Introduction: The role of wildlife behavior in infectious disease
emergence
Emerging Infectious Disease
Over the last 40 years, the emergence of zoonotic diseases has increased (Jones et al.
2008), signaling the escalating importance of understanding infectious disease dynamics
at the human-wildlife-environmental interface. Disease emergence events are often
coupled with ecological perturbations that affect the environment, host, and pathogen,
changing the manner in which pathogen communities connect with susceptible hosts
(Schrag and Wiener 1995, Plowright et al. 2008). Seemingly minor changes in landscape
features or host exposures can have significant influences on disease emergence, as for
example, the role of agricultural intensification in the emergence of the deadly bat-borne
zoonosis, Nipah Virus (Capelle and Morand 2017). Computational models of infectious
disease dynamics often neglect elements of these interactions (Alexander et al. 2012),
which are likely fundamental to disease emergence processes in disturbed landscapes.
Landscape change can interact with and influence wildlife behavior, and therefore,
infectious disease dynamics. For example, natural disturbances (e.g. fragmentation,
extreme weather events) can modify community structure, contact networks, and
pathogen transmission dynamics (Poteet 2006, Watson et al. 2007). Increases in host
density around limited or non-seasonal human-associated resources can increase contact
and transmission rates and create opportunities for cross-species transmission (Becker et
al. 2015). Changes in stress and pollution along the urban-rural gradient can also affect
2
host susceptibility to infectious disease and the outcome of pathogen exposure events
(Bradley and Altizer 2007).
The Effects of Human-Modified Landscapes on Wildlife Behavior
The potential for human-modified ecosystems to influence wildlife host behavior and
disease transmission dynamics is especially complex as changes in behavior can
influence both host exposure and susceptibility (Hawley and Altizer 2011). Studies have
principally focused on two overarching questions in this area of research: 1) how does
social behavior lead to variability in pathogen susceptibility and exposure between
individuals, and 2) how might behavior increase the potential for an individual to act as a
super-spreader or, more generally, increase transmission heterogeneities among
individuals? Here, super-spreader refers to individuals that contribute disproportionately
to pathogen transmission (Lloyd-Smith et al. 2005, Woolhouse and Gowtage-Sequeria
2006). The research focus here has been directed at understanding heterogeneity at the
individual level (Paull et al. 2012). However, there is a limited understanding of the role
that heterogeneous landscapes play in shaping host behavior, and consequently disease
dynamics, representing an area of research ripe for investigation.
To explore these dynamics and test related hypotheses, I use a long-term study population
of banded mongooses (Mungos mungo) in Northern Botswana. This population is
infected with an emerging Mycobacterium tuberculosis complex pathogen,
Mycobacterium mungi (Alexander et al. 2016). After the onset of clinical symptoms,
diseased mongooses usually die within 2-10 months (Alexander et al. 2016). Mortality
associated with M. mungi ranges from 10 to 15% per year in Chobe District, Northern
3
Botswana (Fairbanks 2013b). Unique to tuberculosis pathogens, this strain is transmitted
through scent-marking behaviors used in olfactory communication (See Figure 1 from
(Alexander et al. 2016)). When an infected individual deposits a signal (i.e. a scent
mark), the uninfected individual that investigates the signal is exposed to the pathogen,
and can then become infected. This is the first report of a tuberculosis pathogen being
transmitted through olfactory communication behaviors (Alexander et al. 2016).
4
Figure 1: Banded mongooses become infected with Mycobacterium mungi through
secretions used in olfactory communication behavior. (A) Banded mongooses get injuries
from daily interactions with conspecifics and/or the environment. (B) When engaging in
olfactory communication behaviors, contact with infected anal gland secretions allows
the pathogen to invade the mongoose host through these injuries. (C) Pathogen invasion
results in disease (Alexander et al. 2016).
M. mungi occupies lineage 6 of the M. tuberculosis Complex (MTC), which is comprised
of the West African human-associated pathogens (M. Africanum subtypes) and those
infecting African mammals (See Figure 2 from (Alexander et al. 2016)). The only known
5
outbreaks of M. mungi in banded mongooses have occurred in Northern Botswana and
northwestern Zimbabwe. Other wildlife species infected by wildlife-associated lineage
six pathogens include the rock hyrax (Procavia capensis; dassie bacillus) and meerkat
(Suricata suricatta; M. suricattae), but there is no range overlap between infected
populations. Though the outbreaks in banded mongooses, rock hyraxes, and meerkats are
in Southern Africa, the only known outbreaks of M. africanum and chimpanzee bacillus
are in West Africa.
