropas a través de la centralidad por fuerza, intermediación y de vector propio. En los monos cariblancos se encontró que los individuos con alta centralidad por fuerza poseen una mayor riqueza de parásitos. No obstante, en los monos araña los individuos con alta centralidad por intermediación tienen una mayor riqueza de especies en sus cargas parasitarias. Aunque en los monos maiceros se encontró la misma tendencia que en los monos araña, al incluir en el modelo la dominancia social, se observó que esta por si sola explica la riqueza de las cargas parasitarias, sugiriendo que los individuos con alta jerarquía tienden a tener comunidades de parásitos más grandes que individuos subordinados. Los resultados de este capítulo aportan al entendimiento de las dinámicas de transmisión de parásitos y a la socio- ecología de los monos araña café, los monos cariblancos y monos maiceros a través de acercamientos analíticos novedosos y registros de información de manera no invasiva. Resalta las dinámicas sociales inherentes de la especie como factores determinantes en la transmisión de parásitos y las cargas parasitarias. Finalmente, en el tercer capítulo describimos como las interacciones sociales, el tamaño corporal y la dominancia determinan las cargas parasitarias en una tropa de monos maiceros (Sapajus apella). Adicionalmente, se evaluó si la productividad de frutos carnosos determina los patrones comportamentales de los individuos de la tropa, su masa corporal o si esta es explicada por su estatus social. También, de manera experimental se determinó si las cargas parasitarias representan un costo energético para el hospedero. Además, determinamos la compensación social para los individuos dominantes de la tropa. Durante 18 meses se realizaron monitoreos comportamentales usando muestreos de animal focal de todos los miembros adultos y sub-adultos de la tropa. Sistemáticamente se colectaron datos de las actividades diarias de la tropa y sus patrones comportamentales. Mensualmente se colectaron muestras fecales de todos los individuos adultos y sub-adultos. Mensualmente se registró la biomasa de los miembros del grupo, seis meses después, el 50% de los miembros recibió un tratamiento antiparasitario y se continuó con el monitoreo de la masa corporal de los individuos del grupo. Se encontró que la dominancia es la variable que mejor explica la riqueza de especies en las cargas parasitarias de la tropa de monos maiceros, sugiriendo un potencial costo asociado con el estatus social. Sin embargo, experimentalmente encontramos que las cargas parasitarias no representan un costo energético significativo para el hospedero. Observamos que la masa corporal se mantuvo relativamente estable durante los periodos de escasez, en contraste en los periodos de abundancia la mayoría de los individuos ganaron peso. Los individuos sub-adultos subordinados presentaron una mayor ganancia comparado con el resto de los miembros. Actividades como movimiento, acicalamiento y juego fueron más frecuentes durante la escasez sugiriendo un maximización de energía. También, se encontró diferencias comportamentales asociadas al estatus social, observándose al macho alfa alimentarse más frecuente y por periodos más largos, infligió más agresiones y recibió más acicalamiento que los subordinados. Adicionalmente, el macho fue más pesado que el promedio de la población. Nuestros resultados soportan la hipótesis que la ganancia en masa corporal está determinada por la disponibilidad de recursos y que el tamaño corporal está asociado con la dominancia. Aunque la posición social trae consigo un costo asociado con el riesgo de infección, se observaron una serie de beneficios sociales con el estatus. Sin embargo, el mantenimiento de esta posición genera un alto gasto en energético a través de despliegues de agresiones, evidenciándose en una pérdida de peso durante las épocas de escases y una ganancia menor de biomasa que individuos subordinados.
publishDate 2024
dc.date.issued.none.fl_str_mv 2024-12-12
dc.date.accessioned.none.fl_str_mv 2025-01-20T14:28:51Z
dc.date.available.none.fl_str_mv 2025-01-20T14:28:51Z
dc.type.none.fl_str_mv Trabajo de grado - Doctorado
dc.type.driver.none.fl_str_mv info:eu-repo/semantics/doctoralThesis
dc.type.version.none.fl_str_mv info:eu-repo/semantics/acceptedVersion
dc.type.coar.none.fl_str_mv http://purl.org/coar/resource_type/c_db06
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dc.identifier.instname.none.fl_str_mv instname:Universidad de los Andes
dc.identifier.reponame.none.fl_str_mv reponame:Repositorio Institucional Séneca
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language spa
dc.relation.references.none.fl_str_mv Abondano, L. A., & Link, A. (2012). The social behavior of brown spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. International Journal of Primatology, 33, 769-783.
Agostini, I., Vanderhoeven, E., Di Bitetti, M. S., & Beldomenico, P. M. (2017). Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys. Scientific Reports, 7(1), 12778.
Agostini, I., Vanderhoeven, E., Pfoh, R., Tiddi, B., & Beldomenico, P. M. (2023). Experimental evidence of parasite-induced behavioural alterations modulated by food availability in wild capuchin monkeys. Scientific Reports, 13(1), 3083.
Akinyi, M. Y., Jansen, D., Habig, B., Gesquiere, L. R., Alberts, S. C., & Archie, E. A. (2019). Costs and drivers of helminth parasite infection in wild female baboons. Journal of Animal Ecology, 88(7), 1029-1043.
Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Pulliam JR (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Revisions in Ecology and Evolution Systematics 34(1):517-547.
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M., & Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters, 9(4), 467-484.
Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., ... & Pulliam, J. R. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34(1), 517-547.
Altizer, S., Ostfeld, R. S., Johnson, P. T., Kutz, S., & Harvell, C. D. (2013). Climate change and infectious diseases: from evidence to a predictive framework. science, 341(6145), 514-519.
Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49(3-4), 227-266.
Altmann, J., & Alberts, S. (1987). Body mass and growth rates in a wild primate population. Oecologia, 72, 15-20.
Amici, F., Call, J., & Aureli, F. (2012). Aversion to violation of expectations of food distribution: the role of social tolerance and relative dominance in seven primate species. Behaviour, 345-368.
Anderson, R. M., & May, R. M. (1991). Infectious diseases of humans: dynamics and control. Oxford university press.
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography, 25(1), 88-94.
Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach. Behavioral Ecology and Sociobiology, 63, 649-659.
Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression, fission-fusion dynamics and feeding competition in spider monkeys. Behaviour, 983-1001.
Aureli, F., Schaffner, C. M., Asensio, N., & Lusseau, D. (2012). What is a subgroup? How socioecological factors influence interindividual distance. Behavioral Ecology, 23(6), 1308-1315.
Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., ... & Schaik, C. P. V. (2008). Fission-fusion dynamics: new research frameworks. Current Anthropology, 49(4), 627-654.
Barber, I., & Poulin, R. (2002). Interactions between fish, parasites and disease. Oxford university press.
Barelli, C., Gonzalez-Astudillo, V., Mundry, R., Rovero, F., Hauffe, H. C., & Gillespie, T. R. (2019). Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. Plos One, 14(12), e0225142.
Barton K, Barton MK (2015) Package ‘mumin’. Version 1(18):439.
Bateman, P. W., & Fleming, P. A. (2012). Big city life: carnivores in urban environments. Journal of Zoology, 287(1), 1-23.
Benavides, J. A., Huchard, E., Pettorelli, N., King, A. J., Brown, M. E., Archer, C. E., ... & Cowlishaw, G. (2012). From parasite encounter to infection: Multiple‐scale drivers of parasite richness in a wild social primate population. American Journal of Physical Anthropology, 147(1), 52-63.
Boinski, S. (1987). Habitat use by squirrel monkeys in a tropical lowland forest. Folia Primatologica, 49, 151–67.
Bordes, F., Morand, S., Krasnov, B. R., & Poulin, R. (2010). Parasite diversity and latitudinal gradients in terrestrial mammals. The Biogeography of Host-Parasite Interactions, 89, 98.
Boyer, D. M. (2008). Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. Journal of Human Evolution, 55(6), 1118-1137.
Briard, L., & Ezenwa, V. O. (2021). Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis. Animal Behaviour, 172, 171-182.
Brooks, T. M., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., Rylands, A. B., Konstant, W. R., ... & Hilton‐Taylor, C. (2002). Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology, 16(4), 909-923.
Bürkner, P. C. (2017). Advanced Bayesian multilevel modeling with the R package brms. arXiv preprint arXiv:1705.11123.
Busch, D. S., & Hayward, L. S. (2009). Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biological Conservation, 142(12), 2844-2853.
Campbell, C. J., Fuentes, A., MacKinnon, K. C., Bearder, S. K., & Stumpf, R. (2010). Primates in Perspective. Oxford University Press.
Chapman, C. A., Chapman, L. J., & Wrangham, R. W. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59-70.
Chapman, C. A., Friant, S., Godfrey, K., Liu, C., Sakar, D., Schoof, V. A., ... & Goldberg, T. L. (2016). Social behaviours and networks of vervet monkeys are influenced by gastrointestinal parasites. PloS One, 11(8), e0161113.
Chapman, C. A., Gillespie, T. R., & Speirs, M. L. (2005). Parasite prevalence and richness in sympatric colobines: effects of host density. American Journal of Primatology, 67(2), 259-266.
Chapman, C. A., Rothman, J. M., & Hodder, S. A. (2009). Can parasite infections be a selective force influencing primate group size? A test with red colobus. Primate parasite ecology. The dynamics and study of host-parasite relationships. Cambridge University, Cambridge, 423-440.
Chapman, C. A., Speirs, M. L., Hodder, S. A., & Rothman, J. M. (2010). Colobus monkey parasite infections in wet and dry habitats: implications for climate change. African Journal of Ecology, 48(2), 555-558.
Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L., Lawes, M. J., Saj, T. L., & Ziegler, T. E. (2006). Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. American Journal of Physical Anthropology, 131(4), 525-534.
Chase, J. M., Abrams, P. A., Grover, J. P., Diehl, S., Chesson, P., Holt, R. D., ... & Case, T. J. (2002). The interaction between predation and competition: a review and synthesis. Ecology Letters, 5(2), 302-315.
Clutton-Brock, T. (2016). Mammal societies. John Wiley & Sons.
Clutton-Brock, T. H., Albon, S. D., Gibson, R. M., & Guinness, F. E. (1979). The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Animal Behaviour, 27, 211-225.
Conradt, L., & Roper, T. J. (2000). Activity synchrony and social cohesion: a fission-fusion model. Proceedings of the Royal Society of London. Series B, 267(1458), 2213-2218.
Coop, R. L., & Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology, 26(8-9), 951-962.
Correa-Gómez, D. F., & Stevenson, P. R. (2010). Structure and diversity of riparian forests in a seasonal savanna of the Llanos Orientales Colombianos (Tomo Grande Reserva, Vichada. Orinoquia, 14, 31-48.
Csardi G., & Nepusz T. (2006) The igraph software. Complex Systems, 1695:1-9.
Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science, 287(5452), 443-449.
de Souza Jesus, A., de Oliveira-Ramalho, M. L., El Bizri, H. R., Valsecchi, J., & Mayor, P. (2022). Environmental and biological drivers of prevalence and number of eggs and oocysts of intestinal parasites in red howler monkeys from Central Amazonia. Folia Primatologica, 93(2), 121-138.
Defler, T. R. (2010). Historia natural de los primates colombianos. Universidad Nacional de Colombia.
Defolie, C., Merkling, T., & Fichtel, C. (2020). Patterns and variation in the mammal parasite–glucocorticoid relationship. Biological Reviews, 95(1), 74-93.
di Bitetti, M. S. (1997). Evidence for an important social role of allogrooming in a platyrrhine primate. Animal Behaviour, 54(1), 199-211.
Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. Spider monkeys: Behavior, ecology and evolution of the genus Ateles, 81-137.
Dietz, J. M., Baker, A. J., & Miglioretti, D. (1994). Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 34(2), 115-132.
Dirzo, R., & Raven, P. H. (2003). Global state of biodiversity and loss. Annual Review of Environment and Resources, 28(1), 137-167.
Dobson, A., & Foufopoulos, J. (2001). Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London. Series B, 356(1411), 1001-1012.
Dobson, A., & Meagher, M. (1996). The population dynamics of brucellosis in the Yellowstone National Park. Ecology, 77(4), 1026-1036.
Drewe, J. A. (2010). Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings of the Royal Society B, 277(1681), 633-642.
