key: cord-102891-0z397ppn authors: Wren, Brandi; Ray, Ian S.; Remis, Melissa; Gillespie, Thomas R.; Camp, Joseph title: Social contact behaviors are associated with infection status for whipworm (Trichuris sp.) in wild vervet monkeys (Chlorocebus pygerythrus) date: 2020-10-07 journal: bioRxiv DOI: 10.1101/2020.10.07.329409 sha: doc_id: 102891 cord_uid: 0z397ppn Social grooming in the animal kingdom is common and serves several functions, from removing ectoparasites to maintaining social bonds between conspecifics. We examined whether time spent grooming with others in a highly social mammal species was associated with infection status for gastrointestinal parasites. Of six parasites detected, one (Trichuris sp.) was associated with social grooming behaviors, but more specifically with direct physical contact with others. Individuals infected with Trichuris sp. spent significantly less time grooming conspecifics than those not infected, and time in direct contact with others was the major predictor of infection status. One model correctly predicted infection status for Trichuris sp. with a reliability of 95.17% overall when the variables used were time spent in direct contact and time spent grooming others. This decrease in time spent grooming and interacting with others is likely a sickness behavior displayed by individuals with less energy or motivation for non-essential behaviors. This study highlights the need for an understanding of a study population’s parasitic infections when attempting to interpret animal behavior. We chose Chlorocebus pygerythrus as the study species because individuals 171 exhibit variation in grooming behaviors [56] , allowing us to examine differences in the 172 relationship between social behaviors and parasite infection status. Groups of Ch. 173 pygerythrus in LDNR -and much of the surrounding region -typically vary in size from 174 13-25 individuals [54, 55, 57] . Six groups of Ch. pygerythrus at LDNR are habituated, and 175 researchers have been conducting studies of these groups semi-regularly for more than a 176 decade [58-61]. We collected data from three of the six habituated groups at LDNR: 177 Blesbok group, Donga group, and Bay group. At the commencement of the study there 178 were 14 individuals in the Blesbok group, 16 in the Donga group, and 17 in the Bay 179 group; the total study population fluctuated due to births, migrations, and deaths, and was 180 54 at the conclusion of the study. Here we present data on a total of 55 subjects as well as 181 a subset of 38 of those study subjects. Information on group composition for each social 182 group can be found in Wren [55] and Wren et al. [36, 62] . We located groups using 183 known sleeping sites and home ranges. Data were recorded for only the Blesbok group 184 from July -October 2009 because other researchers were studying the Donga and Bay 185 groups during that time. Data were collected from all three social groups for the 186 Social group differences are presented in Table 3 . These differences are likely due 302 to the different sampling efforts for each social group as noted in the methods section. (Table 3) . However, because ANOVA is robust with respect 326 to violations of homogeneity of variance analyses could still be performed. There were 327 statistically significant differences among groups for: total seconds observed (F (2, 52) = 328 22.79, p < 0.001); number of grooming partners (F (2, 52) = 15.70, p < 0.001); number of 329 grooming partners giving (F (2, 52) = 8.11, p = 0.001); number of total partners (F (2, 52) = 330 19.08, p < 0.001); time self-grooming (F (2, 52) = 3.54, p = 0.036) ( Table 4) . Planned contrasts revealed specific differences among groups and combinations 343 of groups (Tables 5 & 6 ). There were statistically significant differences for all monkeys were lost from sight, but we kept data from all follows longer than 5 min. We 193 used continuous recording for all behavioral data We recorded data on the following variables for all bouts of social grooming: start 195 and stop times, whether grooming was given or received, and identity of grooming or more, the direction of grooming switched (i.e., the individual being groomed 199 began grooming its partner or vice versa) We also recorded data on start and stop times for direct physical contact with another 201 individual and identification of direct social contact partners We collected 332 fecal samples non-invasively from identified individuals 204 directly following defecation, and samples were immediately preserved in a 10% 205 buffered formalin solution. We recorded data on the following variables for We used three methods to detect parasite eggs and cysts in samples in order to 210 reduce the risk of false negatives: fecal flotation, fecal sedimentation, and 211 immunofluorescence microscopy. We isolated helminth eggs and protozoan cysts and 212 oocysts from fecal material using fecal flotation with double centrifugation (at 1800 rpm 213 for 10 min) in NaNO 3 solution and fecal