Figure 2: Phylogenetic relationships among Mycobacterium tuberculosis Complex
(MTC) pathogens and reservoir species. Range overlap for reservoir hosts of lineage 6
MTC and known outbreaks of wildlife-associated lineage six MTC are provided
(Alexander et al. 2016).
Infected banded mongoose populations in Chobe District, Northern Botswana inhabit
both the urban areas of Kasane and Kazungula and the rural area of Chobe National Park.
In urban areas, banded mongooses utilize resources from humans. Previous work
6
identified increased levels of aggression between banded mongooses when foraging in
garbage compared to foraging naturally. The increase in aggressive behavior led to more
injuries, increasing pathogen exposure and transmission of M. mungi (Fairbanks 2013b).
In addition to the increased availability of food resources in the study site, the results
from past work show that the study population also uses anthropogenic resources for
denning when they are available (Laver 2013a). Further, the banded mongoose troops
that live in close association with humans, and therefore utilize anthropogenic resources
(i.e. food, water, and den shelter), have smaller overall home ranges, overall core ranges,
and overall space use dispersion compared to troops that inhabit more remote areas
without human influences (Laver and Alexander 2017). These results show that
anthropogenic resources in human-modified areas are important to mongooses and should
be examined to better understand the conditions that influence host behaviors across the
landscape. This host-pathogen system provides the opportunity to explore how social
behavior and landscape features may interact to modify transmission probabilities across
complex landscapes and is the focus of the following three chapters in this thesis
References
Alexander, K. A., P. N. Laver, A. L. Michel, M. Williams, P. D. van Helden, R. M. Warren, and N. C. G. van Pittius. 2010. Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerging infectious diseases 16:1296.
Alexander, K. A., B. L. Lewis, M. Marathe, S. Eubank, and J. K. Blackburn. 2012. Modeling of wildlife-associated zoonoses: applications and caveats. Vector-Borne and Zoonotic Diseases 12:1005-1018.
Alexander, K. A., C. E. Sanderson, M. H. Larsen, S. Robbe-Austerman, M. C. Williams, and M. V. Palmer. 2016. Emerging Tuberculosis Pathogen Hijacks Social Communication Behavior in the Group-Living Banded Mongoose (Mungos mungo). mBio 7:e00281-00216.
Becker, D. J., D. G. Streicker, and S. Altizer. 2015. Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta‐analysis. Ecology letters 18:483-495.
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Bradley, C. A., and S. Altizer. 2007. Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22:95-102.
Capelle, J., and S. Morand. 2017. Wildlife and emerging diseases in Southeast Asia. Biodiversity Conservation in Southeast Asia: Challenges in a Changing Environment.
Fairbanks, B. M. 2013. Bidirectional interactions between behavior and disease in banded mongooses (Mungos mungo) infected with Mycobacterium mungi.
Hawley, D. M., and S. M. Altizer. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25:48-60.
Jones, K. E., N. G. Patel, M. A. Levy, A. Storeygard, D. Balk, J. L. Gittleman, and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature 451:990-993.
Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359.
Paull, S. H., S. Song, K. M. McClure, L. C. Sackett, A. M. Kilpatrick, and P. T. Johnson. 2012. From superspreaders to disease hotspots: linking transmission across hosts and space. Frontiers in Ecology and the Environment 10:75-82.
Plowright, R. K., S. H. Sokolow, M. E. Gorman, P. Daszak, and J. E. Foley. 2008. Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6:420-429.
Poteet, M. F. 2006. Shifting roles of abiotic and biotic regulation of a multi-host parasite following disturbance. Disease ecology. Oxford University Press, New York, New York, USA:135-153.
Schrag, S. J., and P. Wiener. 1995. Emerging infectious disease: what are the relative roles of ecology and evolution? Trends in Ecology & Evolution 10:319-324.
Watson, J. T., M. Gayer, and M. A. Connolly. 2007. Epidemics after natural disasters. Emerging infectious diseases 13:1.
Woolhouse, M. E., and S. Gowtage-Sequeria. Host range and emerging and reemerging pathogens. 2006.