Duboscq, J., Romano, V., & MacIntosh, A. J. (2019). Social behavior and infectious disease. Encyclopedia of Animal Behavior, 790-800.
Duboscq, J., Romano, V., Sueur, C., & MacIntosh, A. J. (2016). Network centrality and seasonality interact to predict lice load in a social primate. Scientific Reports, 6(1), 22095.
Dufour, J. P., Cogswell, F. B., Phillippi‐Falkenstein, K. M., & Bohm, R. P. (2006). Comparison of efficacy of moxidectin and ivermectin in the treatment of Strongyloides fulleborni infection in rhesus macaques. Journal of Medical Primatology, 35(3), 172-176.
Ebert, D., Lipsitch, M., & Mangin, K. L. (2000). The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist, 156(5), 459-477.
Eisenberg, J. F. (1981). The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. The University of Chicago Press, Chicago.
Eisenberg, J. F., Muckenhirn, N. A., & Rundran, R. (1972). The relation between ecology a social structure in primates. Science, 176(4037), 863-874.
Estrada-Villegas, S., Rivas, L. D., Barrera, J. F., Barrera Rivas, S., Correa, D. F., Argüello Bernal, L. S., ... & Stevenson, P. (2022). Plant, bird, and mammal diversity of the Tomogrande field station, Vichada, Colombia. Biota Colombiana, 23(2).
Evans, J. C., Hodgson, D. J., Boogert, N. J., & Silk, M. J. (2021). Group size and modularity interact to shape the spread of infection and information through animal societies. Behavioral Ecology and Sociobiology, 75, 1-14.
Evans, J. C., Silk, M. J., Boogert, N. J., & Hodgson, D. J. (2020). Infected or informed? Social structure and the simultaneous transmission of information and infectious disease. Oikos, 129(9), 1271-1288.
Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology, 15(3), 446-454.
Ezenwa, V. O. (2004). Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology, 34(4), 535-542.
Ezenwa, V. O., & Worsley-Tonks, K. E. (2018). Social living simultaneously increases infection risk and decreases the cost of infection. Proceedings of the Royal Society B, 285(1892), 20182142.
Ezenwa, V. O., Archie, E. A., Craft, M. E., Hawley, D. M., Martin, L. B., Moore, J., & White, L. (2016). Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology. Proceedings of the Royal Society B, 283(1828), 20153078.
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34(1), 487-515.
Farine, D. R., & Whitehead, H. (2015). Constructing, conducting and interpreting animal social network analysis. Journal of Animal Ecology, 84(5), 1144-1163.
Fedigan, L. M., & Jack, K. (2004). The demographic and reproductive context of male replacements in Cebus capucinus. Behaviour, 141(6), 755-7.
Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., ... & Lindenmayer, D. B. (2009). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology, 20(4), 685-690.
Fragaszy, D. M., Izar, P., Liu, Q., Eshchar, Y., Young, L. A., & Visalberghi, E. (2016). Body mass in wild bearded capuchins, (Sapajus libidinosus): Ontogeny and sexual dimorphism. American Journal of Primatology, 78(4), 473-484.
Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica, 8(1), 12-24.
Freeland, W. J. (1979). Primate social groups as biological islands. Ecology, 60(4), 719-728.
Friant, S., Ziegler, T. E., & Goldberg, T. L. (2016). Primate reinfection with gastrointestinal parasites: behavioural and physiological predictors of parasite acquisition. Animal Behaviour, 117, 105-113.
Fujii K, Jin J, Vandeleest J et al (2021) Perc: using percolation and conductance to find information flow certainty in a direct network. R package version 0.1. https://cran.r-project.org/web/packages/Perc/index.html
Galvis, N. F., Rodríguez, D., & Stevenson, P. R. (2024). Body Mass Gain in Wild Brown Capuchins (Sapajus apella) in Relation to Fruit Production and Social Dominance. American Journal of Primatology, e23683.
Garamszegi, L. Z. (2011). Climate change increases the risk of malaria in birds. Global Change Biology, 17(5), 1751-1759.
Gazes, R. P., Schrock, A. E., Leard, C. N., & Lutz, M. C. (2022). Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks. American Journal of Primatology, 84(3), e23365.
Ghai, R. R., Fugere, V., Chapman, C. A., Goldberg, T. L., & Davies, T. J. (2015). Sickness behaviour associated with non-lethal infections in wild primates. Proceedings of the Royal Society B, 282(1814), 20151436.
Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology, 27, 1129-1143.
Gillespie, T. R., & Chapman, C. A. (2006). Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology, 20(2), 441-448.
Gillespie, T. R., & Chapman, C. A. (2008). Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. American Journal of Primatology, 70(3), 222-230.
Godfrey, S. S., Keatley, S., Botero, A., Thompson, C. K., Wayne, A. F., Lymbery, A. J., ... & Thompson, R. A. (2018). Trypanosome co-infections increase in a declining marsupial population. International Journal for Parasitology: Parasites and Wildlife, 7(2), 221-227.
Godfrey, S. S., Moore, J. A., Nelson, N. J., & Bull, C. M. (2010). Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). International Journal for Parasitology, 40(13), 1575-1585.
Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T., & Evans, R. (1988). Seasonal food shortages, weight loss, and the timing of births in saddle-backed tamarins (Saguinus fuscicollis). Journal of Animal Ecology, 57, 893–902.
Gómez-Posada, C., Rey-Goyeneche, J., & Tenorio, E. A. (2019). Ranging responses to fruit and arthropod availability by a tufted capuchin group (Sapajus apella) in the Colombian Amazon. Movement Ecology of Neotropical Forest Mammals: Focus on Social Animals, (pp. 195-215). Switzerland: Springer.
Gómez, J. M., Nunn, C. L., & Verdú, M. (2013). Centrality in primate–parasite networks reveals the potential for the transmission of emerging infectious diseases to humans. Proceedings of the National Academy of Sciences, 110(19), 7738-7741.
Gonçalves, G. H. P., Leal, D. A. G., Roratto, P. A., de Souza Junior, J. C., Souza, S. S., Peruchi, A. R., ... & Greinert-Goulart, J. A. (2024). Diversity of gastrointestinal parasites and molecular characterization of Giardia duodenalis in free-living and captive howler monkeys (Alouatta guariba clamitans) in southern Brazil. Veterinary Parasitology: Regional Studies and Reports, 52, 101048.
Gregory, R. D., Keymer, A. E., & Harvey, P. H. (1996). Helminth parasite richness among vertebrates. Biodiversity & Conservation, 5, 985-997.
Griffin, R. H., & Nunn, C. L. (2012). Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology, 26, 779-800.
Guégan, J. F., & Kennedy, C. R. (1993). Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis. Parasitology, 106(1), 91-100.
Gutiérrez, J. S., Piersma, T., & Thieltges, D. W. (2019). Micro‐and macroparasite species richness in birds: The role of host life history and ecology. Journal of Animal Ecology, 88(8), 1226-1239.
Habig B, Jansen DA, Akinyi MY, Gesquiere LR, Alberts SC, Archie EA (2019) Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus). Behavioral Ecology and Sociobiology, 73:1–16.
Habig, B., & Archie, E. A. (2015). Social status, immune response and parasitism in males: a meta-analysis. Philosophical Transactions of the Royal Society B, 370(1669), 20140109.
Habig, B., Chowdhury, S., Monfort, S. L., Brown, J. L., Swedell, L., & Foerster, S. (2021). Predictors of helminth parasite infection in female chacma baboons (Papio ursinus). International Journal for Parasitology: Parasites and Wildlife, 14, 308-320.
Habig, B., Doellman, M. M., Woods, K., Olansen, J., & Archie, E. A. (2018). Social status and parasitism in male and female vertebrates: a meta-analysis. Scientific Reports, 8(1), 3629.
Hawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E., & Stephenson, J. F. (2021). Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology, 148(3), 274-288.
Henzi, S. P., Lusseau, D., Weingrill, T., Van Schaik, C. P., & Barrett, L. (2009). Cyclicity in the structure of female baboon social networks. Behavioral Ecology and Sociobiology, 63, 1015-1021.
Hernandez, A. D., MacIntosh, A. J., & Huffman, M. A. (2009). Primate parasite ecology: patterns and predictions from an on-going study of Japanese macaques. Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, 387-402.
Herrera, J., & Nunn, C. L. (2019). Behavioural ecology and infectious disease: implications for conservation of biodiversity. Philosophical Transactions of the Royal Society B, 374(1781), 20180054.
Holmes, P. H. (1993). Interactions between parasites and animal nutrition: the veterinary consequences. Proceedings of the Nutrition Society, 52(1), 113-120.
Horii, Y., Imada, I., Yanagida, T., Usui, M., & Mori, A. (1982). Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates, 23, 416-431.
Hoyt, J. R., Langwig, K. E., White, J. P., Kaarakka, H. M., Redell, J. A., Kurta, A., ... & Kilpatrick, A. M. (2018). Cryptic connections illuminate pathogen transmission within community networks. Nature, 563(7733), 710-713.
Hudson, P. J., Dobson, A. P., & Newborn, D. (1999). TECHNICAL COMMENTS-Population Cycles and Parasitism-Response. Science-International Edition-AAAS, 286(5449).
Isbell, L. A., Pruetz, J. D., Lewis, M., & Young, T. P. (1999). Rank differences in ecological behavior: a comparative study of patas monkeys (Erythrocebus patas) and vervets (Cercopithecus aethiops). International Journal of Primatology, 20, 257-272.
Izar, P., Verderane, M. P., Peternelli‐dos‐Santos, L., Mendonça‐Furtado, O., Presotto, A., Tokuda, M., ... & Fragaszy, D. (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology, 74(4), 315-331.
Jack, K. M., Schoof, V. A., Sheller, C. R., Rich, C. I., Klingelhofer, P. P., Ziegler, T. E., & Fedigan, L. (2014). Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus). General and Comparative Endocrinology, 195, 58-67.
Janson C.H (1986). The matting system as a determinant of social evolution in capuchin monkeys (Cebus). In J. Else & P. Lee (Eds.). Primate ecology and conservation (pp. 169–179), Cambridge, UK: Cambridge University Press.
Janson, C. (1985). Aggresive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18, 125-138.
Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure. In J. G., Fleagle, C. H. Janson & K. Reed (Eds.). Primate Communities (pp. 237–267). Cambridge: Cambridge University Press.
Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates: foraging costs and predation risks. Behavioral Ecology, 6(3), 326-336.
Janson, C.H. (1984). Female choice and matting system of the brown capuchin (Cebus apella). Zeitschrift fur Tierpsychologie 85:177-200.
Johnson-Delaney, C. A. (2009). Parasites of captive nonhuman primates. Veterinary Clinics: Exotic Animal Practice, 12(3), 563-581.
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, 451(7181), 990-993.
Kamiya, T., ODwyer, K., Nakagawa, S., & Poulin, R. (2014). What determines species richness of parasitic organisms? A meta‐analysis across animal, plant and fungal hosts. Biological Reviews, 89(1), 123-134.
Kappeler, P. M. (2017). Sex roles and adult sex ratios: insights from mammalian biology and consequences for primate behaviour. Philosophical Transactions of the Royal Society B, 372(1729), 20160321.
Kappeler, P. M. (2019). A framework for studying social complexity. Behavioral Ecology and Sociobiology, 73, 1-14.
Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707-740.
Kappeler, P. M., Barrett, L., Blumstein, D. T., & Clutton-Brock, T. H. (2013). Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philosophical Transactions of the Royal Society B, 368(1618), 20120337.
Kappeler, P. M., Clutton-Brock, T., Shultz, S., & Lukas, D. (2019). Social complexity: patterns, processes, and evolution. Behavioral Ecology and Sociobiology, 73, 1-6.
Kappeler, P. M., Cremer, S., & Nunn, C. L. (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Philosophical Transactions of the Royal Society B, 370(1669), 20140116.
Kappeler, P. M., Periera, M. E., & van Schaik, C. P. (2003). Primate life histories. In Primate Life Histories and Socioecology (pp. 25-40). University of Chicago Press Chicago.
Kessler, M. J., Yarbrough, B., Rawlins, R. G., & Berard, J. (1984). Intestinal Parasites of the Free‐Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatto). Journal of Medical Primatology, 13(2), 57-66.