sedimentation with dilute soapy water We 406 equation, based on a higher -2 Log likelihood (37.68) and lower Nagelkerke Trichuris sp. and 86.11% of observed presence of Trichuris sp Infected individuals at LDNR spent 415 an average of 4% of their observed time grooming others, while those not infected with 416 this parasite spent an average of 14% of their observed time grooming others. However, 417 no differences existed in time spent being groomed by others. Overall, for the entire 418 sample (n = 55), study subjects spent about 20% of their time in direct contact with 419 another individual. The subset used for parasitological analysis spent 6.5% (n = 38) of 420 their time in direct contact with another individual. This large difference is primarily 421 influenced by the inclusion of infants and mothers with infants in the entire sample of n = 422 55, but only mothers in the smaller subset of n = 38. These mother-infant dyads remain in 423 almost constant contact for the first weeks of a monkey's life and this inflates the overall 424 mean for the group. Because there were not enough fecal samples from these infants, 425 their behavioral data was not included in hypothesis testing These results do not support the hypothesis that social grooming facilitates 429 transmission of this type of gastrointestinal parasite. One possible explanation for these 430 results is that individuals that are infected with Trichuris sp. experience degraded health 431 and/or less motivation to groom others and interact with others. Red colobus monkeys 432 (Procolobus rufomitratus) in Uganda that were infected with Trichuris sp. decreased their 433 time spent performing a number of behaviors Those 434 same individuals spent more time resting as well as ingesting plant species and/or parts 435 that suggest self-medicative behavior. Whipworm is known to cause anemia, chronic 436 dysentery, rectal prolapse, and poor growth in humans with symptomatic infections [68], 437 so less energy, motivation, or interest for behaviors like social grooming should not be 438 surprising in other species Another possible explanation is that Trichuris sp. more directly alters host 440 behavior in vervet monkeys. Gastrointestinal parasites are known to alter host behavior in 441 some host-parasite relationships, an idea referred to as the manipulation hypothesis For example, Toxoplasma gondii causes intermediate rodent hosts to be more 443 attracted to the scent of felid predators Dicrocoelium dendriticum causes infected ants to wait on the tips of blades of grass 445 where they can be ingested by sheep, the parasite's definitive host. Because manipulation host to a definitive host, and vervet monkeys do not serve as intermediate 448 hosts for Trichuris sp Other studies have found multiple morphotypes of Trichuris sp. in nonhuman 451 primate hosts in captivity in Nigeria [74,75], suggesting that potentially multiple species 452 of Trichuris sp. may infect nonhuman primates. The major implication of this has been 453 seen as relevant for public health because it may mean that the species of Trichuris sp 76] noted that ill or infected animals display altered behavior, and argued 459 that these sickness behaviors can be adaptive. One study of chimpanzees (Pan 460 troglodytes schweinfurthii) revealed that infected individuals exhibit altered behavior, 461 most fittingly described as lethargy The Ghai et al. [67] study that revealed that Trichuris sp. 464 was associated with a reduction in grooming and mating and also found that individuals 465 infected with this parasite took longer to switch behaviors than those individuals that 466 were not infected This study suggests that the gastrointestinal parasite Trichuris sp. is associated 469 with behavioral differences, specifically decreased time spent grooming others and time 470 spent in direct contact with others, in vervet monkey hosts. These behavioral differences 471 are extreme enough to influence group means when assessing behavior. Further, if an 472 individual is less likely to groom or interact with conspecifics, then they may also 473 experience lower social status and thus lower reproductive fitness We would like to thank the Mpumalanga Parks and Tourism Agency We are also grateful 481 to Katie Dean, Claire Detrich, Ruby Malzoni, Liz Sperling Moses for assistance in the laboratory Grooming systems of insects: structure, mechanics Pollen transport and deposition by bumble bees in Erythronium: 489 influences of floral nectar and bee grooming Grooming patterns in the primitively eusocial wasp 491 Polistes dominulus A video-tracking method to identify and understand circadian patterns in 493 Drosophila grooming Hoxb8 is required for normal grooming behaviour in 496 mice Self-grooming by rodents in social and sexual 498 contexts Costs and 500 constraints of anti-parasitic grooming in adult and juvenile 501 rodents Neurobiology of rodent self-grooming and its value for translational 504 neuroscience Relationship of bill morphology to grooming 506 behaviour in