Abstract
A study aimed at assessing the structure of rodent and shrew assemblages
inhabiting a degradation gradient while considering rainfall patterns,
was conducted in one of few remaining lowland tropical forests in
Eastern Africa. We collected a unique dataset of rodents and shrews,
representing 24 species (19 rodents, 5 shrews). The most abundant
species alternated in dominance as species abundance significantly
fluctuated across the study period following a degradation gradient
(F2,33 = 5.68, p = 0.007). While only generalist species
were observed near the degraded forest edge, habitat specialists such asDeomys ferrugineus, Malacomys longipes and Scutisorex
congicus , were observed in the primary forest interior suggesting a
significant (X2 = 1165.329, P<0.001)
association between species and their associated habitats and habitat
attributes. There was also an observed correlation between rainfall
patterns and species abundance. Capturing more species in adjacent
fallows and along the degraded forest edge suggests that many species
are able to live in degraded habitats that offer a variety of food
resources. The continued pressure on forest resources, however, may lead
to changes in habitat structure. This, coupled with the dependence of
forest ecological functions on rainfall, which is typically not the
case, may ultimately cause the local extinction of highly specialized
but less adaptable species.
Key words: Habitat degradation, Rainfall patterns, Habitat
association, Rodents, Shrews
1.0 INTRODUCTION
Deforestation in Uganda has been severe over the years due to the
continued dependence on natural resources for food, energy, medicine and
the growing human settlements close to protected areas. Forests in
Uganda have been severely degraded and their diversity compromised. Obua
et al. (2010) noted an estimated loss of 86% of Uganda’s tropical moist
forest especially on private land, while National Forestry Authority
reported an 88% and 2 % loss of tropical well stocked forest on
private land and protected areas, respectively, between 1990 and 2015
(NFA 2016). This is mainly as a result of the increasing human
population that has overtime encroached on forested areas for both
settlement and farming (Mulugo et al. 2019).
Few countries of equivalent size have as rich and diverse rodent and
shrew fauna as Uganda. Apart from many species of rats and mice there is
a great variety of other forms including gerbils, squirrels, flying
squirrels, porcupines, cane rats, mole rats, and dormice (Delany 1975).
The main factors causing this high diversity are the geographical
position at the margin of several major biogeographical areas (Linder et
al. 2012) and the wide range of altitudes and the complex array of
vegetation which support a characteristic rodent fauna (Delany 1975).
A variety of micro habitats with varying characteristics can be found in
tropical forests, and rodents and shrews are two of the most
species-rich groups of mammals that live there (Carleton & Musser
2005). Because of their diversity and abundance, they are some of the
most significant players in the ecological dynamics of forest ecosystems
(Angelici & Luiselli 2005). They are essential to the transport of
nutrients and materials through the ecosystem and to the food web
(Nicolas et al. 2009). In disturbed ecosystems, rodents play important
roles in succession as seed dispersers (Nicolas et al. 2009). In
contrast, shrews prey on insects and smaller vertebrates (Nicolas et al.
2009) and the population dynamics of their prey are regulated by their
voracious feeding habits. Shrews and rodents are both eaten by larger
vertebrates like birds and snakes. They are economically important as
crop pests and medically important, with many zoonotic heamoparasites
such as borrelia, trypanosomes, bacilli, plasmodia and coccobacilli
(Katakweba et al. 2012), and can also be employed in ecological
evaluation for conservation
decision-making.
One of the elements that shapes and influences small mammal groups in
tropical forests is habitat structure (Tews et al. 2004). In a Brazilian
rain forest, Pardini et al. (2005) discovered that the forest structure
affected both the overall abundance of species and the abundance of
particular species on an individual basis. In Africa, where the majority
of these natural areas are threatened by anthropogenic activities, there
has generally been a dearth of ecological study on rodents and shrews in
all habitats (Nicolas et al. 2009, Obua et al. 2010). Even though there
is a lot of forest damage in Africa, these activities’ immediate and
long-term repercussions are rarely examined (Malcom & Ray 2000). Few
studies have specifically looked at how habitat degradation affects
small mammal groups over time in Africa (e.g. Struhsaker 1997, Malcolm
& Ray 2000). Small mammal communities’ reactions, whether individual or
collective, provide evidence of the effects of disruptions. Some of the
most significant human-mediated disruptions to forest ecosystems are
expanding agriculture, selective harvesting for lumber, and charcoal
burning, among others (Malcolm & Ray 2000, Baranga 2007, Obua et al.