Köndgen, S., Kühl, H., NGoran, P. K., Walsh, P. D., Schenk, S., Ernst, N., ... & Leendertz, F. H. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology, 18(4), 260-264.
Krause, J., Hensor, E. M. A., & Ruxton, G. D. (2002). 13 Fish as Prey. E-CONTENTS, 284.
Krause, J., Hensor, E. M. A., & Ruxton, G. D. (2002). Chapter: 13 Fish as Prey. E-CONTENTS, 284.
Krause, J., James, R., Franks, D. W., & Croft, D. P. (Eds.). (2015). Animal social networks. Oxford University Press, USA.
Kuznetsova A, Brockhoff PB, Christensen RH (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistic Softwares, 82:1–26.
Kuznetsova, A. (2015). Package ‘lmerTest’. R Package Version, 2-0.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software, 82(13).
Lempang, M. E. P., Dewayanti, F. K., Syahrani, L., Permana, D. H., Malaka, R., Asih, P. B. S., & Syafruddin, D. (2022). Primate malaria: an emerging challenge of zoonotic malaria in Indonesia. One Health, 14, 100389.
Leung, T. L., & Koprivnikar, J. (2019). Your infections are what you eat: how host ecology shapes the helminth parasite communities of lizards. Journal of Animal Ecology, 88(3), 416-426.
Li, J., Dong, H., Wang, R., Yu, F., Wu, Y., Chang, Y., ... & Zhang, L. (2017). An investigation of parasitic infections and review of molecular characterization of the intestinal protozoa in nonhuman primates in China from 2009 to 2015. International Journal for Parasitology: Parasites and Wildlife, 6(1), 8-15.
Lima, L. B., Bellay, S., Giacomini, H. C., Isaac, A., & Lima-Junior, D. P. (2016). Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain. Parasitology, 143(3), 343-349.
Lynch-Alfaro, J. W. (2007). Subgrouping patterns in a group of wild Cebus apella nigritus. International Journal of Primatology, 28, 271-289.
Lynch-Alfaro, J. W. L., Silva Jr, J. D. S. E., & Rylands, A. B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74(4), 273-286.
MacIntosh, A. J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M. A., & Hernandez, A. D. (2012). Monkeys in the middle: parasite transmission through the social network of a wild primate. PloS One, 7(12), e51144.
Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness‐related benefits of dominance in primates. American Journal of Physical Anthropology, 147(4), 652-660.
Manson, J. H., Rose, L. M., Perry, S., & Gros-Louis, J. (1999). Dynamics of female–female relationships in wild Cebus capucinus: data from two Costa Rican sites. International Journal of Primatology, 20, 679-706.
Martínez-Mota, R., Kowalewski, M. M., & Gillespie, T. R. (2015). Ecological determinants of parasitism in howler monkeys: Howler monkeys: Adaptive radiation, Systematics, and Morphology, 259-285.
Martínez‐Mota, R., Garber, P. A., Palme, R., & Gillespie, T. R. (2017). The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra). American Journal of Primatology, 79(8), e22669.
McElroy, E. J., & De Buron, I. (2014). Host performance as a target of manipulation by parasites: a meta-analysis. The Journal of Parasitology, 100(4), 399-410.
Meade, B. J. (1984). Host-parasite Dynamics Amoun Amboseli Baboons (Doctoral dissertation).
Mendonça-Furtado, O., Edaes, M., Palme, R., Rodrigues, A., Siqueira, J., & Izar, P. (2014). Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behavioural Processes, 109, 79-88.
Milotic, M., Lymbery, A., Thompson, A., Doherty, J. F., & Godfrey, S. (2020). Parasites are endangered by the conservation of their hosts: Meta-analyses of the effect of host captivity on the odds of parasite infection. Biological Conservation, 248, 108702.
Milton, K. (1980). The Foraging Strategy of Howler Monkeys. New York: Columbia University Press.
Milton, K., & May, M. L. (1976). Body weight, diet and home range area in primates. Nature, 259(5543), 459-462.
Møller, A. P., Dufva, R. E. I. J. A., & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behavior, 22(65102), 60405-2.
Montenegro, M. M. V. (2011). Ecologia de Cebus flavius (Schreber, 1774) em remanescentes de Mata Atlântica no estado da Paraíba. Doctoral dissertation, Universidade de São Paulo.
Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.
Morand, S., & Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology, 12, 717-727.
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., ... & Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology, 121(1), 65-73.
Moreira, C. M., Peternelli dos Santos, L., de Sousa, M. B. C., & Izar, P. (2016). Variation in glucocorticoid levels: survival and reproductive demands in wild black capuchins (Sapajus nigritus). International Journal of Psychological Research, 9(2), 20-29.
Mosdossy, K. N., Melin, A. D., & Fedigan, L. M. (2015). Quantifying seasonal fallback on invertebrates, pith, and bromeliad leaves by white‐faced capuchin monkeys (Cebus capucinus) in a tropical dry forest. American Journal of Physical Anthropology, 158(1), 67-77.
Muehlenbein, M. P., & Watts, D. P. (2010). The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. BioPsychoSocial Medicine, 4, 1-12.
Müller-Klein, N., Heistermann, M., Strube, C., Morbach, Z. M., Lilie, N., Franz, M., ... & Ostner, J. (2019). Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate. Behavioral Ecology, 30(2), 322-335.
Munger, J. C., & Karasov, W. H. (1989). Sublethal parasites and host energy budgets: Tapeworm infection in white‐footed mice. Ecology, 70(4), 904-9.
Murray, D. L., Cary, J. R., & Keith, L. B. (1997). Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology, 250-264.
Myall, A., Price, J. R., Peach, R. L., Abbas, M., Mookerjee, S., Zhu, N., ... & Barahona, M. (2022). Prediction of hospital-onset COVID-19 infections using dynamic networks of patient contact: an international retrospective cohort study. The Lancet Digital Health, 4(8), e573-e583.
Natoli, E., Say, L., Cafazzo, S., Bonanni, R., Schmid, M., & Pontier, D. (2005). Bold attitude makes male urban feral domestic cats more vulnerable to Feline Immunodeficiency Virus. Neuroscience & Biobehavioral Reviews, 29(1), 151-157.
Newton-Fisher, N. E., Reynolds, V., & Plumptre, A. J. (2000). Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. International Journal of Primatology, 21(4), 613-628.
Nunn CL, Craft ME, Gillespie TR et al (2015) The sociality–health–fitness nexus: synthesis, conclusions and future directions. Philosophical Transactions of the Royal Society B, 370(1669):20140115
Nunn, C. L., & Altizer, S. M. (2005). The global mammal parasite database: an online resource for infectious disease records in wild primates. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 14(1), 1-2.
Nunn, C. L., & Altizer, S. M. (2006). Infectious diseases in primates: behaviour. Ecology and evolution. Oxford University Press.
Nunn, C. L., Altizer, S. M., Sechrest, W., & Cunningham, A. A. (2005). Latitudinal gradients of parasite species richness in primates. Diversity and Distributions, 11(3), 249-256.
Nunn, C. L., Altizer, S., Jones, K. E., & Sechrest, W. (2003). Comparative tests of parasite species richness in primates. The American Naturalist, 162(5), 597-614.
Nunn, C. L., Craft, M. E., Gillespie, T. R., Schaller, M., & Kappeler, P. M. (2015). The sociality–health–fitness nexus: synthesis, conclusions and future directions. Philosophical Transactions of the Royal Society B, 370(1669), 20140115.
Nunn, C., & Altizer, S. (2006). Infectious diseases in primates: behavior, ecology and evolution. OUP Oxford.
Parker, J. M., Goldenberg, S. Z., Letitiya, D., & Wittemyer, G. (2020). Strongylid infection varies with age, sex, movement and social factors in wild African elephants. Parasitology, 147(3), 348-359.
Parkins, J. J., & Holmes, P. H. (1989). Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews, 2(1), 227-246.
Parr, N. A., Fedigan, L. M., & Kutz, S. J. (2013). Predictors of parasitism in wild white-faced capuchins (Cebus capucinus). International Journal of Primatology, 34, 1137-1152.
Parsons, M. B., Gillespie, T. R., Lonsdorf, E. V., Travis, D., Lipende, I., Gilagiza, B., ... & Vazquez-Prokopec, G. M. (2014). Global positioning system data-loggers: a tool to quantify fine-scale movement of domestic animals to evaluate potential for zoonotic transmission to an endangered wildlife population. PloS One, 9(11), e110984.
Patrono, L. V., Pléh, K., Samuni, L., Ulrich, M., Röthemeier, C., Sachse, A., ... & Leendertz, F. H. (2020). Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nature Microbiology, 5(7), 955-965.
Pedersen, A. B., & Fenton, A. (2015). The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31(5), 200-211.
Pereira, M. E. (1993). Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In Lemur social systems and their ecological basis (pp. 205-221). Boston, MA: Springer US.
Perry, S. (1996). Female‐female social relationships in wild white‐faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40(2), 167-182.
Perry, S., Godoy, I., & Lammers, W. (2012). The Lomas Barbudal Monkey Project: two decades of research on Cebus capucinus. Long-term Field Studies of Primates, 141-163.
Pierron, M., Sueur, C., Shimada, M., MacIntosh, A. J., & Romano, V. (2024). Epidemiological Consequences of Individual Centrality on Wild Chimpanzees. American Journal of Primatology, e23682.
Pimm, S. L., Russell, G. J., Gittleman, J. L., & Brooks, T. M. (1995). The future of biodiversity. Science, 269(5222), 347-350.
Poppi, D. P., Sykes, A. R., & Dynes, R. A. (1990). The effect of endoparasitism on host nutrition-the implications for nutrient manipulation. CABI Record Number: 19911433767
Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs, 65(3), 283-302.
Poulin, R. (2013). Explaining variability in parasite aggregation levels among host samples. Parasitology, 140(4), 541-546.
Poulin, R., & Filion, A. (2021). Evolution of social behaviour in an infectious world: comparative analysis of social network structure versus parasite richness. Behavioral Ecology and Sociobiology, 75, 1-9.
Poulin, R., & Morand, S. (2004). Parasite biodiversity. Smithsonian Institution.
Preisser, W. (2019). Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents. Ecography, 42(7), 1315-1330.
R Core Team (2023). R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna, Austria.
Ramos-Fernández, G., Boyer, D., & Gómez, V. P. (2006). A complex social structure with fission–fusion properties can emerge from a simple foraging model. Behavioral ecology and sociobiology, 60, 536-549.
Ramos-Fernández, G., Boyer, D., Aureli, F., & Vick, L. G. (2009). Association networks in spider monkeys (Ateles geoffroyi). Behavioral Ecology and Sociobiology, 63, 999-1013.
Rimbach, R., Bisanzio, D., Galvis, N., Link, A., Di Fiore, A., & Gillespie, T. R. (2015). Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philosophical Transactions of the Royal Society B, 370(1669), 20140110.
Roberts et al. (2002). Parasite community ecology and bio- diversity. Pages 63–82 In Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H., & Dobson, A. P. (Eds.). (2002). The Ecology of Wildlife diseases (Vol. 501). Oxford: Oxford University Press.
Roberts, M. G. et al. (2002). Parasite community ecology and biodiversity. In: Hudson, P. J. et al. (eds), The ecology of wildlife diseases. Oxford Univ. Press, pp. 63-82.
Romano, V., Duboscq, J., Sarabian, C., Thomas, E., Sueur, C., & MacIntosh, A. J. (2016). Modeling infection transmission in primate networks to predict centrality‐based risk. American Journal of Primatology, 78(7), 767-779.
Romano, V., MacIntosh, A. J., & Sueur, C. (2020). Stemming the flow: information, infection, and social evolution. Trends in Ecology & Evolution, 35(10), 849-853.
Romano, V., Shen, M., Pansanel, J., MacIntosh, A. J., & Sueur, C. (2018). Social transmission in networks: global efficiency peaks with intermediate levels of modularity. Behavioral Ecology and Sociobiology, 72, 1-10.
Rondón, S., Ortiz, M., León, C., Galvis, N., Link, A., & González, C. (2017). Seasonality, richness and prevalence of intestinal parasites of three neotropical primates (Alouatta seniculus, Ateles hybridus and Cebus versicolor) in a fragmented forest in Colombia. International Journal for Parasitology: Parasites and Wildlife, 6(3), 202-208.
