Effects Of Habitat Overlap On Helminth Transmission Between Sympatric Baboons, Vervet Monkeys And Ungulates In Amboseli Ecosystem, Kenya
Abstract
In natural ecosystems, helminths and their diverse hosts co-exist as interacting ecological
communities, however the factors that determine which helminths (s) infect which host
(s) are not well understood. Habitat overlap is predicted to influence helminth
transmission and infection patterns, including helminths co-occurrence across sympatric
host taxa. The overall objective of this study was to determine the effects of habitat
overlap between sympatric hosts on transmission of helminths in Amboseli ecosystem,
Kenya. The focal animal was the baboon population, which has been the subject of
studies for decades by the Amboseli Baboon Research Project, while the sympatric
animals included Vervet monkeys, cattle, sheep, goats (domestic ungulates) and
wildebeests, impala, Grant’s gazelles and Thomson’s gazelles (wild ungulates). The
Amboseli baboon population is structured in to six social groups, which are well known
in terms of their ranges and numbers.
The first specific objective of this study was to determine the degree of habitat overlap
among the social groups of baboons and between baboons and the other sympatric host
species. Key individuals of a baboon social group were tracked daily for 7days and
(Global positioning system) GPS coordinates of their point locations uploaded in
BIOTAS software to generate home ranges by Minimum Convex Polygons (MCP)
method. The home range map, size (km2) and degree of overlap between baboon groups
were calculated using the software. The degree of overlap between baboon groups and
other sympatric hosts was determined through frequency sightings of the sympatric hosts
and their dung pile counts in the home range of each baboon group. Results revealed that
the home ranges of each baboon group at 100% MCP overlapped with the ranges of at
least four other baboon groups, while home ranges at 50% MCP overlapped with at least
one other baboon group home range. Degree of habitat overlap between baboon and
sympatric hosts based on mean dung pile counts (94.2) was higher at 100% MCP
compared to degree of overlap (25.6) at 50% MCP of baboon habitat. In addition the
degree of habitat overlap between baboon and sympatric hosts based on mean frequency
sightings was higher (8.8) at 100% MCP compared to degree of overlap (4.5) at 50%
MCP of baboon habitat. These results indicated that the degree of overlap across baboon
home ranges and between baboon and sympatric hosts varied according to the proportion
of habitat used by baboons.
The second objective was to determine helminth prevalence, abundance and species
richness in all the nine sympatric hosts. Sedimentation and floatation techniques were
used to assess 1138 formalin-fixed faecal samples collected in the dry and wet season. A
total of 16 types of helminth eggs were identified by both sedimentation and floatation
fecal assessment methods. Out of these, eight were nematodes, which included
Strongylids, Enterobius sp., Strongyloides spp., Primasubulura sp., Trichuris spp.,
Streptopharagus sp., unidentified species of Spirurina, and unidentified species of
Spirurids. The cestodes included Moniezia expansa and Moniezia benedini. Trematodes
included Paramphistomum sp., Fasciola gigantica and Fasciola hepatica. Differences in
helminth prevalence were recorded across all host species (χ2 = 200.37, df = 8, p =
0.0001) and between seasons (χ2 = 23.87, df = 1, p = 0.0001), using the sedimentation
method. Moreover, prevalence of helminths significantly differed across baboon social
groups (χ2 = 22.43, df = 5, p = 0.0001) as well as between seasons with higher prevalence
in the dry (χ2 = 13.56, df = 1, p = 0.019) compared to the wet season (χ2 = 18.26, df = 1, p
= 0.003). The floatation method also revealed differences in prevalence of helminths
across host taxa (χ2 = 54.505, df = 8, p<0.0001). Prevalence of helminths across baboon
groups differed significantly (χ2 = 27.754, df = 5, p<0.0001) but not between seasons (χ2
= 1.680, df = 1, p = 0.195). Helminth prevalence obtained by floatation method across all
the nine sympatric host species was significantly higher (χ2 = 157.472, df = 1, p<0.001)
than when determined by sedimentation method. In contrast, helminth species richness
was significantly higher when determined by sedimentation method (χ2 = 132.703, df = 5,
p<0.001) than when floatation method was used. Concordance between floatation and
sedimentation methods was low (0.101) according to Cohens’ kappa statistic. It was
found that mean abundance of helminths varied across host taxa and across baboon social
groups. Helminth species richness across the host species community ranged from two to
eight, with mean species richness of 5.1 ± 1.9. These results indicate that in a sympatric
host community, prevalence, abundance and species richness of helminths was highly
variable across host taxa. Similar infection patterns were observed between social groups
irrespective of their very close proximity of spatial overlap. Seasonality strongly
influenced patterns of helminth infection within and across host species. It is likely that
the factors that determine intergroup variation in helminth infection are multiple and
includes the demographic structures of social groups such as age and sex and habitat
heterogeneities.