Variation in olfactory behavior across the landscape: inferences about
pathogen shedding in wild banded mongoose (Mungos mungo)
populations
Abstract
Infectious disease transmission is driven by a complex suite of drivers with behavior and
landscape dynamics contributing importantly to epidemic patterns across host-pathogen
systems. However, our understanding of the interaction between landscape, behavior, and
infectious diseases remains limited. In the banded mongoose (Mungos mungo), a novel
tuberculosis pathogen, Mycobacterium mungi, has emerged in Northern Botswana and is
transmitted through olfactory communication behaviors. Using this host-pathogen
system, we assess the influence of landscape use and mongoose behaviors on the
frequency of olfactory communication observations. We use remote sensing camera traps
at den sites to eliminate observer influence across human-modified and urban landscapes
(n=18 troops, 18,229 detections of banded mongooses from 7,497 photographs). We
identified a significant influence of landscape, vigilance behavior, and the interaction
between the two on the frequency of olfactory communication behaviors that are
associated with disease transmission. Vigilance across the landscape is multifaceted,
associated with territorial defense and predator avoidance and can be a stimulant for
olfactory communication in some land use areas and an inhibitor in others. While
vigilance in lodge areas increased olfactory behaviors, in natural and urban landscapes
with putatively higher predator risk, vigilance had a negative impact. Our results
9
underscore the complexity of the interaction between landscape and behavior and the
importance this may have on pathogen transmission dynamics.
Introduction
Human-mediated landscape change is increasingly linked to zoonotic disease emergence
(Jones et al. 2008). Outbreaks of disease have occurred, however, across a wide array of
landscape types and host-pathogen systems, challenging our ability to develop a full
mechanistic understanding of the process (Brearley et al. 2012). Urbanization can have
complex impacts on the environment and wildlife hosts with changes in stress and
pollution exposures occurring along the urban-rural gradient, affecting host susceptibility
to infectious diseases (Bradley and Altizer 2007). High concentrations of resources in
modified habitats can influence pathogen exposure through increased contact due to host
aggregation or indirectly through changes in host behavior (Becker and Hall 2014,
Becker et al. 2015, Flint et al. 2016). For example, banded mongoose troops in Northern
Botswana were more aggressive when foraging in garbage than when they were in other
habitats. The elevation in aggressive behavior led to more injuries, increasing pathogen
invasion potential for the emerging pathogen Mycobacterium mungi (Flint et al. 2016).
The foraging plasticity of foxes (Vulpes vulpes L.) in urban areas has also been linked to
lower infection levels of Echinococcus multilocularis, as foxes primarily consume waste
instead of rodents, the intermediate host for this parasite. Understanding comparative
behavior dynamics across landscape type is central to determining how these divergent
areas may influence host ecology.
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The changes brought about by human population expansion (i.e. urbanization) can alter
the biology of hosts, pathogens, and vectors in human-modified landscapes (Bradley and
Altizer 2007, Gottdenker et al. 2014). The rate of urbanization is accelerating (Ramalho
and Hobbs 2012, DeSA 2013) with urban ecosystems becoming increasingly common
(Magle et al. 2012). The process of urbanization is one of extreme ecological change
influencing ecosystem processes as well as wildlife community structure. Wildlife
behavior is identified as one of the first things to change in human-modified
environments (Plotkin 1988, Lowry et al. 2013) and behavior is increasingly recognized
as a critical variable influencing infectious disease dynamics (Dizney and Dearing 2013).
While these urbanized areas were once considered to be suitable for only a few species,
we are now observing use by a wide array of wildlife species (Ditchkoff et al. 2006), with
consequent implications to zoonotic disease transmission in these landscapes. These
novel, anthropogenically-influenced landscapes tend to be subject to sustained processes
of ecological change (i.e. ongoing urbanization and development) that can modify the
fitness of wildlife species through complex and interdependent mechanisms (Brearley et
al. 2012, Russo and Ancillotto 2015). Understanding these potential effects of
urbanization on wildlife populations has been identified as central to conservation
planning (Angeloni et al. 2008) and increasingly public and animal health (McKinney
2002, Wu et al. 2017).
Communication is often seen as a key behavior central to individual and group fitness in
many social species, which can be influenced strongly by environment (Hutton and
McGraw 2016). Animals show an enormous diversity in whether, when, where, and how
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they communicate, ranging from auditory signals, like the roar of a lion to broadcast
ownership of a territory and stay in contact with other members in the social group
(Grinnell and McComb 2001), to visual signals, like the brightly colored plumage of
male cardinals to help females assess the health of potential mates (Bradburry and
Vehrencamp 2011). A common mode of communication is through olfaction, where
individuals deposit scents with chemical cues in the environment to communicate with
conspecifics in various social contexts (Arakawa et al. 2008). Olfactory communication
is common among mammalian species and plays a crucial role in spatial organization and
sexual and other social behaviors (Stoddart 1976, Brown and Macdonald 1985).