Rozins, C., Silk, M. J., Croft, D. P., Delahay, R. J., Hodgson, D. J., McDonald, R. A., ... & Boots, M. (2018). Social structure contains epidemics and regulates individual roles in disease transmission in a group‐living mammal. Ecology and Evolution, 8(23), 12044-12055.
Rushmore, J., Bisanzio, D., & Gillespie, T. R. (2017). Making new connections: insights from primate–parasite networks. Trends in Parasitology, 33(7), 547-560.
Rushmore, J., Caillaud, D., Hall, R. J., Stumpf, R. M., Meyers, L. A., & Altizer, S. (2014). Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of the Royal Society Interface, 11(97), 20140349.
Rushmore, J., Caillaud, D., Matamba, L., Stumpf, R. M., Borgatti, S. P., & Altizer, S. (2013). Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology, 82(5), 976-986.
Rynkiewicz, E. C., Pedersen, A. B., & Fenton, A. (2015). An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in Parasitology, 31(5), 212-221.
Sadoughi, B., Anzà, S., Defolie, C., Manin, V., Müller-Klein, N., Murillo, T., ... & Wu, D. (2022). Parasites in a social world: Lessons from primates. Animal Behavior and Parasitism, 35-52.
Sah, P., Leu, S. T., Cross, P. C., Hudson, P. J., & Bansal, S. (2017). Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proceedings of the National Academy of Sciences, 114(16), 4165-4170.
Salzer, J. S., Carroll, D. S., Williams-Newkirk, A. J., Lang, S., Peterhans, J. K., Rwego, I. B., ... & Gillespie, T. R. (2015). Effects of anthropogenic and demographic factors on patterns of parasitism in African small mammal communities. Parasitology, 142(3), 512-522.
Sánchez, C. A., Becker, D. J., Teitelbaum, C. S., Barriga, P., Brown, L. M., Majewska, A. A., ... & Altizer, S. (2018). On the relationship between body condition and parasite infection in wildlife: a review and meta‐analysis. Ecology Letters, 21(12), 1869-1884.
Sapolsky, R. (2006). Social cultures among nonhuman primates. Current Anthropology, 47(4), 641-656.
Sapolsky, R. M. (2004). Social status and health in humans and other animals. Annual Revisions in Anthropology, 33(1), 393-418.
Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308(5722), 648-652.
Sargis, E. J. (2000). The functional morphology of the postcranium of Ptilocercus and Tupaiines (Scandentia, Tupaiidae): implications for the relationships of primates and other archontan mammals. City University of New York.
Schino, G., & Aureli, F. (2008). Grooming reciprocation among female primates: a meta-analysis. Biology Letters, 4(1), 9-11.
Setchell, J. M., & Dixson, A. F. (2001). Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormones and Behavior, 39(3), 177-184.
Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior, 58(5), 720-728.
Shedden, A., Dunn, J. C., Martínez-Mota, R., Cristóbal-Azkárate, J., Gillingham, P. K., MacSwiney-González, C., ... & Korstjens, A. H. (2022). Forest maturity has a stronger influence on the prevalence of spider monkeys than howler monkeys in an anthropogenically impacted rainforest landscape. Primates, 63(3), 283-291.
Shimooka, Y. (2003). Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates, 44, 83-90.
Silk, J. B. (2007). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1480), 539-559.
Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., ... & Cheney, D. L. (2010). Female chacma baboons form strong, equitable, and enduring social bonds. Behavioral Ecology and Sociobiology, 64, 1733-1747.
Silk, M. J., Croft, D. P., Delahay, R. J., Hodgson, D. J., Boots, M., Weber, N., & McDonald, R. A. (2017). Using social network measures in wildlife disease ecology, epidemiology, and management. BioScience, 67(3), 245-257.
Simmen, B., Morino, L., Blanc, S., & Garcia, C. (2021). The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates. Scientific Reports, 11(1), 14196.
Smith, J. M., & Szathmary, E. (1997). The major transitions in evolution. OUP Oxford.
Smith, K. F., Acevedo‐Whitehouse, K., & Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation, 12(1), 1-12.
Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523-559.
Smyth, K. N., & Drea, C. M. (2016). Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females. Behavioral Ecology, 27(1), 148-157.
Solórzano-García, B., & Pérez-Ponce de León, G. (2018). Parasites of neotropical primates: a review. International Journal of Primatology, 39, 155-182.
Solórzano-García, B., White, J. M., & Shedden, A. (2023). Parasitism in heterogeneous landscapes: Association between conserved habitats and gastrointestinal parasites in populations of wild mammals. Acta Tropical, 237, 106751.
Sosa, S., Puga-Gonzalez, I., Hu, F., Pansanel, J., Xie, X., & Sueur, C. (2020a). A multilevel statistical toolkit to study animal social networks: The Animal Network Toolkit Software (ANTs) R package. Scientific Reports, 10(1), 12507.
Sosa, S., Sueur, C., & Puga-González, I. (2020b). Network measures in animal social network analysis: Their strengths, limits, interpretations and uses.
Sosa, S., Sueur, C., & Puga-Gonzalez, I. (2021). Network measures in animal social network analysis: Their strengths, limits, interpretations and uses. Methods in Ecology and Evolution, 12 (1), 10–21.
Stafford, B. J., & Szalay, F. S. (2000). Craniodental functional morphology and taxonomy of dermopterans. Journal of Mammalogy, 81(2), 360-385.
Stevenson P.R, Quiñones, M. J., Ahumada, J. A. (2000). Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica, 32(3), 533-544.
Stevenson, P. R. (2001). The relationship between fruit production and primate abundance in Neotropical communities. Biological Journal of the Linnean Society, 72(1), 161-178.
Stevenson, P. R. (2004). Phenological patterns of woody vegetation at Tinigua Park, Colombia: methodological comparisons with emphasis on fruit production/Patrones fenológicos de vegetación leñosa en el Parque Tinigua, Colombia: comparaciones metodológicas con énfasis en la producción de frutos. Caldasia, 125-150.
Stevenson, P. R., Aldana, A. M., Cárdenas, S., & Negret, P. J. (2018). Flooding and soil composition determine beta diversity of lowland forests in Northern South America. Biotropica, 50(4), 568-577.
Stevenson, P. R., Quiñones, M. J., & Ahumada, J. A. (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. International Journal of Primatology, 19, 313-324.
Sueur, C., King, A. J., Conradt, L., Kerth, G., Lusseau, D., Mettke‐Hofmann, C., ... & Aureli, F. (2011b). Collective decision‐making and fission–fusion dynamics: a conceptual framework. Oikos, 120(11), 1608-1617.
Sueur, C., Petit, O., & Deneubourg, J. L. (2010). Short-term group fission processes in macaques: a social networking approach. Journal of Experimental Biology, 213(8), 1338-1346.
Sueur, C., Petit, O., De Marco, A., Jacobs, A. T., Watanabe, K., & Thierry, B. (2011). A comparative network analysis of social style in macaques. Animal Behaviour, 82(4), 845-852.
Sumner, K. M., McCabe, C. M., & Nunn, C. L. (2018). Network size, structure, and pathogen transmission: a simulation study comparing different community detection algorithms. Behaviour, 155(7-9), 639-670.
Sykes, A. R. (1994). Parasitism and production in farm animals. Animal Science, 59(2), 155-172.
Symington, M. M. (1988). Demography, ranging patterns, and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru. American Journal of Primatology, 15(1), 45-67.
Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47-61.
Teichroeb, J. A., Kutz, S. J., Parkar, U., Thompson, R. A., & Sicotte, P. (2009). Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng‐Fiema, Ghana: Possible anthropozoonotic transmission. American Journal of Physical Anthropology, 140(3), 498-507.
Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton: Princeton Univ. Press.
Terborgh, J. (1986). Keystone plant resources in the tropical forests. In M. E. Soule (Ed.). Conservation Biology: The Science of Scarcity and Diversity (pp. 330-344), Sunderland, MA: Sinauer.
Tibbetts, E. A., Pardo-Sanchez, J., & Weise, C. (2022). The establishment and maintenance of dominance hierarchies. Philosophical Transactions of the Royal Society B, 377(1845), 20200450.
Tiddi, B., Aureli, F., & Schino, G. (2012). Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate. PloS One, 7(5), e36641.
Townsend, A. K., Hawley, D. M., Stephenson, J. F., & Williams, K. E. (2020). Emerging infectious disease and the challenges of social distancing in human and non-human animals. Proceedings of the Royal Society B, 287(1932), 20201039.
Tutin, C. E., Ham, R. M., White, L. J., & Harrison, M. J. (1997). The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42(1), 1-24.
Ungerfeld, R., & Correa, O. (2007). Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs. Applied Animal Behaviour Science, 105(1-3), 249-253.
Van Schaik, C. P. (1983). Why are diurnal primates living in groups?. Behaviour, 120-144.
Vitone, N. D., Altizer, S., & Nunn, C. L. (2004). Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research, 6(2), 183-199.
Vogel, E. R., & Janson, C. H. (2007). Predicting the frequency of food‐related agonism in white‐faced capuchin monkeys (Cebus capucinus), using a novel focal‐tree method. American Journal of Primatology, 69(5), 533-550.
Vogel, E. R., Munch, S. B., & Janson, C. H. (2007). Understanding escalated aggression over food resources in white-faced capuchin monkeys. Animal Behaviour, 74(1), 71-80.
White, L. A., Forester, J. D., & Craft, M. E. (2017). Using contact networks to explore mechanisms of parasite transmission in wildlife. Biological Reviews, 92(1), 389-409.
Whitten, P. L. (1983). Diet and dominance among female vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 5(2), 139-159.
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 262-300.
Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949-970.
Wren, B., Ray, I. S., Remis, M., Gillespie, T. R., & Camp, J. (2021). Social contact behaviors are associated with infection status for Trichuris sp. in wild vervet monkeys (Chlorocebus pygerythrus). Plos One, 16(4), e0240872.
Zhao, Q. K. (1994). Seasonal changes in body weight of Macaca thibetana at Mt. Emei, China. American Journal of Primatology, 32(3), 223-226.