The third objective was to test the influence of habitat overlap among baboon groups and
between baboons and sympatric host species in determining helminth infection patterns.
Since the degree of home range overlap between baboon home ranges did not vary at
100% MCP, only values at 50% MCP were tested to determine influence of degree of
habitat overlap on helminth prevalence, abundance and species richness. Further, dung
pile count and frequency of sighting alternative hosts in baboon home ranges were used
as indices of degree of overlap. Specifically, relationships were tested between dung pile
counts, mean frequency of animal sightings, Shannon-Wiener diversity index, host
species diversity and both helminths prevalence and abundance in baboons. The results
indicated a lack of statistical association between degree of habitat overlap across baboon
groups and their helminths prevalence, abundance and species richness (p > 0.05). These
findings indicate that the degree of habitat overlap between social groups does not
influence helminths prevalence, abundance and species richness.
Statistical analysis showed that at 50% MCP of baboon home ranges, the degree of
overlap (based on dung pile counts) between baboon and sympatric hosts did not
significantly influence mean helminth prevalence (r2 = 0.441, t = -1.777, p = 0.150) and
mean helminth abundance (r2 = 0.222, t = -1.068, p = 0.3458). Results also indicated that
the degree of habitat overlap between baboon and sympatric hosts indicated by ShannonWiener diversity index, host diversity and mean frequency of sightings, did not
statistically influence helminth prevalence and abundance. However, host diversity (r2 =
0.665, F(1,4) = 7.594, p = 0.05) and Shannon-Wiener diversity index (r2 = 0.727, F(1,4) =
10.64, p = 0.031) significantly influenced helminths species richness in baboon groups.
Both indices showed that the degree of habitat overlap between baboons and other
sympatric host species did not significantly influence helminths prevalence and
abundance in baboons. However, increased habitat overlap with more diverse
communities of sympatric hosts showed a declining trend in helminths species richness in
baboons.
The fourth objective was to genetically determine the species of nematodes shared among
sympatric baboons, vervet monkeys and ungulates in Amboseli ecosystem. A total of 977
DNA samples were extracted from larvae cultured from faecal material collected from all
the sympatric hosts during the dry and wet seasons. The DNA was amplified by both
mitochondrial and internal transcribed spacers of ribosomal genes followed by
sequencing. A total of 67 sequences were used for identification of the nematodes and
phylogenetic reconstruction. Strongyloides stercoralis, Strongyloides fuelleborni,
Trichostrongylus colubriformis, and Oesophagostomum bifurcum were identified from
baboons. Cooperia oncophora was identified from cattle, Haemonchus contortus from
goats and Teladosargia circumcincta from Grant’s gazelles. In addition, a nematode that
displayed viviparity and identified to be a member of the sub-family Cyathostominae was
shared in the six sympatric hosts; baboons, vervet monkeys, Thomson’s gazelle, impalas,
goats and cattle. Results indicated that habitat overlap facilitated Cyathostominae sharing
across hosts, irrespective of their evolutionary relatedness, which may imply a host shift.
Specifically, it was most likely that the viviparous nematode underwent a shift to
colonize a new host range that includes unusual hosts for members of the sub-family
Cyathostominae. Phylogenetic analysis of Strongyloides fuelleborni demonstrated
geographical structuring rather than host structuring; specifically, the species in Kenya
were genetically distinct from those previously found in Tanzania, Gabon and Japan. In
addition, phylogenetic analysis revealed two genetic populations of S. stercoralis in
baboons, which had different evolutionary trajectories. The baboon population harboured
helminth species of zoonotic potential (S. fuelleborni, S. stercoralis, O. bifurcum, T.
colubrifomis), which is a risk to the pastoral community in Amboseli ecosystem.
Overall, the results from this study demonstrate that habitat range of baboon social
groups exhibited variable overlap with other baboon groups, however overlap did not
influence helminth infection patterns across social groups. Further, the overlap between
baboons and other sympatric hosts was variable, but the degree of overlap did not
significantly influence helminth prevalence and abundance, except helminths species
richness across baboon groups. This study also found out that in sympatry, multiple
species of helminths, Cyathostominae, Trichuris spp., Moniezia benedini, Moniezia
expansa, Primasubulura sp., Enterobius sp., and Spirurina, were commonly shared but at
different levels across host taxa, with some hosts harboring more helminths richness than
others. Specifically, baboon harboured more helminths species than any host in the
community. This is the first study in Kenya to determine helminth infection pattern in a
multi-host community involving both wildlife and livestock that belong to multiple
phylogenies. Presence of Oesophagostomum bifurcum, Enterobius sp., Strongyloides sp.,
Trichostrongylus colubriformis in the Amboseli animal community is of public health
interest because of their zoonotic potential, hence this study recommends a study to
determine their prevalence in the human community in the region.
Publisher
University of Nairobi