2010). Depending on the extent, severity, and kind of the disturbance,
as well as the context of the landscape, human-induced habitat
alterations have both direct and indirect consequences on small mammal
groups (Malcolm & Ray 2000).
A number of surveys of rodents and shrews of Uganda Forest Reserves have
been previously conducted. Basuta and Kasenene (1987) reported 14
species from a study in Kibale Forest National Park, Davenport et al.
(1996) and Howard et al. (1996) reported on more comprehensive small
mammal surveys from Ugandan forests. In the Mabira Central Forest
Reserve (CFR), Dickinson & Kityo (1996) conducted earlier surveys of
the rodent and shrew population, followed by the recent survey conducted
by Waswa et al. (2016) and Ssuuna et al. (2020). These studies assessed
small mammals throughout the forest with a variety of objectives;
Dickinson & Kityo (1996) focused on the distribution of species,
whereas Waswa et al. (2016) examined the composition and
organization of rodent communities and Ssuuna et al. (2020)
assessed rodent communities in different forest compartments with
varying degrees of degradation. However none of these studies has looked
at spatial and temporal dynamics of rodent and shrew communities in MCFR
along a degradation gradient while considering habitat characteristics
and rainfall patterns.
Mabira CFR is uniquely located between metropolitans of Lugazi, Mukono,
Jinja, and Kampala city (Fig. 1). As a result, the forest is under a lot
of pressure to provide a variety of products, the most important of
which are charcoal and timber. The forest is currently being invaded by
the invasive paper mulberry, which has taken over all of the forest
boundaries as gaps have opened up. Numerous groups of rodents and shrews
that depend on forests, particularly highly specialized ones with low
degrees of adaptation, may be pushed toward local extinction as the size
of natural habitats declines. The situation is made worse by the general
lack of studies, species monitoring programs, and/or habitat monitoring
programs in the region, which causes biodiversity to decline in the
absence of a baseline.
A thorough grasp of rodents and shrew ecological niches is necessary to
properly explain their importance to the dynamics of the forest
ecosystem. Such data is required to classify specific forest sections’
management regimes and/or forest habitats according to how important
they are to the local wildlife. It is hoped that the study highlights
the effect of forest habitat deterioration on a micro scale hence
stimulate fresh approaches for management of MCFR and other forests in
Uganda. Mainly the study focuses on temporal and spatial changes in
assemblages of rodents and shrews living along a degradation gradient.
The main specific objectives are: (i) to assess the diversity and
distribution of rodents and shrews along a habitat degradation gradient;
(ii) to evaluate how habitat characteristics affect the occurrence of
rodents and shrews along a habitat degradation gradient; (iii) to
analyse how rainfall patterns affect the abundance of rodents and shrews
along a degradation gradient.
2.0 METHODS
2.1 Study areas
The study was conducted in Mabira (CFR); (Fig. 1) in Uganda Griffin
Falls (0°26’14.28”N, 32°57’14.31”E, 1179 m a.s.l.) from August
2018-December 2019. This is the largest forest reserve in Central Uganda
(Colwell & Coddington 1994), managed by Uganda National Forestry
Authority (NFA) as a Central Forest Reserve (CFR). According to Howard
(1991) MCFR is considered secondary regenerating, in which the most
dominant vegetation represents sub culmination communities, heavily
influenced by man through continued excess of illegal resource use and
encroachment. However, some parts are now fully regenerated with tall
mature trees especially in the strict nature reserve compartment of the
forest (Ministry of water and environment 2010). The MCFR’s vegetation
is classified as a semi-deciduous medium altitude forest. Mabira forest
continues to exist in central Uganda as an isolated but sizable forest
island without any land linkages to the various little pockets of forest
in the Lake Victoria basin. Mabira (CFR) has a special position as the
last substantial sanctuary for forest biota in this area due to its
survival as the only fairly large contiguous forest estate in this area
(Kityo 2008).