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spelling Stevenson Díaz, Pablo Robertovirtual::22173-1Link Ospina, Andrésvirtual::22176-1Galvis Ramírez, Nelson FabiánSolórzano García, BrendaMolina Escobar, Jorge Albertovirtual::22177-1Facultad de Ciencias::Centro de Investigaciones Ecológicas la Macarena2025-01-20T14:28:51Z2025-01-20T14:28:51Z2024-12-12https://hdl.handle.net/1992/75481instname:Universidad de los Andesreponame:Repositorio Institucional Sénecarepourl:https://repositorio.uniandes.edu.co/Durante las dos últimas décadas tanto en ecología como en epidemiología el poder entender que variables determinan la riqueza de parásitos en primates ha sido de gran interés. Se ha planteado que variables ambientales como la temperatura, la humedad relativa y la precipitación son factores que determinan la riqueza de parásitos en diferentes grupos de vertebrados. Sin embargo, los resultados de los diferentes estudios que han puesto a prueba estas variables han sido inconclusos, por consiguiente, se ha sugerido que existen otras fuerzas que tienen una mayor influencia como el tamaño del grupo, la densidad poblacional, dieta del hospedero y/o las dinámicas comportamentales. Teniendo en cuenta los diferentes supuestos asociados a las variables ambientales, poblacionales y comportamentales, en este estudio evaluamos la potencial relación entre la riqueza de parásitos gastrointestinales con el tamaño del grupo, la densidad poblacional, los patrones de agrupamiento, la estructura social, la dieta, el tamaño corporal y la dominancia social en primates, los cuales son detallados en tres capítulos distintos. En el primer capítulo, mediante un metaanálisis evaluamos si el tamaño poblacional, la densidad poblacional y la dieta explican la riqueza de las cargas parasitarias de 163 especies de primates. También, mediante un estudio de caso evaluamos si la temperatura, la humedad relativa y la pluviosidad explican la riqueza de especies en las cargas parasitarias de monos cariblancos (Cebus versicolor), monos maiceros (Sapajus apella) y monos araña café (Ateles hybridus). Los resultados de este capítulo sugieren que la riqueza de parásitos incrementa positivamente con el tamaño del grupo y la densidad poblacional, como una potencial consecuencia de un mayor riesgo de infección. Al igual que previos estudios, nuestros resultados no evidencian un patrón claro entre la dieta y la riqueza de parásitos en primates, rechazando la hipótesis de que el tipo de dieta puede determinar la comunidad de parásitos del hospedero. También, se encontró que ni la temperatura, la humedad y la precipitación explican la riqueza de parásitos en las tres especies de primates estudiadas. Sin embargo, existe una tendencia a observarse una mayor riqueza de parásitos durante la época seca en la tropa de monos araña café y de cariblancos. Los resultados de este trabajo son un aporte para el entendimiento de los factores que influencian las cargas parasitarias en primates neotropicales, evidenciando la complejidad de las dinámicas de transmisión de parásitos. En el segundo capítulo, implementando análisis de redes sociales describimos como la estructura social, los patrones de cohesividad, la jerarquía social, el tamaño corporal y las relaciones entre individuos medidas a través de métricas de centralidad, influencian las cargas parasitarias y las dinámicas de transmisión de parásitos en monos araña café (Ateles hybridus), monos maiceros (Sapajus apella) y (Cebus versicolor) que habitan en bosques de tierras bajas en Colombia. Los resultados de este estudio resaltan la fluidez en los patrones de agrupación y la estructura social altamente modular de la tropa de monos araña, aportando evidencia a la complejidad de la estructura social tipo fisión – fusión que ha sido reportada en otras especies de monos araña. Adicionalmente, se encontró que esta especie ajusta su patrón de agrupación a la disponibilidad de recursos observándose una menor cohesividad durante las épocas de escases. En contraste tanto en los monos maiceros y los monos cariblancos, se registró una mayor cohesividad y una estructura grupal compacta, la cual no es afectada por la productividad de frutos. Adicionalmente, se encontró que la estructura social no explica la riqueza de parásitos en ninguna de las tres especies de primates. En los monos maiceros y en los monos cariblancos no se encontró una relación entre la cohesividad de los grupos con la riqueza de especies de sus cargas parasitarias, mientras que en los monos araña se evidenció que el patrón de agrupamiento explica las cargas parasitarias, registrándose una mayor riqueza de parásitos durante los periodos de cohesividad social más altos. Al combinar estos resultados con la estructura social altamente modular observada en los monos araña, se evidencia que este estudio soporta la hipótesis del cuello de botella epidemiológico. En las tres especies de primates se determinó la importancia de los integrantes de las tropas a través de la centralidad por fuerza, intermediación y de vector propio. En los monos cariblancos se encontró que los individuos con alta centralidad por fuerza poseen una mayor riqueza de parásitos. No obstante, en los monos araña los individuos con alta centralidad por intermediación tienen una mayor riqueza de especies en sus cargas parasitarias. Aunque en los monos maiceros se encontró la misma tendencia que en los monos araña, al incluir en el modelo la dominancia social, se observó que esta por si sola explica la riqueza de las cargas parasitarias, sugiriendo que los individuos con alta jerarquía tienden a tener comunidades de parásitos más grandes que individuos subordinados. Los resultados de este capítulo aportan al entendimiento de las dinámicas de transmisión de parásitos y a la socio- ecología de los monos araña café, los monos cariblancos y monos maiceros a través de acercamientos analíticos novedosos y registros de información de manera no invasiva. Resalta las dinámicas sociales inherentes de la especie como factores determinantes en la transmisión de parásitos y las cargas parasitarias. Finalmente, en el tercer capítulo describimos como las interacciones sociales, el tamaño corporal y la dominancia determinan las cargas parasitarias en una tropa de monos maiceros (Sapajus apella). Adicionalmente, se evaluó si la productividad de frutos carnosos determina los patrones comportamentales de los individuos de la tropa, su masa corporal o si esta es explicada por su estatus social. También, de manera experimental se determinó si las cargas parasitarias representan un costo energético para el hospedero. Además, determinamos la compensación social para los individuos dominantes de la tropa. Durante 18 meses se realizaron monitoreos comportamentales usando muestreos de animal focal de todos los miembros adultos y sub-adultos de la tropa. Sistemáticamente se colectaron datos de las actividades diarias de la tropa y sus patrones comportamentales. Mensualmente se colectaron muestras fecales de todos los individuos adultos y sub-adultos. Mensualmente se registró la biomasa de los miembros del grupo, seis meses después, el 50% de los miembros recibió un tratamiento antiparasitario y se continuó con el monitoreo de la masa corporal de los individuos del grupo. Se encontró que la dominancia es la variable que mejor explica la riqueza de especies en las cargas parasitarias de la tropa de monos maiceros, sugiriendo un potencial costo asociado con el estatus social. Sin embargo, experimentalmente encontramos que las cargas parasitarias no representan un costo energético significativo para el hospedero. Observamos que la masa corporal se mantuvo relativamente estable durante los periodos de escasez, en contraste en los periodos de abundancia la mayoría de los individuos ganaron peso. Los individuos sub-adultos subordinados presentaron una mayor ganancia comparado con el resto de los miembros. Actividades como movimiento, acicalamiento y juego fueron más frecuentes durante la escasez sugiriendo un maximización de energía. También, se encontró diferencias comportamentales asociadas al estatus social, observándose al macho alfa alimentarse más frecuente y por periodos más largos, infligió más agresiones y recibió más acicalamiento que los subordinados. Adicionalmente, el macho fue más pesado que el promedio de la población. Nuestros resultados soportan la hipótesis que la ganancia en masa corporal está determinada por la disponibilidad de recursos y que el tamaño corporal está asociado con la dominancia. Aunque la posición social trae consigo un costo asociado con el riesgo de infección, se observaron una serie de beneficios sociales con el estatus. Sin embargo, el mantenimiento de esta posición genera un alto gasto en energético a través de despliegues de agresiones, evidenciándose en una pérdida de peso durante las épocas de escases y una ganancia menor de biomasa que individuos subordinados.COLCIENCIAS convocatoria 727 del 2015Proyecto Semilla - Facultad de Ciencias, Universidad de los AndesDoctoradoPrimatologíaEpidemiologíaParasitologíaEcologíaComportamiento animal100 páginasapplication/pdfspaUniversidad de los AndesDoctorado en Ciencias - BiologíaFacultad de CienciasDepartamento de Ciencias BiológicasAttribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Dinámicas de transmisión de parásitos gastrointestinales en primates neotropicales: análisis bajo una mirada socio-ecológicaTrabajo de grado - Doctoradoinfo:eu-repo/semantics/doctoralThesisinfo:eu-repo/semantics/acceptedVersionhttp://purl.org/coar/resource_type/c_db06Texthttps://purl.org/redcol/resource_type/TDPrimates neotropicalesParásitos gastrointestinalesAnálisis de redes socialesTransmisión de parásitosEstructura socialPatrones de agrupamientoCohesividad socialCentralidadModularidadDominancia socialTamaño corporalCebus versicolorAteles hybridusSapajus apellaBiologíaAbondano, L. A., & Link, A. (2012). The social behavior of brown spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. International Journal of Primatology, 33, 769-783.Agostini, I., Vanderhoeven, E., Di Bitetti, M. S., & Beldomenico, P. M. (2017). Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys. Scientific Reports, 7(1), 12778.Agostini, I., Vanderhoeven, E., Pfoh, R., Tiddi, B., & Beldomenico, P. M. (2023). Experimental evidence of parasite-induced behavioural alterations modulated by food availability in wild capuchin monkeys. Scientific Reports, 13(1), 3083.Akinyi, M. Y., Jansen, D., Habig, B., Gesquiere, L. R., Alberts, S. C., & Archie, E. A. (2019). Costs and drivers of helminth parasite infection in wild female baboons. Journal of Animal Ecology, 88(7), 1029-1043.Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Pulliam JR (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Revisions in Ecology and Evolution Systematics 34(1):517-547.Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M., & Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters, 9(4), 467-484.Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., ... & Pulliam, J. R. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34(1), 517-547.Altizer, S., Ostfeld, R. S., Johnson, P. T., Kutz, S., & Harvell, C. D. (2013). Climate change and infectious diseases: from evidence to a predictive framework. science, 341(6145), 514-519.Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49(3-4), 227-266.Altmann, J., & Alberts, S. (1987). Body mass and growth rates in a wild primate population. Oecologia, 72, 15-20.Amici, F., Call, J., & Aureli, F. (2012). Aversion to violation of expectations of food distribution: the role of social tolerance and relative dominance in seven primate species. Behaviour, 345-368.Anderson, R. M., & May, R. M. (1991). Infectious diseases of humans: dynamics and control. Oxford university press.Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography, 25(1), 88-94.Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach. Behavioral Ecology and Sociobiology, 63, 649-659.Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression, fission-fusion dynamics and feeding competition in spider monkeys. Behaviour, 983-1001.Aureli, F., Schaffner, C. M., Asensio, N., & Lusseau, D. (2012). What is a subgroup? How socioecological factors influence interindividual distance. Behavioral Ecology, 23(6), 1308-1315.Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., ... & Schaik, C. P. V. (2008). Fission-fusion dynamics: new research frameworks. Current Anthropology, 49(4), 627-654.Barber, I., & Poulin, R. (2002). Interactions between fish, parasites and disease. Oxford university press.Barelli, C., Gonzalez-Astudillo, V., Mundry, R., Rovero, F., Hauffe, H. C., & Gillespie, T. R. (2019). Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. Plos One, 14(12), e0225142.Barton K, Barton MK (2015) Package ‘mumin’. Version 1(18):439.Bateman, P. W., & Fleming, P. A. (2012). Big city life: carnivores in urban environments. Journal of Zoology, 287(1), 1-23.Benavides, J. A., Huchard, E., Pettorelli, N., King, A. J., Brown, M. E., Archer, C. E., ... & Cowlishaw, G. (2012). From parasite encounter to infection: Multiple‐scale drivers of parasite richness in a wild social primate population. American Journal of Physical Anthropology, 147(1), 52-63.Boinski, S. (1987). Habitat use by squirrel monkeys in a tropical lowland forest. Folia Primatologica, 49, 151–67.Bordes, F., Morand, S., Krasnov, B. R., & Poulin, R. (2010). Parasite diversity and latitudinal gradients in terrestrial mammals. The Biogeography of Host-Parasite Interactions, 89, 98.Boyer, D. M. (2008). Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. Journal of Human Evolution, 55(6), 1118-1137.Briard, L., & Ezenwa, V. O. (2021). Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis. Animal Behaviour, 172, 171-182.Brooks, T. M., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., Rylands, A. B., Konstant, W. R., ... & Hilton‐Taylor, C. (2002). Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology, 16(4), 909-923.Bürkner, P. C. (2017). Advanced Bayesian multilevel modeling with the R package brms. arXiv preprint arXiv:1705.11123.Busch, D. S., & Hayward, L. S. (2009). Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biological Conservation, 142(12), 2844-2853.Campbell, C. J., Fuentes, A., MacKinnon, K. C., Bearder, S. K., & Stumpf, R. (2010). Primates in Perspective. Oxford University Press.Chapman, C. A., Chapman, L. J., & Wrangham, R. W. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59-70.Chapman, C. A., Friant, S., Godfrey, K., Liu, C., Sakar, D., Schoof, V. A., ... & Goldberg, T. L. (2016). Social behaviours and networks of vervet monkeys are influenced by gastrointestinal parasites. PloS One, 11(8), e0161113.Chapman, C. A., Gillespie, T. R., & Speirs, M. L. (2005). Parasite prevalence and richness in sympatric colobines: effects of host density. American Journal of Primatology, 67(2), 259-266.Chapman, C. A., Rothman, J. M., & Hodder, S. A. (2009). Can parasite infections be a selective force influencing primate group size? A test with red colobus. Primate parasite ecology. The dynamics and study of host-parasite relationships. Cambridge University, Cambridge, 423-440.Chapman, C. A., Speirs, M. L., Hodder, S. A., & Rothman, J. M. (2010). Colobus monkey parasite infections in wet and dry habitats: implications for climate change. African Journal of Ecology, 48(2), 555-558.Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L., Lawes, M. J., Saj, T. L., & Ziegler, T. E. (2006). Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. American Journal of Physical Anthropology, 131(4), 525-534.Chase, J. M., Abrams, P. A., Grover, J. P., Diehl, S., Chesson, P., Holt, R. D., ... & Case, T. J. (2002). The interaction between predation and competition: a review and synthesis. Ecology Letters, 5(2), 302-315.Clutton-Brock, T. (2016). Mammal societies. John Wiley & Sons.Clutton-Brock, T. H., Albon, S. D., Gibson, R. M., & Guinness, F. E. (1979). The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Animal Behaviour, 27, 211-225.Conradt, L., & Roper, T. J. (2000). Activity synchrony and social cohesion: a fission-fusion model. Proceedings of the Royal Society of London. Series B, 267(1458), 2213-2218.Coop, R. L., & Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology, 26(8-9), 951-962.Correa-Gómez, D. F., & Stevenson, P. R. (2010). Structure and diversity of riparian forests in a seasonal savanna of the Llanos Orientales Colombianos (Tomo Grande Reserva, Vichada. Orinoquia, 14, 31-48.Csardi G., & Nepusz T. (2006) The igraph software. Complex Systems, 1695:1-9.Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science, 287(5452), 443-449.de Souza Jesus, A., de Oliveira-Ramalho, M. L., El Bizri, H. R., Valsecchi, J., & Mayor, P. (2022). Environmental and biological drivers of prevalence and number of eggs and oocysts of intestinal parasites in red howler monkeys from Central Amazonia. Folia Primatologica, 93(2), 121-138.Defler, T. R. (2010). Historia natural de los primates colombianos. Universidad Nacional de Colombia.Defolie, C., Merkling, T., & Fichtel, C. (2020). Patterns and variation in the mammal parasite–glucocorticoid relationship. Biological Reviews, 95(1), 74-93.di Bitetti, M. S. (1997). Evidence for an important social role of allogrooming in a platyrrhine primate. Animal Behaviour, 54(1), 199-211.Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. Spider monkeys: Behavior, ecology and evolution of the genus Ateles, 81-137.Dietz, J. M., Baker, A. J., & Miglioretti, D. (1994). Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 34(2), 115-132.Dirzo, R., & Raven, P. H. (2003). Global state of biodiversity and loss. Annual Review of Environment and Resources, 28(1), 137-167.Dobson, A., & Foufopoulos, J. (2001). Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London. Series B, 356(1411), 1001-1012.Dobson, A., & Meagher, M. (1996). The population dynamics of brucellosis in the Yellowstone National Park. Ecology, 77(4), 1026-1036.Drewe, J. A. (2010). Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings of the Royal Society B, 277(1681), 633-642.Duboscq, J., Romano, V., & MacIntosh, A. J. (2019). Social behavior and infectious disease. Encyclopedia of Animal Behavior, 790-800.Duboscq, J., Romano, V., Sueur, C., & MacIntosh, A. J. (2016). Network centrality and seasonality interact to predict lice load in a social primate. Scientific Reports, 6(1), 22095.Dufour, J. P., Cogswell, F. B., Phillippi‐Falkenstein, K. M., & Bohm, R. P. (2006). Comparison of efficacy of moxidectin and ivermectin in the treatment of Strongyloides fulleborni infection in rhesus macaques. Journal of Medical Primatology, 35(3), 172-176.Ebert, D., Lipsitch, M., & Mangin, K. L. (2000). The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist, 156(5), 459-477.Eisenberg, J. F. (1981). The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. The University of Chicago Press, Chicago.Eisenberg, J. F., Muckenhirn, N. A., & Rundran, R. (1972). The relation between ecology a social structure in primates. Science, 176(4037), 863-874.Estrada-Villegas, S., Rivas, L. D., Barrera, J. F., Barrera Rivas, S., Correa, D. F., Argüello Bernal, L. S., ... & Stevenson, P. (2022). Plant, bird, and mammal diversity of the Tomogrande field station, Vichada, Colombia. Biota Colombiana, 23(2).Evans, J. C., Hodgson, D. J., Boogert, N. J., & Silk, M. J. (2021). Group size and modularity interact to shape the spread of infection and information through animal societies. Behavioral Ecology and Sociobiology, 75, 1-14.Evans, J. C., Silk, M. J., Boogert, N. J., & Hodgson, D. J. (2020). Infected or informed? Social structure and the simultaneous transmission of information and infectious disease. Oikos, 129(9), 1271-1288.Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology, 15(3), 446-454.Ezenwa, V. O. (2004). Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology, 34(4), 535-542.Ezenwa, V. O., & Worsley-Tonks, K. E. (2018). Social living simultaneously increases infection risk and decreases the cost of infection. Proceedings of the Royal Society B, 285(1892), 20182142.Ezenwa, V. O., Archie, E. A., Craft, M. E., Hawley, D. M., Martin, L. B., Moore, J., & White, L. (2016). Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology. Proceedings of the Royal Society B, 283(1828), 20153078.Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34(1), 487-515.Farine, D. R., & Whitehead, H. (2015). Constructing, conducting and interpreting animal social network analysis. Journal of Animal Ecology, 84(5), 1144-1163.Fedigan, L. M., & Jack, K. (2004). The demographic and reproductive context of male replacements in Cebus capucinus. Behaviour, 141(6), 755-7.Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., ... & Lindenmayer, D. B. (2009). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology, 20(4), 685-690.Fragaszy, D. M., Izar, P., Liu, Q., Eshchar, Y., Young, L. A., & Visalberghi, E. (2016). Body mass in wild bearded capuchins, (Sapajus libidinosus): Ontogeny and sexual dimorphism. American Journal of Primatology, 78(4), 473-484.Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica, 8(1), 12-24.Freeland, W. J. (1979). Primate social groups as biological islands. Ecology, 60(4), 719-728.Friant, S., Ziegler, T. E., & Goldberg, T. L. (2016). Primate reinfection with gastrointestinal parasites: behavioural and physiological predictors of parasite acquisition. Animal Behaviour, 117, 105-113.Fujii K, Jin J, Vandeleest J et al (2021) Perc: using percolation and conductance to find information flow certainty in a direct network. R package version 0.1. https://cran.r-project.org/web/packages/Perc/index.htmlGalvis, N. F., Rodríguez, D., & Stevenson, P. R. (2024). Body Mass Gain in Wild Brown Capuchins (Sapajus apella) in Relation to Fruit Production and Social Dominance. American Journal of Primatology, e23683.Garamszegi, L. Z. (2011). Climate change increases the risk of malaria in birds. Global Change Biology, 17(5), 1751-1759.Gazes, R. P., Schrock, A. E., Leard, C. N., & Lutz, M. C. (2022). Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks. American Journal of Primatology, 84(3), e23365.Ghai, R. R., Fugere, V., Chapman, C. A., Goldberg, T. L., & Davies, T. J. (2015). Sickness behaviour associated with non-lethal infections in wild primates. Proceedings of the Royal Society B, 282(1814), 20151436.Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology, 27, 1129-1143.Gillespie, T. R., & Chapman, C. A. (2006). Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology, 20(2), 441-448.Gillespie, T. R., & Chapman, C. A. (2008). Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. American Journal of Primatology, 70(3), 222-230.Godfrey, S. S., Keatley, S., Botero, A., Thompson, C. K., Wayne, A. F., Lymbery, A. J., ... & Thompson, R. A. (2018). Trypanosome co-infections increase in a declining marsupial population. International Journal for Parasitology: Parasites and Wildlife, 7(2), 221-227.Godfrey, S. S., Moore, J. A., Nelson, N. J., & Bull, C. M. (2010). Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). International Journal for Parasitology, 40(13), 1575-1585.Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T., & Evans, R. (1988). Seasonal food shortages, weight loss, and the timing of births in saddle-backed tamarins (Saguinus fuscicollis). Journal of Animal Ecology, 57, 893–902.Gómez-Posada, C., Rey-Goyeneche, J., & Tenorio, E. A. (2019). Ranging responses to fruit and arthropod availability by a tufted capuchin group (Sapajus apella) in the Colombian Amazon. Movement Ecology of Neotropical Forest Mammals: Focus on Social Animals, (pp. 195-215). Switzerland: Springer.Gómez, J. M., Nunn, C. L., & Verdú, M. (2013). Centrality in primate–parasite networks reveals the potential for the transmission of emerging infectious diseases to humans. Proceedings of the National Academy of Sciences, 110(19), 7738-7741.Gonçalves, G. H. P., Leal, D. A. G., Roratto, P. A., de Souza Junior, J. C., Souza, S. S., Peruchi, A. R., ... & Greinert-Goulart, J. A. (2024). Diversity of gastrointestinal parasites and molecular characterization of Giardia duodenalis in free-living and captive howler monkeys (Alouatta guariba clamitans) in southern Brazil. Veterinary Parasitology: Regional Studies and Reports, 52, 101048.Gregory, R. D., Keymer, A. E., & Harvey, P. H. (1996). Helminth parasite richness among vertebrates. Biodiversity & Conservation, 5, 985-997.Griffin, R. H., & Nunn, C. L. (2012). Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology, 26, 779-800.Guégan, J. F., & Kennedy, C. R. (1993). Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis. Parasitology, 106(1), 91-100.Gutiérrez, J. S., Piersma, T., & Thieltges, D. W. (2019). Micro‐and macroparasite species richness in birds: The role of host life history and ecology. Journal of Animal Ecology, 88(8), 1226-1239.Habig B, Jansen DA, Akinyi MY, Gesquiere LR, Alberts SC, Archie EA (2019) Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus). Behavioral Ecology and Sociobiology, 73:1–16.Habig, B., & Archie, E. A. (2015). Social status, immune response and parasitism in males: a meta-analysis. Philosophical Transactions of the Royal Society B, 370(1669), 20140109.Habig, B., Chowdhury, S., Monfort, S. L., Brown, J. L., Swedell, L., & Foerster, S. (2021). Predictors of helminth parasite infection in female chacma baboons (Papio ursinus). International Journal for Parasitology: Parasites and Wildlife, 14, 308-320.Habig, B., Doellman, M. M., Woods, K., Olansen, J., & Archie, E. A. (2018). Social status and parasitism in male and female vertebrates: a meta-analysis. Scientific Reports, 8(1), 3629.Hawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E., & Stephenson, J. F. (2021). Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology, 148(3), 274-288.Henzi, S. P., Lusseau, D., Weingrill, T., Van Schaik, C. P., & Barrett, L. (2009). Cyclicity in the structure of female baboon social networks. Behavioral Ecology and Sociobiology, 63, 1015-1021.Hernandez, A. D., MacIntosh, A. J., & Huffman, M. A. (2009). Primate parasite ecology: patterns and predictions from an on-going study of Japanese macaques. Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, 387-402.Herrera, J., & Nunn, C. L. (2019). Behavioural ecology and infectious disease: implications for conservation of biodiversity. Philosophical Transactions of the Royal Society B, 374(1781), 20180054.Holmes, P. H. (1993). Interactions between parasites and animal nutrition: the veterinary consequences. Proceedings of the Nutrition Society, 52(1), 113-120.Horii, Y., Imada, I., Yanagida, T., Usui, M., & Mori, A. (1982). Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates, 23, 416-431.Hoyt, J. R., Langwig, K. E., White, J. P., Kaarakka, H. M., Redell, J. A., Kurta, A., ... & Kilpatrick, A. M. (2018). Cryptic connections illuminate pathogen transmission within community networks. Nature, 563(7733), 710-713.Hudson, P. J., Dobson, A. P., & Newborn, D. (1999). TECHNICAL COMMENTS-Population Cycles and Parasitism-Response. Science-International Edition-AAAS, 286(5449).Isbell, L. A., Pruetz, J. D., Lewis, M., & Young, T. P. (1999). Rank differences in ecological behavior: a comparative study of patas monkeys (Erythrocebus patas) and vervets (Cercopithecus aethiops). International Journal of Primatology, 20, 257-272.Izar, P., Verderane, M. P., Peternelli‐dos‐Santos, L., Mendonça‐Furtado, O., Presotto, A., Tokuda, M., ... & Fragaszy, D. (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology, 74(4), 315-331.Jack, K. M., Schoof, V. A., Sheller, C. R., Rich, C. I., Klingelhofer, P. P., Ziegler, T. E., & Fedigan, L. (2014). Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus). General and Comparative Endocrinology, 195, 58-67.Janson C.H (1986). The matting system as a determinant of social evolution in capuchin monkeys (Cebus). In J. Else & P. Lee (Eds.). Primate ecology and conservation (pp. 169–179), Cambridge, UK: Cambridge University Press.Janson, C. (1985). Aggresive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18, 125-138.Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure. In J. G., Fleagle, C. H. Janson & K. Reed (Eds.). Primate Communities (pp. 237–267). Cambridge: Cambridge University Press.Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates: foraging costs and predation risks. Behavioral Ecology, 6(3), 326-336.Janson, C.H. (1984). Female choice and matting system of the brown capuchin (Cebus apella). Zeitschrift fur Tierpsychologie 85:177-200.Johnson-Delaney, C. A. (2009). Parasites of captive nonhuman primates. Veterinary Clinics: Exotic Animal Practice, 12(3), 563-581.Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, 451(7181), 990-993.Kamiya, T., ODwyer, K., Nakagawa, S., & Poulin, R. (2014). What determines species richness of parasitic organisms? A meta‐analysis across animal, plant and fungal hosts. Biological Reviews, 89(1), 123-134.Kappeler, P. M. (2017). Sex roles and adult sex ratios: insights from mammalian biology and consequences for primate behaviour. Philosophical Transactions of the Royal Society B, 372(1729), 20160321.Kappeler, P. M. (2019). A framework for studying social complexity. Behavioral Ecology and Sociobiology, 73, 1-14.Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707-740.Kappeler, P. M., Barrett, L., Blumstein, D. T., & Clutton-Brock, T. H. (2013). Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philosophical Transactions of the Royal Society B, 368(1618), 20120337.Kappeler, P. M., Clutton-Brock, T., Shultz, S., & Lukas, D. (2019). Social complexity: patterns, processes, and evolution. Behavioral Ecology and Sociobiology, 73, 1-6.Kappeler, P. M., Cremer, S., & Nunn, C. L. (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Philosophical Transactions of the Royal Society B, 370(1669), 20140116.Kappeler, P. M., Periera, M. E., & van Schaik, C. P. (2003). Primate life histories. In Primate Life Histories and Socioecology (pp. 25-40). University of Chicago Press Chicago.Kessler, M. J., Yarbrough, B., Rawlins, R. G., & Berard, J. (1984). Intestinal Parasites of the Free‐Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatto). Journal of Medical Primatology, 13(2), 57-66.Köndgen, S., Kühl, H., NGoran, P. K., Walsh, P. D., Schenk, S., Ernst, N., ... & Leendertz, F. H. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology, 18(4), 260-264.Krause, J., Hensor, E. M. A., & Ruxton, G. D. (2002). 13 Fish as Prey. E-CONTENTS, 284.Krause, J., Hensor, E. M. A., & Ruxton, G. D. (2002). Chapter: 13 Fish as Prey. E-CONTENTS, 284.Krause, J., James, R., Franks, D. W., & Croft, D. P. (Eds.). (2015). Animal social networks. Oxford University Press, USA.Kuznetsova A, Brockhoff PB, Christensen RH (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistic Softwares, 82:1–26.Kuznetsova, A. (2015). Package ‘lmerTest’. R Package Version, 2-0.Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software, 82(13).Lempang, M. E. P., Dewayanti, F. K., Syahrani, L., Permana, D. H., Malaka, R., Asih, P. B. S., & Syafruddin, D. (2022). Primate malaria: an emerging challenge of zoonotic malaria in Indonesia. One Health, 14, 100389.Leung, T. L., & Koprivnikar, J. (2019). Your infections are what you eat: how host ecology shapes the helminth parasite communities of lizards. Journal of Animal Ecology, 88(3), 416-426.Li, J., Dong, H., Wang, R., Yu, F., Wu, Y., Chang, Y., ... & Zhang, L. (2017). An investigation of parasitic infections and review of molecular characterization of the intestinal protozoa in nonhuman primates in China from 2009 to 2015. International Journal for Parasitology: Parasites and Wildlife, 6(1), 8-15.Lima, L. B., Bellay, S., Giacomini, H. C., Isaac, A., & Lima-Junior, D. P. (2016). Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain. Parasitology, 143(3), 343-349.Lynch-Alfaro, J. W. (2007). Subgrouping patterns in a group of wild Cebus apella nigritus. International Journal of Primatology, 28, 271-289.Lynch-Alfaro, J. W. L., Silva Jr, J. D. S. E., & Rylands, A. B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74(4), 273-286.MacIntosh, A. J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M. A., & Hernandez, A. D. (2012). Monkeys in the middle: parasite transmission through the social network of a wild primate. PloS One, 7(12), e51144.Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness‐related benefits of dominance in primates. American Journal of Physical Anthropology, 147(4), 652-660.Manson, J. H., Rose, L. M., Perry, S., & Gros-Louis, J. (1999). Dynamics of female–female relationships in wild Cebus capucinus: data from two Costa Rican sites. International Journal of Primatology, 20, 679-706.Martínez-Mota, R., Kowalewski, M. M., & Gillespie, T. R. (2015). Ecological determinants of parasitism in howler monkeys: Howler monkeys: Adaptive radiation, Systematics, and Morphology, 259-285.Martínez‐Mota, R., Garber, P. A., Palme, R., & Gillespie, T. R. (2017). The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra). American Journal of Primatology, 79(8), e22669.McElroy, E. J., & De Buron, I. (2014). Host performance as a target of manipulation by parasites: a meta-analysis. The Journal of Parasitology, 100(4), 399-410.Meade, B. J. (1984). Host-parasite Dynamics Amoun Amboseli Baboons (Doctoral dissertation).Mendonça-Furtado, O., Edaes, M., Palme, R., Rodrigues, A., Siqueira, J., & Izar, P. (2014). Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behavioural Processes, 109, 79-88.Milotic, M., Lymbery, A., Thompson, A., Doherty, J. F., & Godfrey, S. (2020). Parasites are endangered by the conservation of their hosts: Meta-analyses of the effect of host captivity on the odds of parasite infection. Biological Conservation, 248, 108702.Milton, K. (1980). The Foraging Strategy of Howler Monkeys. New York: Columbia University Press.Milton, K., & May, M. L. (1976). Body weight, diet and home range area in primates. Nature, 259(5543), 459-462.Møller, A. P., Dufva, R. E. I. J. A., & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behavior, 22(65102), 60405-2.Montenegro, M. M. V. (2011). Ecologia de Cebus flavius (Schreber, 1774) em remanescentes de Mata Atlântica no estado da Paraíba. Doctoral dissertation, Universidade de São Paulo.Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.Morand, S., & Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology, 12, 717-727.Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., ... & Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology, 121(1), 65-73.Moreira, C. M., Peternelli dos Santos, L., de Sousa, M. B. C., & Izar, P. (2016). Variation in glucocorticoid levels: survival and reproductive demands in wild black capuchins (Sapajus nigritus). International Journal of Psychological Research, 9(2), 20-29.Mosdossy, K. N., Melin, A. D., & Fedigan, L. M. (2015). Quantifying seasonal fallback on invertebrates, pith, and bromeliad leaves by white‐faced capuchin monkeys (Cebus capucinus) in a tropical dry forest. American Journal of Physical Anthropology, 158(1), 67-77.Muehlenbein, M. P., & Watts, D. P. (2010). The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. BioPsychoSocial Medicine, 4, 1-12.Müller-Klein, N., Heistermann, M., Strube, C., Morbach, Z. M., Lilie, N., Franz, M., ... & Ostner, J. (2019). Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate. Behavioral Ecology, 30(2), 322-335.Munger, J. C., & Karasov, W. H. (1989). Sublethal parasites and host energy budgets: Tapeworm infection in white‐footed mice. Ecology, 70(4), 904-9.Murray, D. L., Cary, J. R., & Keith, L. B. (1997). Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology, 250-264.Myall, A., Price, J. R., Peach, R. L., Abbas, M., Mookerjee, S., Zhu, N., ... & Barahona, M. (2022). Prediction of hospital-onset COVID-19 infections using dynamic networks of patient contact: an international retrospective cohort study. The Lancet Digital Health, 4(8), e573-e583.Natoli, E., Say, L., Cafazzo, S., Bonanni, R., Schmid, M., & Pontier, D. (2005). Bold attitude makes male urban feral domestic cats more vulnerable to Feline Immunodeficiency Virus. Neuroscience & Biobehavioral Reviews, 29(1), 151-157.Newton-Fisher, N. E., Reynolds, V., & Plumptre, A. J. (2000). Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. International Journal of Primatology, 21(4), 613-628.Nunn CL, Craft ME, Gillespie TR et al (2015) The sociality–health–fitness nexus: synthesis, conclusions and future directions. Philosophical Transactions of the Royal Society B, 370(1669):20140115Nunn, C. L., & Altizer, S. M. (2005). The global mammal parasite database: an online resource for infectious disease records in wild primates. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 14(1), 1-2.Nunn, C. L., & Altizer, S. M. (2006). Infectious diseases in primates: behaviour. Ecology and evolution. Oxford University Press.Nunn, C. L., Altizer, S. M., Sechrest, W., & Cunningham, A. A. (2005). Latitudinal gradients of parasite species richness in primates. Diversity and Distributions, 11(3), 249-256.Nunn, C. L., Altizer, S., Jones, K. E., & Sechrest, W. (2003). Comparative tests of parasite species richness in primates. The American Naturalist, 162(5), 597-614.Nunn, C. L., Craft, M. E., Gillespie, T. R., Schaller, M., & Kappeler, P. M. (2015). The sociality–health–fitness nexus: synthesis, conclusions and future directions. Philosophical Transactions of the Royal Society B, 370(1669), 20140115.Nunn, C., & Altizer, S. (2006). Infectious diseases in primates: behavior, ecology and evolution. OUP Oxford.Parker, J. M., Goldenberg, S. Z., Letitiya, D., & Wittemyer, G. (2020). Strongylid infection varies with age, sex, movement and social factors in wild African elephants. Parasitology, 147(3), 348-359.Parkins, J. J., & Holmes, P. H. (1989). Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews, 2(1), 227-246.Parr, N. A., Fedigan, L. M., & Kutz, S. J. (2013). Predictors of parasitism in wild white-faced capuchins (Cebus capucinus). International Journal of Primatology, 34, 1137-1152.Parsons, M. B., Gillespie, T. R., Lonsdorf, E. V., Travis, D., Lipende, I., Gilagiza, B., ... & Vazquez-Prokopec, G. M. (2014). Global positioning system data-loggers: a tool to quantify fine-scale movement of domestic animals to evaluate potential for zoonotic transmission to an endangered wildlife population. PloS One, 9(11), e110984.Patrono, L. V., Pléh, K., Samuni, L., Ulrich, M., Röthemeier, C., Sachse, A., ... & Leendertz, F. H. (2020). Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nature Microbiology, 5(7), 955-965.Pedersen, A. B., & Fenton, A. (2015). The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31(5), 200-211.Pereira, M. E. (1993). Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In Lemur social systems and their ecological basis (pp. 205-221). Boston, MA: Springer US.Perry, S. (1996). Female‐female social relationships in wild white‐faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40(2), 167-182.Perry, S., Godoy, I., & Lammers, W. (2012). The Lomas Barbudal Monkey Project: two decades of research on Cebus capucinus. Long-term Field Studies of Primates, 141-163.Pierron, M., Sueur, C., Shimada, M., MacIntosh, A. J., & Romano, V. (2024). Epidemiological Consequences of Individual Centrality on Wild Chimpanzees. American Journal of Primatology, e23682.Pimm, S. L., Russell, G. J., Gittleman, J. L., & Brooks, T. M. (1995). The future of biodiversity. Science, 269(5222), 347-350.Poppi, D. P., Sykes, A. R., & Dynes, R. A. (1990). The effect of endoparasitism on host nutrition-the implications for nutrient manipulation. CABI Record Number: 19911433767Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs, 65(3), 283-302.Poulin, R. (2013). Explaining variability in parasite aggregation levels among host samples. Parasitology, 140(4), 541-546.Poulin, R., & Filion, A. (2021). Evolution of social behaviour in an infectious world: comparative analysis of social network structure versus parasite richness. Behavioral Ecology and Sociobiology, 75, 1-9.Poulin, R., & Morand, S. (2004). Parasite biodiversity. Smithsonian Institution.Preisser, W. (2019). Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents. Ecography, 42(7), 1315-1330.R Core Team (2023). R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna, Austria.Ramos-Fernández, G., Boyer, D., & Gómez, V. P. (2006). A complex social structure with fission–fusion properties can emerge from a simple foraging model. Behavioral ecology and sociobiology, 60, 536-549.Ramos-Fernández, G., Boyer, D., Aureli, F., & Vick, L. G. (2009). Association networks in spider monkeys (Ateles geoffroyi). Behavioral Ecology and Sociobiology, 63, 999-1013.Rimbach, R., Bisanzio, D., Galvis, N., Link, A., Di Fiore, A., & Gillespie, T. R. (2015). Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philosophical Transactions of the Royal Society B, 370(1669), 20140110.Roberts et al. (2002). Parasite community ecology and bio- diversity. Pages 63–82 In Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H., & Dobson, A. P. (Eds.). (2002). The Ecology of Wildlife diseases (Vol. 501). Oxford: Oxford University Press.Roberts, M. G. et al. (2002). Parasite community ecology and biodiversity. In: Hudson, P. J. et al. (eds), The ecology of wildlife diseases. Oxford Univ. Press, pp. 63-82.Romano, V., Duboscq, J., Sarabian, C., Thomas, E., Sueur, C., & MacIntosh, A. J. (2016). Modeling infection transmission in primate networks to predict centrality‐based risk. American Journal of Primatology, 78(7), 767-779.Romano, V., MacIntosh, A. J., & Sueur, C. (2020). Stemming the flow: information, infection, and social evolution. Trends in Ecology & Evolution, 35(10), 849-853.Romano, V., Shen, M., Pansanel, J., MacIntosh, A. J., & Sueur, C. (2018). Social transmission in networks: global efficiency peaks with intermediate levels of modularity. Behavioral Ecology and Sociobiology, 72, 1-10.Rondón, S., Ortiz, M., León, C., Galvis, N., Link, A., & González, C. (2017). Seasonality, richness and prevalence of intestinal parasites of three neotropical primates (Alouatta seniculus, Ateles hybridus and Cebus versicolor) in a fragmented forest in Colombia. International Journal for Parasitology: Parasites and Wildlife, 6(3), 202-208.Rozins, C., Silk, M. J., Croft, D. P., Delahay, R. J., Hodgson, D. J., McDonald, R. A., ... & Boots, M. (2018). Social structure contains epidemics and regulates individual roles in disease transmission in a group‐living mammal. Ecology and Evolution, 8(23), 12044-12055.Rushmore, J., Bisanzio, D., & Gillespie, T. R. (2017). Making new connections: insights from primate–parasite networks. Trends in Parasitology, 33(7), 547-560.Rushmore, J., Caillaud, D., Hall, R. J., Stumpf, R. M., Meyers, L. A., & Altizer, S. (2014). Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of the Royal Society Interface, 11(97), 20140349.Rushmore, J., Caillaud, D., Matamba, L., Stumpf, R. M., Borgatti, S. P., & Altizer, S. (2013). Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology, 82(5), 976-986.Rynkiewicz, E. C., Pedersen, A. B., & Fenton, A. (2015). An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in Parasitology, 31(5), 212-221.Sadoughi, B., Anzà, S., Defolie, C., Manin, V., Müller-Klein, N., Murillo, T., ... & Wu, D. (2022). Parasites in a social world: Lessons from primates. Animal Behavior and Parasitism, 35-52.Sah, P., Leu, S. T., Cross, P. C., Hudson, P. J., & Bansal, S. (2017). Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proceedings of the National Academy of Sciences, 114(16), 4165-4170.Salzer, J. S., Carroll, D. S., Williams-Newkirk, A. J., Lang, S., Peterhans, J. K., Rwego, I. B., ... & Gillespie, T. R. (2015). Effects of anthropogenic and demographic factors on patterns of parasitism in African small mammal communities. Parasitology, 142(3), 512-522.Sánchez, C. A., Becker, D. J., Teitelbaum, C. S., Barriga, P., Brown, L. M., Majewska, A. A., ... & Altizer, S. (2018). On the relationship between body condition and parasite infection in wildlife: a review and meta‐analysis. Ecology Letters, 21(12), 1869-1884.Sapolsky, R. (2006). Social cultures among nonhuman primates. Current Anthropology, 47(4), 641-656.Sapolsky, R. M. (2004). Social status and health in humans and other animals. Annual Revisions in Anthropology, 33(1), 393-418.Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308(5722), 648-652.Sargis, E. J. (2000). The functional morphology of the postcranium of Ptilocercus and Tupaiines (Scandentia, Tupaiidae): implications for the relationships of primates and other archontan mammals. City University of New York.Schino, G., & Aureli, F. (2008). Grooming reciprocation among female primates: a meta-analysis. Biology Letters, 4(1), 9-11.Setchell, J. M., & Dixson, A. F. (2001). Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormones and Behavior, 39(3), 177-184.Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior, 58(5), 720-728.Shedden, A., Dunn, J. C., Martínez-Mota, R., Cristóbal-Azkárate, J., Gillingham, P. K., MacSwiney-González, C., ... & Korstjens, A. H. (2022). Forest maturity has a stronger influence on the prevalence of spider monkeys than howler monkeys in an anthropogenically impacted rainforest landscape. Primates, 63(3), 283-291.Shimooka, Y. (2003). Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates, 44, 83-90.Silk, J. B. (2007). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1480), 539-559.Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., ... & Cheney, D. L. (2010). Female chacma baboons form strong, equitable, and enduring social bonds. Behavioral Ecology and Sociobiology, 64, 1733-1747.Silk, M. J., Croft, D. P., Delahay, R. J., Hodgson, D. J., Boots, M., Weber, N., & McDonald, R. A. (2017). Using social network measures in wildlife disease ecology, epidemiology, and management. BioScience, 67(3), 245-257.Simmen, B., Morino, L., Blanc, S., & Garcia, C. (2021). The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates. Scientific Reports, 11(1), 14196.Smith, J. M., & Szathmary, E. (1997). The major transitions in evolution. OUP Oxford.Smith, K. F., Acevedo‐Whitehouse, K., & Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation, 12(1), 1-12.Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523-559.Smyth, K. N., & Drea, C. M. (2016). Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females. Behavioral Ecology, 27(1), 148-157.Solórzano-García, B., & Pérez-Ponce de León, G. (2018). Parasites of neotropical primates: a review. International Journal of Primatology, 39, 155-182.Solórzano-García, B., White, J. M., & Shedden, A. (2023). Parasitism in heterogeneous landscapes: Association between conserved habitats and gastrointestinal parasites in populations of wild mammals. Acta Tropical, 237, 106751.Sosa, S., Puga-Gonzalez, I., Hu, F., Pansanel, J., Xie, X., & Sueur, C. (2020a). A multilevel statistical toolkit to study animal social networks: The Animal Network Toolkit Software (ANTs) R package. Scientific Reports, 10(1), 12507.Sosa, S., Sueur, C., & Puga-González, I. (2020b). Network measures in animal social network analysis: Their strengths, limits, interpretations and uses.Sosa, S., Sueur, C., & Puga-Gonzalez, I. (2021). Network measures in animal social network analysis: Their strengths, limits, interpretations and uses. Methods in Ecology and Evolution, 12 (1), 10–21.Stafford, B. J., & Szalay, F. S. (2000). Craniodental functional morphology and taxonomy of dermopterans. Journal of Mammalogy, 81(2), 360-385.Stevenson P.R, Quiñones, M. J., Ahumada, J. A. (2000). Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica, 32(3), 533-544.Stevenson, P. R. (2001). The relationship between fruit production and primate abundance in Neotropical communities. Biological Journal of the Linnean Society, 72(1), 161-178.Stevenson, P. R. (2004). Phenological patterns of woody vegetation at Tinigua Park, Colombia: methodological comparisons with emphasis on fruit production/Patrones fenológicos de vegetación leñosa en el Parque Tinigua, Colombia: comparaciones metodológicas con énfasis en la producción de frutos. Caldasia, 125-150.Stevenson, P. R., Aldana, A. M., Cárdenas, S., & Negret, P. J. (2018). Flooding and soil composition determine beta diversity of lowland forests in Northern South America. Biotropica, 50(4), 568-577.Stevenson, P. R., Quiñones, M. J., & Ahumada, J. A. (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. International Journal of Primatology, 19, 313-324.Sueur, C., King, A. J., Conradt, L., Kerth, G., Lusseau, D., Mettke‐Hofmann, C., ... & Aureli, F. (2011b). Collective decision‐making and fission–fusion dynamics: a conceptual framework. Oikos, 120(11), 1608-1617.Sueur, C., Petit, O., & Deneubourg, J. L. (2010). Short-term group fission processes in macaques: a social networking approach. Journal of Experimental Biology, 213(8), 1338-1346.Sueur, C., Petit, O., De Marco, A., Jacobs, A. T., Watanabe, K., & Thierry, B. (2011). A comparative network analysis of social style in macaques. Animal Behaviour, 82(4), 845-852.Sumner, K. M., McCabe, C. M., & Nunn, C. L. (2018). Network size, structure, and pathogen transmission: a simulation study comparing different community detection algorithms. Behaviour, 155(7-9), 639-670.Sykes, A. R. (1994). Parasitism and production in farm animals. Animal Science, 59(2), 155-172.Symington, M. M. (1988). Demography, ranging patterns, and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru. American Journal of Primatology, 15(1), 45-67.Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47-61.Teichroeb, J. A., Kutz, S. J., Parkar, U., Thompson, R. A., & Sicotte, P. (2009). Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng‐Fiema, Ghana: Possible anthropozoonotic transmission. American Journal of Physical Anthropology, 140(3), 498-507.Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton: Princeton Univ. Press.Terborgh, J. (1986). Keystone plant resources in the tropical forests. In M. E. Soule (Ed.). Conservation Biology: The Science of Scarcity and Diversity (pp. 330-344), Sunderland, MA: Sinauer.Tibbetts, E. A., Pardo-Sanchez, J., & Weise, C. (2022). The establishment and maintenance of dominance hierarchies. Philosophical Transactions of the Royal Society B, 377(1845), 20200450.Tiddi, B., Aureli, F., & Schino, G. (2012). Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate. PloS One, 7(5), e36641.Townsend, A. K., Hawley, D. M., Stephenson, J. F., & Williams, K. E. (2020). Emerging infectious disease and the challenges of social distancing in human and non-human animals. Proceedings of the Royal Society B, 287(1932), 20201039.Tutin, C. E., Ham, R. M., White, L. J., & Harrison, M. J. (1997). The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42(1), 1-24.Ungerfeld, R., & Correa, O. (2007). Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs. Applied Animal Behaviour Science, 105(1-3), 249-253.Van Schaik, C. P. (1983). Why are diurnal primates living in groups?. Behaviour, 120-144.Vitone, N. D., Altizer, S., & Nunn, C. L. (2004). Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research, 6(2), 183-199.Vogel, E. R., & Janson, C. H. (2007). Predicting the frequency of food‐related agonism in white‐faced capuchin monkeys (Cebus capucinus), using a novel focal‐tree method. American Journal of Primatology, 69(5), 533-550.Vogel, E. R., Munch, S. B., & Janson, C. H. (2007). Understanding escalated aggression over food resources in white-faced capuchin monkeys. Animal Behaviour, 74(1), 71-80.White, L. A., Forester, J. D., & Craft, M. E. (2017). Using contact networks to explore mechanisms of parasite transmission in wildlife. Biological Reviews, 92(1), 389-409.Whitten, P. L. (1983). Diet and dominance among female vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 5(2), 139-159.Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 262-300.Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949-970.Wren, B., Ray, I. S., Remis, M., Gillespie, T. R., & Camp, J. (2021). Social contact behaviors are associated with infection status for Trichuris sp. in wild vervet monkeys (Chlorocebus pygerythrus). Plos One, 16(4), e0240872.Zhao, Q. K. (1994). Seasonal changes in body weight of Macaca thibetana at Mt. Emei, China. American Journal of Primatology, 32(3), 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