Information such as the depositor’s identity (Boogert et al. 2006), reproductive status
(Washabaugh and Snowdon 1998), competitive abilities (Rich and Hurst 1999), and even
health status (Kavaliers and Colwell 1995, Penn et al. 1998, Klein et al. 1999, Willis and
Poulin 2000, Zala et al. 2004) can be communicated to conspecifics. Numerous
mammalian species have successfully inhabited urban ecosystems, but limited attention
has been directed at understanding how transformed landscapes may influence this key
behavior (Hutton and McGraw 2016). We know even less about the manner in which
changes in communication may change infectious disease transmission.
In Northern Botswana, an emerging Mycobacterium tuberculosis pathogen, M. mungi
infects the highly social banded mongoose (Mungos mungo). Pathogen transmission
occurs through olfactory communication (anal gland scent marks and urine (Alexander et
al. 2016). In this species, olfactory behaviors are utilized in both inter- and intra-group
communication (Jordan et al. 2010) and play a crucial role in territorial defense (Rood
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1975, Müller and Manser 2007) and reproduction (Jordan et al. 2010, Jordan et al. 2011a,
Jordan et al. 2011b, Jordan et al. 2011c). We use this host-pathogen system to investigate
the influence of landscape change on olfactory communication and disease transmission.
Methods
Study Site and Species
We studied 15 troops ranging from eight to 50 individuals. The study population in
Northern Botswana occupies the town of Kasane and urban-transiting Kazungula and
Chobe National Park. Banded mongoose troops occur across land use type with territories
that can span different land use designations (See study site map in Chapter 3).
Banded mongooses are small (<2kg), diurnal mesocarnivores that live in social groups
(Rood 1975). Troops are territorial and occupy home ranges that spatially decrease with
increasing association with humans (Laver and Alexander 2017). Home ranges of
adjacent troops regularly overlap in these higher density environments. Home ranges are
defended against intrusions and boundaries can be demarcated by feces, urine, and other
scent marks (Rood 1975, Müller and Manser 2007). Intertroop conflicts do occur and can
result in mortality, but can also lead to intergroup group breeding events (Jordan et al.
2010). Mongooses are communal breeders with a low reproductive skew with females of
the same troop going into estrous simultaneously (Cant 2000). Lactating females
allosuckle pups and pack members cooperate in raising the young at communal dens with
some adults staying behind to guard pups while others forage (Cant 2003). Once the pups
are old enough to accompany adults on foraging bouts, a pack member escorts them
(Cant 2003). In our study site, pups emerge from dens throughout the wet season
13
(November-March), but first matings of the breeding season occur in August (Laver and
Alexander 2017).
There are several documented predators to banded mongooses such as birds of prey,
1975), African rock pythons (Python sebae)(Rood 1975, Otali and Gilchrist 2004, Laver
et al. 2012), warthogs (Phacochoerus africanus), and monitor lizards (Varanus
exanthematicus) (Otali and Gilchrist 2004). Banded mongoose group members
cooperatively gather to inspect predator cues (Müller and Manser 2007, Furrer and
Manser 2009) and bunch together to attack or mob predators and competitors (Rood
1975). They also emit alarm calls and pack members rush to assist individuals calling in
distress (Furrer and Manser 2009).
In the human-dominated landscape, mortality is more commonly associated with
vehicles, human conflict, and predation by domestic animals than in other areas (Laver
and Alexander 2017). Human responses to banded mongooses can be quite divergent,
from feeding mongooses to direct persecution when banded mongooses are perceived as
pests (e.g. hot oil being poured into active den sites, stoning). Banded mongoose will
mob domestic dogs that threaten the group, often resulting in fatal injuries for the banded
mongoose (11%, n=20/188 deaths recorded from 2008-2016)
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The study population is infected with a novel strain of tuberculosis, Mycobacterium
mungi, and diseased individuals usually die within three months (Alexander et al. 2010).
Sick individuals are identifiable through observation of clinical symptoms of infection
including anorexia, hunched body posture, matted fur, excessive watering of the eye,
sneezing, nasal enlargement and/or deviation of the nasal planum accompanied with a
build-up of mucus, enlarged testicles, and lethargy. Sick individuals are not evicted from
the troop, but they often lag behind during group movements (Alexander et al. 2016).
Behavioral Data
Radio tracking and camera traps
Study banded mongooses were followed with the use of radio telemetry. Within each
troop, one or two banded mongooses were trapped and fitted with radio collars as
previously described (Alexander et al. 2010). The 15 collared troops were tracked five
days a week, alternating seven troops on the first day and the other eight troops the
following day.
