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Title:The effects of habitat disturbance, host traits, and host physiology on patterns of gastrointestinal parasite infection in black howler monkeys (Alouatta pigra)
Author(s):Martinez Mota, Rodolfo
Director of Research:Garber, Paul A.
Doctoral Committee Chair(s):Garber, Paul A.
Doctoral Committee Member(s):Ambrose, Stanley H.; Stumpf, Rebecca M.; Gillespie, Thomas R.
Department / Program:Anthropology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):Howler monkeys
Abstract:Anthropogenic forest disturbance associated with the conversion of forest into monocultures for agricultural production or cattle ranching, and the increased human presence linked to wood extraction and selective logging, can alter host-parasite dynamics and increase the risk of infectious diseases in wild primates. However, little is known regarding the proximate ecological factors that drive this relationship, and whether such effects are maintained over time affecting primate population viability and health. In this dissertation, I examined the impact of anthropogenic forest disturbance on the health of endangered black howler monkeys (Alouatta pigra), using a multifactorial model that integrated information on parasitic infection patterns, stress hormones, host characteristics, and ecological conditions. Specifically, I explored 1) whether rates of gastrointestinal parasite infection were higher in black howlers inhabiting forest fragments characterized by increased levels of anthropogenic disturbance, and 2) whether rates of parasitism were directly affected by changes in howler age, reproductive condition, and stress hormones. Over the course of a year (February 2011 to February 2012), I studied seven black howler groups living in five fragments of tropical deciduous forest that varied in their degree of anthropogenic disturbance at Escárcega, State of Campeche, Mexico (18°16’N, 90°43’W). I monitored 44 individually recognized howlers, including 15 adult males, 15 adult females, and 14 immature howlers. From these individuals, I collected non-invasively 673 fecal samples that were used for parasitological and glucocorticoid (i.e., stress hormones) analyses. In each fragment, I assessed variation in ecological disturbance through measures of fragment size and fragment shape, and through estimations of wood extraction (stump-to-tree ratio), percentage of canopy closure, and tree biomass. Rainfall data also were recorded. In this dissertation, I found that black howler monkeys at Escárcega, Mexico were host to seven parasite taxa, including Trypanoxyuris minutus (Oxyuridae), Parabronema sp. (Habronematidae), an unidentified strongyle nematode (Strongylidae), Controrchis biliophilus (Dicrocoeliidae), an unidentified trematode (Dicrocoeliidae), Entamoeba coli, and Entamoeba sp. (Entamoebidae). The most influential factors on parasite prevalence and parasite species richness were howler age and monthly precipitation. Parasite prevalence and parasite species richness increased with howler age. Adult howlers had higher helminth prevalence (mean prevalence ± SD= 69.8 ± 13.7%) compared to older (> 6 months of age; mean prevalence ± SD= 43.9 ± 20.5%) and younger juveniles (<6 months of age; prevalence ± SD= 28.1 ± 27.2%). Similarly, parasite species richness was 1.8 - 2.7-fold higher in adults than in older and younger juveniles. Increased parasitic infection in adults may be related to the fact that older individuals have been exposed to infective stages of different parasite species over prolonged periods of time compared to immature howlers. Seasonal rainfall had mixed effects depending on the parasite type: while protozoan prevalence significantly increased with rainfall, helminth prevalence decreased. Measures of forest disturbance including fragment size (ranging from 2 - 9 ha to 2100 ha) and shape (ranging from more regular to more irregular forms [2.3 to 4.7]), perimeter-to-area ratio (ranging from 0.001 to 0.061), logging rates (stump-tree ratio ranging from 0.008 to 0.11), tree density (ranging from 600 to 1000 trees/ha), canopy cover (ranging from 70% to 95%), and howler density (ranging from 12 to 300 ind/km2) had minimal effects on patterns of intestinal parasitic infection. Similarly, howler group size (ranging from 4 to 13 individuals), female reproductive condition (e.g., non-pregnant, pregnant, and lactating), and stress levels (measured through glucocorticoid hormones ranging from 400 to 2100 ng/g) did not have significant effects on parasite prevalence and parasite species richness. This dissertation moves beyond the traditional perspective that fragmented habitats are uniformly detrimental to howler monkey health and survivorship to a model of howler monkey adaptability, in which howlers are able to successfully survive and reproduce in disturbed habitats due to a species-specific adaptive pattern in behavior (e.g., a similar activity budget across howler populations), demography (e.g., social groups characterized by small size and minimal changes in composition), and physiology (e.g., low stress levels, limited multiple parasitic infections). Overall, this perspective represents a critical step in assessing ecosystem health and disease risk faced by black howler monkeys and other primates living in disturbed environments.
Issue Date:2015-04-22
Rights Information:Copyright 2015 Rodolfo Martinez-Mota
Date Available in IDEALS:2015-07-22
Date Deposited:May 2015

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