Seasonal Effects on Great Ape Health: A Case Study of Wild Chimpanzees and Western Gorillas

<div><p>Among factors affecting animal health, environmental influences may directly or indirectly impact host nutritional condition, fecundity, and their degree of parasitism. Our closest relatives, the great apes, are all endangered and particularly sensitive to infectious diseases. Both chimpanzees and western gorillas experience large seasonal variations in fruit availability but only western gorillas accordingly show large changes in their degree of frugivory. The aim of this study is to investigate and compare factors affecting health (through records of clinical signs, urine, and faecal samples) of habituated wild ape populations: a community (N = 46 individuals) of chimpanzees (<em>Pan troglodytes</em>) in Kanyawara, Kibale National Park (Uganda), and a western gorilla (<em>G. gorilla</em>) group (N = 13) in Bai Hokou in the Dzanga-Ndoki National Park (Central African Republic). Ape health monitoring was carried out in the wet and dry seasons (chimpanzees: July–December 2006; gorillas: April–July 2008 and December 2008–February 2009). Compared to chimpanzees, western gorillas were shown to have marginally greater parasite diversity, higher prevalence and intensity of both parasite and urine infections, and lower occurrence of diarrhea and wounds. Parasite infections (prevalence and load), but not abnormal urine parameters, were significantly higher during the dry season of the study period for western gorillas, who thus appeared more affected by the large temporal changes in the environment in comparison to chimpanzees. Infant gorillas were the most susceptible among all the age/sex classes (of both apes) having much more intense infections and urine blood concentrations, again during the dry season. Long term studies are needed to confirm the influence of seasonal factors on health and parasitism of these great apes. However, this study suggest climate change and forest fragmentation leading to potentially larger seasonal fluctuations of the environment may affect patterns of ape parasitism and further exacerbate health impacts on great ape populations that live in highly seasonal habitats.</p> </div

Summary of general body conditions and clinical signs.

<p>Percentage of days with at least one individual with each symptom for chimpanzees (N = 132 days) and gorillas (N = 188 days). <i>Wounds</i> consisted of bites or cuts caused by falls from trees, intra and inter (only for gorillas, but caused by vegetation) group aggressive interactions. <i>Skin lesions</i> consisted in itchy white spots (sometimes with little crusts) on body and face of all group members, possibly produced by either a fungus or ringworms. <i>Worms in faeces</i>, in chimpanzees two <i>Bertiella</i> sp segments associated with whole leaves of <i>Aneilema aecquinoctiale</i>. <i>Diarrhoea</i>, in gorillas 2 cases caused by stress related during inter-group interactions, one severe case from a 2 year-old infant lasting two days, mild diarrhoea during dry season (N = 9). Asterisks indicate a different sample size for chimpanzees: *N = 127, ** N = 125.</p

Comparative summary of average concentration and statistics for selected urine variables for chimpanzees and western gorillas.

<p>In parenthesis the range of maximum and minimum values recorded. Columns named “Anova” show ANOVA's results of the three different factors tested: species, season and age/sex class. See text for details on statistical method.</p

Average strongyle load across populations and age/sex classes.

<p>Vertical bars denote 0.95 confidence intervals.</p

Seasonal subdivision of the study period and biological sample sizes.

<p>In parenthesis: minimum and maximum values.</p

Summary of coproscopy (a–b) and macroscopic results (c) for both chimpanzees and western gorillas.

*<p>Feces either from a adult female or male, or a subadult of the Makumba group</p><p>Given the uncertainty of juvenile and infant sex in gorillas, only the average value for all individuals per each of these two classes is provided for western gorillas. Strongyl large eggs: (50×90 µ) on average, more round and fringes than the small strongyl eggs (40×80 µ) and <i>Strongyloides fullebornii</i>.</p

Averages per time period of strongyle load (a) in chimpanzees and (b) in western gorillas.

<p>The grey area distinguishes the months of dry season in comparison to months of wet season.</p

Immunization reduces adult worm burden, but does not affect their development.

<p>Mice were immunized three times s.c. with 100,000 Mf in alum. Control mice received alum alone. <i>L. sigmodontis</i> challenge infection was performed one week after the last immunization. Numbers of worms on days 15 (A), 56 (B), 70 (C) and 90 (D) p.i. (additional experiments see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s005" target="_blank">Figure S5A</a>–C), gender balance (E) (individual experiments see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s005" target="_blank">Figure S5D</a>, E), as well as length of males (F) and females (G) at day 90 p.i. (10/90 percentile, outliers are indicated, individual experiments see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s005" target="_blank">Figure S5F</a>–I) were analyzed with Student's t-test (** <i>P</i><0.01, *** <i>P</i><0.001).</p

Mice immunized with Mf in alum have reduced numbers of Mf.

<p>Mice were immunized three times s.c. with 100,000 Mf in alum. Control mice received alum alone. <i>L. sigmodontis</i> infection was performed one week after the last immunization. Microfilaraemia was monitored twice a week throughout patency. (A) Kinetics of Mf load of sham-treated (dashed line) and immunized (black line) mice in the peripheral blood. One representative of three independent experiments with ten mice per group is shown (2-way ANOVA, mean ± SEM), including both Mf⁻ and Mf⁺ mice. For additional experiments see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s003" target="_blank">figure S3A</a>, B. (B) Percentage of Mf⁺ mice of three independent experiments was analyzed using Student's t-test. Each mouse with peripheral Mf at any given time point was defined as Mf⁺. (C, D) Mf burden in the pleural space days 70 (C) and 90 (D) p.i.. Graphs show one representative of three (C) and two (D) independent experiments (at least seven mice each group, see also <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s003" target="_blank">Figure S3C</a>–E) and were analyzed with Welch-corrected t-test. Numbers below the symbols indicate the number of Mf⁺ mice (median, * <i>P</i><0.05, ** <i>P</i><0.005).</p

Immunization inhibits embryogenesis in female worms.

<p>Mice were immunized three times s.c. with 100,000 Mf in alum. Control mice received alum alone. <i>L. sigmodontis</i> challenge infection was performed one week after the last immunization. Seventy days after infection female worms were analyzed for their embryonic stages. Representative pictures of oocyte (A; micron bar 10 µm), divided egg (B; 10 µm), pretzel stage (C; 15 µm) and stretched Mf (D; 30 µm) are shown. (E) Embryogram illustrating the composition of embryonic stages in female worms. If present, three female worms of each mouse were investigated (27 females in the control group, 28 females from the immunized group, additional experiments see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001558#pntd.0001558.s004" target="_blank">Figure S4</a>). Statistical analysis was performed with Mann-Whitney U-test (mean ± SEM, ** <i>P</i><0.01, *** <i>P</i><0.001).</p