A challenging problem in the study of wildlife behavior is obtaining observational data
that is not influenced by the observer. Banded mongoose troops range across land type
and respond strongly to the observation of humans in certain land types (i.e. urban,
residential, national park) or in places they do not expect to see people (e.g., behind
certain buildings or in hedgerows). Fleeing responses are common making behavioral
studies challenging. In order to overcome these limitations, we deployed camera traps at
den sites. This allowed us to track mongooses and place the camera trap before they came
15
out of the den, allowing us to capture data across troops and land use in a study location
that could be common to all study troops across land type.
We placed cameras at den sites of 15 banded mongoose study troops (January 2016 to
March 2017). As banded mongooses change dens every two to three days, remote sensing
cameras were placed at the identified den sites of the troops tracked that day and moved
when the troop vacated the site. If the den was not located during the day, we used
homing telemetry to track towards the troop and locate mongoose at night while the troop
was in the den. If the den was within a gated area, or an area considered dangerous to
enter at night, we returned the next morning to attempt to locate the den and place the
camera before banded mongooses emerged from the den. In the event the animals were
out before the camera could be placed, the camera would be deployed later in the day and
data collection commencing the next uninterrupted den emergence event.
Cameras were placed using naturally occurring objects (e.g. trees, shrubs, fences), as well
as self-made mounts to obtain a favorable angle and distance between the camera and the
area of interest. Den sites were classified by land area as follows: 1) lodge areas,
including landscaped areas that were watered daily, guest rooms, kitchens, and staff
housing, 2) residential areas, including private homes and local village residential plots,
3) urban areas, such as the hospital and shopping areas, 4) undeveloped areas not within
the protected area of the national park or forest reserves, but still susceptible to some
human or vehicle traffic, and 5) the national park, which was the protected area of Chobe
National Park.
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Animal research activities were conducted through the use of an approved protocol from
the Virginia Tech Institutional Animal Care and Use Committee (IACUC #16-217) and
under permit from the Botswana Ministry of Environment, Natural Resources
Conservation and Tourism (EWT 8/36/4 XXVI).
Behavioral observations from photographs
For each photograph the date and time, the number of individuals within each
photograph, and their behavioral state (i.e., olfactory, marking, non-vigilant, and vigilant)
were tallied (See Table 1 for ethogram). Both the marking and olfactory behaviors
contribute to olfactory communication. The marking behaviors included: (1) anal scent
marks which are deposited by dragging secretions from the anal gland across a surface;
(2) cheek marks or wipes; (3) urination or defecation; (4) urination followed by stomping
the back limbs coined token dance urination; and (4) feces that are deposited at specific
marking sites called latrines (Müller and Manser 2007, Jordan et al. 2010, Fairbanks et al.
2014). The olfaction behaviors crucial for investigating chemical cues included: (1)
smelling the ground or an object; (2) smelling the location where a scent was deposited;
and (3) smelling another mongoose. All other behaviors were grouped into vigilant and
non-vigilant behaviors (Table 1).
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Table 1. Ethogram for banded mongooses (Mungos mungo). The behaviors were grouped
into four categories: (1) non-vigilant, (2) olfactory behaviors, (3) marking behaviors, and
(4) vigilant behaviors.
Category Behavior Description Non-vigilant
Forage Digging for food item, manipulating food item, chewing
Running Trotting or running
Walking Walking
Play (alone) Manipulating non-food object, usually interspersed with bouncing and play calls
Contact garbage or human food
Contact with garbage or human food, primarily while foraging in it
Emerge Emerging from den or other structure
Excavate Digging at den site. Differs from digging for food in that both front paws are usually used synchronously for excavating, the depth is usually greater than for foraging, and no food items are eaten.
Social play Rough and tumble contact or chasing interspersed with bouncing and play call
Aggression/defense Agonistic contact with at least one other mongoose. Distinguished from play by aggressive sounds, lack of bouncing, and more forceful motions that may cause injury (e.g. forceful scratching and biting rather than pawing and mouthing)
Copulate Mating
Allofeed Feeding another mongoose, typically a pup
Jerky greeting A greeting where two animals jerk their heads back and forth while approaching each other, culminating in bodily contact with continued jerking of the head
Clasp One mongoose clasping another with front paws, similar to a mating position, but without intromission. Often performed during play.
Beg Performed by pups and sub adults. Following and sometimes touching another mongoose while emitting begging calls.
18
Lead An individual incites the group to move from the current
location with contact calls that are louder and faster than usual while walking or trotting away from the current location.