2.2 Study design
The study was conducted in the village of Namusa in the MCFR for 12
months between August 2018 and December 2019. Data were intermittently
collected (with a one-month break after two months of data collection)
along a gradient of habitat degradation that included a primary forest
interior, a degraded forest edge, and fallows, gardens, sugarcane
plantations, homesteads close to the forest, collectively referred to as
adjacent habitats (Figure 1). For every sampling regime, nine transects
were set in subjectively selected sites, namely primary forest interior,
depleted forest edges and adjacent habitats (Figure 1). Rodents and
shrews were trapped using Sherman traps set in transects of 200 m with
20 stations and an inter-station distance of 10 m with a trapping effort
of 40 traps per transect (Mulungu et al. 2011). Traps were baited with a
mixture of peanut butter, maize flour, ripe bananas and silver fish, and
traps laid out for 3 nights. Morphometric measurements were taken from
every captured specimen including the total length (TL), tail vertebrae
length (TV), hind foot length (Hf), ear length, and weight (Wt). All
measurements were recorded in millimeters and weight in grams. All
specimens collected were kept as wet specimens in 75% ethanol and kept
as vouchers in Makerere zoological museum. Collected specimens were
identified to species using morphometric measurements cross references
with published identification guides (Brambell 1973, Delany 1975, Thorn
& Kerbis 2009, Monadjem et al. 2015) For selected individuals of each
morphotype, identifications were confirmed by sequencing of partial
mitochondrial cytochrome b gene (i.e. DNA barcoding) from 96%
ethanol-preserved samples at the Institute of Vertebrate Biology (IVB)
of the Czech Academy of Sciences. Obtained sequences were compared with
the sequences in GenBank and further unpublished sequences in the
database of IVB. The barcoding protocol (i.e. used primers, PCR
conditions and sequencing) is described in Bryja et al. (2014).
Microhabitat variables were also subjectively recorded by observation
for every transect. These were canopy cover (Delineated by percentage
cover where any cover below 40% was considered as no canopy cover),
forest undergrowth (measured by low, medium, max), while water source
(with aa 500m proximity) and leaf litter (which was measured by presence
or absence). Vegetation cover type (garden, fallow and plantation) was
used for adjacent habitats.
Average
monthly rainfall data was obtained from the Sugar Cooperation of Uganda
Lugazi (SCOUL) and used to assess how species abundance fluctuates with
rainfall over time
2.3 Data analysis
Trapping success (TS) was computed using the formula;
\begin{equation}
TS=\left(\frac{N_{i}}{T_{n}}\right)\times 100\nonumber \\
\end{equation}Where; \(N_{i}=\) number of specimens
collected\(,T_{n}=total\ number\ of\ traps\ se\)t.
Shannon-Wiener diversity index was computed from the formula;
H’=−pi ∑ ln pi
where
pi is the proportion of individuals found in species i
ln Natural logarithm
Species abundance was assessed based on the number of individuals
recorded for every species.
Correspondence analysis (CA) was performed for the different sampling
sites to show the chi-square distance among sites and also assess the
significance of association between species and habitats.
To certify adequate sample size, rarefaction curves were developed using
Vegan statistical package in R (Oksanen et al. 2016). Where the smoothed
averages of the individual curves represent the statistical expectation
of species accumulation per sampling site.
Small mammal community composition and association was measured using
“multipatt” function in “R” using packages “vegan” and
“indicspecies” (Miquel De Caceres 2013). In order to run an indicator
species analysis, a vector containing the classification of the sites
micro habitat types into groups was done using non-hierarchical cluster
analysis with different “r” functions in packages “indicspecies” and
“vegan”. In order to determine which species can be used as indicators
of different sampling sites; an approach commonly used in ecology is the
use of the Indicator Value index (Dufr^ene & Legendre 1997, De
Caceres et al. 2010). The approach calculates the “IndVal” (indicator
value) index between the species and each site group and then looks for
the group corresponding to the highest association value, the
statistical significance of this relationship is then tested using a
permutation test. All analyses were performed with R statistical
software R Core Team (2013). Multiple linear regression was carried out
to assess the relationship between species richness and species
abundance with rainfall. The assumption is that species richness and
abundance follow rainfall patterns. Line graphs were made to examine for
any temporal trends in species richness and abundance, while cross
correlation graphs were made to seek for relationship patterns between
species richness, abundance and rainfall.