birds Comparative analysis of time spent grooming by 508 birds in relation to parasite load Of great tits and fleas: sleep baby 510 sleep Do grooming behaviours affect 512 visual properties of feathers in male domestic canaries, Serinus 513 canaria? Grooming in primates: implications for its utilitarian 517 function The distribution of grooming and related behaviours among 519 adult female vervet monkeys Intragroup cohesion and intergroup hostility: the relation between 521 grooming distributions and intergroup competition among female 522 primates Grooming down the 524 hierarchy: allogrooming in captive brown capuchin monkeys The development of grooming and its expression in adult 527 animals Elimination of external parasites (lice) is the primary 529 function of grooming in free-ranging Japanese macaques Insects groom their antennae to enhance olfactory acuity Grooming behaviour as a 535 mechanism of insect disease defense Beta-endorphin concentrations in 537 cerebrospinal fluid of monkeys are influenced by grooming relationships Seyfarth RM. A model of social grooming among adult female monkeys Functional significance of social grooming in primates Silk JB. Social components of fitness in primate groups Grooming reciprocation among female primates: a meta-550 analysis Infection strategies of 552 retroviruses and social grouping of domestic cats Gorilla susceptibility to Ebola virus: the cost of sociality Dynamics of a multihost 558 pathogen in a carnivore community Integrating contact network 560 structure into tuberculosis epidemiology in meerkats in South Africa: 561 implications for control Social network analysis of wild chimpanzees provides insights for predicting 564 infectious disease risk Making connections: insights from 566 primate-parasite networks Number of Grooming Partners 570 Is Associated with Hookworm Infection in Wild Vervet Monkeys 571 (Chlorocebus pygerythrus) Social bonds between unrelated 577 females increase reproductive success in feral horses Social bonds of female baboons enhance 580 infant survival Fitness increases 582 with partner and neighbour allopreening Heart rate responses to social interactions in 586 free-moving rhesus macaques (Macaca mulatta): a pilot study Grooming in Barbary 589 macaques: better to give than to receive? The social 594 transmission of disease between adult male and female reproductives of the 595 dampwood termite Zootermopsis angusticollis Infectious diseases in primates: behavior, 598 ecology and evolution Primate parasite ecology: the dynamics and 600 study of host-parasite relationships No effects of a feather mite on 602 body condition, survivorship, or grooming behaviour in the Seychelles 603 warbler, Acrocephalus sechellensis Emerging 607 infectious disease and the challenges of social distancing in human and non-608 human animals Who infects whom? Social networks and tuberculosis transmission 611 in wild meerkats Social transfer of pathogenic fungus promotes 614 active immunisation in ant colonies A vegetation classification and management plan for the A floristic description and 619 utilisation of two home ranges by vervet monkeys in Loskop Dam Nature 620 Wren BT. Behavioural ecology of primate-parasite interactions Social and ecological influences on activity budgets of 624 vervet monkeys, and their implications for group living When females trade 627 grooming for grooming: testing partner control and partner choice models of 628 cooperation in two primate species 632 59. van de Waal E, Renevey N, Favre CM, Bshary R. Selective attention to 633 philopatric models causes directed social learning in wild vervet monkeys Pansini R. Induced cooperation to access a shareable reward increases the 636 hierarchical segregation of wild vervet monkeys Helminths of Vervet Monkeys Chlorocebus aethiops, from Loskop Dam Nature Reserve Measuring behaviour: an introductory guide Noninvasive assessment of gastrointestinal parasite infections in 646 free-ranging primates A legacy of low-impact logging does not elevate 649 prevalence of potentially pathogenic protozoa in free-ranging gorillas and 650 chimpanzees in the Republic of Congo: logging and parasitism in African 651 apes Sickness 655 behaviour associated with non-lethal infections in wild primates The public health significance of 658 Trichuris trichiura Modification of intermediate host behaviour by 660 parasites Host specificity Parasites and the behaviour of animals Parasite manipulation of host behaviour: an update and frequently 666 asked questions The effect of Toxoplasma gondii on animal behaviour: playing 668 cat and mouse Prevalence and 670 morphotype diversity of Trichuris species and other soil-transmitted helminths 671 in captive non-human primates in northern Nigeria Gastrointestinal helminths of resident wildlife at the Federal 675 University of Agriculture Zoological Park Biological basis of the behaviour of sick animals Wrangham 680 RW. Noninvasive monitoring of the health of Pan troglodytes schweinfurthii 681 in the Kibale National Park, Uganda