Follow Walking or trotting in a direction that the leading animal is moving. Usually accompanied by mimicking the leading call.
Lying down Lying down with very little movement, whether asleep or awake.
Sit or stand still Sitting or standing with little to no movement. Head is below horizontal
Groom Scratching, gnawing, or licking oneself. (Counted as resting behavior because generally interspersed with lying down or sitting during periods when the troop is resting)
Allogroom Licking or gnawing another mongoose. Typically performed during a troop resting periods.
Social rest Lying while in physical contact with at least one other mongoose
Social sit or stand Sitting or standing while in physical contact at least one other mongoose
Olfactory Behaviors
Smell Smelling the ground or an object
Scent smell Smelling an area that is known to be scent marked Social smell Smelling another mongoose Marking Behaviors
Defecate/urinate Excretion
Token dance urination
Urination involving the stereotypical stomping of ground with hind limbs
Latrine Defecation Feces are deposited in token amounts at specific sites called latrines
Social scent mark Rubbing another mongoose with anal glands
Scent mark Rubbing ground or object with anal glands
Over-marking One individual places its scent mark directly over the scent mark of another individual
Cheek mark Rubbing the side of the ‘face’ on surfaces and along the ground
19
Vigilance Behaviors
Vigilance Head is horizontal or above horizontal but not oriented to another mongoose. Head bobbing may occur. Gaze may be direct toward a perceived threat. All four legs are on the ground.
Bipedal Vigilance Head is horizontal or above horizontal but not oriented to another mongoose Head bobbing may occur. Gaze may be direct toward a perceived threat. Standing on back two legs.
Scanning Head is horizontal or above horizontal and scans the landscape.
Flee Trotting or running from a perceived threat
Alarm call Any of several calls used when a perceived threat is present. Often accompanied by vigilance or fleeing.
Vigilance while chewing
Exhibits vigilance behaviors while chewing
Observation Time
The length of camera observation periods varied by trap event and den sites. Each camera
trap event was defined as the start time in which the first photo was taken to the end time
of the series. If there were no photos for 10 minutes, the next photo would be considered
a new event (Flint et al. 2016). For the instances that a single photograph was collected, it
was given the lowest time interval designation of 10 seconds, since that is the lapse time
for the remote sensing camera traps to capture another photograph.
Data Analysis
Olfactory communication behavior was analyzed using generalized linear mixed models
in the glmmADMB package in RStudio Version 1.1.383. The top model was selected
using the Akaike’s Information Criterion adjusted for small sample sizes (AICc)
(Burnham and Anderson 2003). The den sites were used as the random effects (1|Den).
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We used a negative binomial distribution with a log link. The fixed effects were set as
land use, the presence of pups, season (wet and dry), and vigilance (Table 2). When
significance of the top model was indicated (α ≤ 0.05), the Tukey-Kramer adjustment in
the Multcomp package was used to compare least-square mean estimates to determine
differences.
The number of mongooses, observation minutes, and photographs obtained during an
observation event varied between and within den sites. To standardize data and account
for the unequal observations, the offset was calculated by the equation
where p is the number of photos, t is the observation time in minutes for that
observational period, and b is the number of banded mongooses observed across all
photos in that observational period.
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Table 2: Variables used in candidate models describing olfactory communication
behavior with justification and supporting literature. Candidate models represent banded
mongoose olfactory communication behavior in Northern Botswana.
22
Results
From January 2016 to March 2017, we sampled 281 den nights from 18 troops leading to
1,815 observation periods (15 radio-collared troops, three opportunistically sampled
troops). There were 18,229 detections of banded mongooses from 7,497 photographs.
Land use, vigilance, and an interaction between these variables explained variation in
olfactory communication behavior across den sites and troops (Table 3). There were no
competing models. Sick mongooses were captured in photos (n=98). However, across
photos, we did not observe olfactory behavior in these sick individuals.
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Table 3: Modeling rankings for banded mongoose olfactory communication behavior in
Northern Botswana, with k (number of parameters), Akaike’s information criteria (AIC)
value, Akaike’s information criteria, corrected for small sample size (AICc), difference in
AICc value between best supported model and ith model (ΔAICc), wi (model weight),
and ERi (evidence ratio).
Olfactory Communication Behavior
Vigilant behavior was an informative parameter for olfactory communication behavior
(Table 4; t=5.66, p =<0.001) and had a positive correlation with olfactory behavior. The
top model also had an interaction between vigilance and land use areas indicating that the
relationship with vigilance and olfactory communication was dependent on land use area.
The coefficient for vigilance in the national park (-6.75) and urban (-0.60) land use areas
had a negative association with olfactory communication, whereas vigilance at the lodges
24
(0.84) had a positive association (Vigilance: National Park t=-4.03, p =< 0.001 and
Vigilance: Urban t= -3.80, p =< 0.001). The interaction of vigilance in the residential
areas also had a negative association, but it was not significantly different than zero.
Table 4: Parameter estimates of our best supported model for banded mongoose
olfactory communication in Northern Botswana.
Olfactory communication varied by land use areas with the highest in the urban land use
areas. The estimate for the undeveloped land area was significantly different than zero
and negatively associated with olfactory communication (t= -2.88, p=0.004). The least
square means of undeveloped land use area was significantly less than the lodges, the
national park, and the urban land use areas, but not the residential land use area (Figure
Table 5).
25
Table 5: The mean differences, standard errors, p-values, and 95% confidence intervals
for the differences in banded mongoose olfactory communication across the land use
areas in Northern Botswana.
Discussion
Individual behavior can influence infectious disease transmission and understanding how
this might be modified across a landscape is of fundamental importance, particularly
when these behaviors themselves provide a transmission route for infectious disease. We
identified the importance of the landscape and vigilance behavior in shaping the olfactory
communication behaviors that may influence disease transmission of M. mungi. Olfactory
communication was significantly lower in the undeveloped landscape than in the national
park, lodges, and urban areas. However, in land use areas where olfactory communication
was higher, vigilance was a stimulant in some land use areas (i.e., lodges) and an
26
inhibitor in others (i.e., national park, urban). Olfactory communication is a common
form of communication for mammalian species and is involved in numerous mechanisms
from territoriality to sexual reproduction (Brown and Macdonald 1985). The interaction
between behaviors, here, vigilance, land use, and olfaction was bidirectional, providing
insight into the complex interaction between land type and behavior.
Vigilance behaviors are fundamental to fitness across species, providing information on
predation risk (Beauchamp 2015). Nothing has more unforgiving impacts to overall
fitness than being killed by a predator (Lima and Dill 1990). Vigilance allows for early
detection of predators and varies in accordance with type and abundance of predators
(Laundré et al. 2010). Where larger predators may invoke a fleeing behavior, others such
as domestic dogs can elicit mobbing and aggressive behaviors (Lima and Dill 1990). In
order to avoid predation, individuals must assess the predation risk in an environment and
decide whether to invest in anti-predator behaviors or other fitness-promoting activities
(e.g. foraging, acquiring a mate) (Lima and Dill 1990). While most studies assess the
trade-offs associated with vigilance and feeding behavior (Lima and Dill 1990), this
trade-off likely extends to other behaviors such as olfaction communication.
In addition to the threat of predation, vigilance behaviors are also associated with
territorial defense (Beauchamp 2015). Troops respond more aggressively to known
neighboring troops than unknown troops, which is likely related to competition for
resources as well as breeding opportunities (Müller and Manser 2007). Previous research
in our study site shows that mongooses living in association with humans have smaller
27
overall home ranges, overall core ranges, and overall space use dispersion (Laver and
Alexander 2017). This decrease in space use is likely the result of non-seasonal resource
provisioning and denning opportunities associated with human waste and buildings in
transformed landscapes. The groups living in association with humans den in man-made
structures, feed from refuge sites, and drink from anthropogenic water (i.e gray-water,
sewage, and lawn sprinklers) (Laver and Alexander 2017). In addition to using man-made
den sites, anthropogenic den sites such as drains and buildings remain intact much longer
and are used by multiple troops, but not simultaneously (Chapter 3). Though olfactory
communication behaviors were highest in the urban, lodge, and national park land use
areas, the concentration of troops around human-mediated resources in the urban and
lodge land use areas likely results in more encounters with neighboring troops, where
between troop exposure to scent marks may occur since those behaviors are associated
with territorial defense (Rood 1975, Müller and Manser 2007). During inter-pack
encounters, while some individuals rush towards the interaction with the other group,
others mark or counter-mark objects surrounding the event and intra-group copulations
are sometimes observed (Cant et al. 2002, Müller and Manser 2007).
Similar to the urban land use areas, the lodges also have a constant human presence (i.e.
full-time staff and tourists), but the Botswana tourism industry is based on wildlife
viewing opportunities, so the humans in lodge environments rarely pose a threat to
banded mongooses. Further, the lodges typically have fences to deter megafauna
populations, but other animals (e.g. banded mongooses, warthogs, vervet monkeys
(Chlorocebus pygerythrus), Chobe bush buck (tragelaphus scriptus ornatus)) regularly
28
utilize these areas (See animal and human presence across landuse in Table 6). These
fenced environments preserve riparian forests in the region providing mature, closed
canopies with an open cultivated lawn understory that likely allows the detection of
predators from afar and a delay in flight response. Flushing behavior is the distance
between an observer and animal when it flees and is used to determine tolerance of
predators (Petrelli et al. 2017). If the mongooses are able to see threats from afar, they
might invest in olfactory communication behaviors. Though the banded mongooses in the
urban areas still face the threat of competition, because of the infrastructure in this area
there is a likely a shorter line of sight. Similarly, the national park land use areas has tall
grasses, likely reducing the line of sight, and therefore, the ability to detect predators
from afar. Considering that there was a negative association between vigilance and
olfactory communication in the urban and national park land use areas, the mongooses
here might initiate flight behaviors once a threat is detected.
29
Table 6: The mean animal and human presence per camera trap day across the land use
areas in Northern Botswana. These values were derived from 74 remote sensing camera
traps placed at active banded mongoose den sites. For more information about the species
captured, see Supplementary Table 1 in Appendix.
Previous research in our study system identified reduced activity, decline in alert
behaviors, and increased resting behaviors among clinically ill mongoose (Fairbanks et
al. 2014). In this study, we did not observe any clinically ill mongooses engaging in
olfactory behaviors. This may have important implications to pathogen transmission
dynamics suggesting that a window of pathogen transmission may be bounded by the
interaction between pathogen shedding and the clinical impacts of disease hindering the
ability to undertake normal behaviors. Here, behavior may have a bidirectional affect.
Pathogen shedding is directed through olfactory behavior but sickness behavior might
30
lead to containment of contagion at the individual level with the reduction or cessation of
pathogen shedding. Scent marking behaviors can be costly and may be reduced when
energy investments are required elsewhere, such as immunity (Gosling et al. 2000). For
example, male house mice (Mus musculus domesticus) reduced scent marking during
experimental infections with Salmonella enterica C5TS (Zala et al. 2004). In Uganda,
banded mongooses that had higher levels of infection with the protozoan parasites,
Isospora, and the nematode worm, Toxocara, scent marked at lower rates than did
mongooses with lower infection levels. (Mitchell et al. 2017). Counter-marking of scent
marks from the opposite sex among individuals with high parasite loads were also
reduced (Mitchell et al. 2017). It is unclear if M. mungi has a latency period and how
pathogen shedding occurs over the course of disease. Further research is needed to
evaluate the influence of clinical disease on pathogen shedding among infected
individuals and the influence this may have on epidemic behavior and pathogen spread.
Landscape-behavior interactions may influence the transmission of other infectious
diseases, as for example, leptospirosis (Leptospira sp), which is transmitted through urine
and infects 45% of sampled banded mongooses in our study site (Jobbins and Alexander
2015). While there is great interest in developing our understanding of the role of
individual behavior in shaping disease transmission dynamics, our work demonstrates the
fundamental influence that the landscape may have on these interactions. Complex
landscapes may organically create heterogeneity in pathogen transmission dynamics
between individuals across land type.
31
Acknowledgments
We are grateful to numerous CARACAL team members for their assistance in the field
and reviewing photographs. We also thank Mark Vandewalle for logistical and field
assistance. This project was supported by the National Science Foundation Ecology and
Evolution of Infectious Diseases (#1518663) and Morris Animal Foundation (#D14ZO-
083).
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34
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Characteristics of banded mongoose (Mungos mungo) communal den
sites across the human-wildlife interface in Northern Botswana
Abstract
Denning behavior is a critical life history attribute for many mammalian species and can
be impacted by urbanization, affecting species reproductive success and survival in these
landscapes. Banded mongooses (Mungos mungo) in Northern Botswana are infected with
a novel Mycobacterium tuberculosis complex pathogen, M. mungi that is transmitted
through olfactory communication networks and infected scent marks that allow the
pathogen to move through the population through both direct and environmental
transmission routes. Here, we studied characteristics of active banded mongoose den sites
across 24 troops and 308 den sites in Northern Botswana (348 den nights from 2008-2010
and 281 den nights from 2016-2017). Dens were located across the human-wildlife
interface (national park, lodge, urban, residential, undeveloped). Cluster and
Classification and Regression Trees (CART) analysis of the den sites identified important
differences in den site characteristics across the land area designation. Habitat type was
the most important factor for den sites located at lodges, associated with the presence of
gallery forest and teak woodlands. Distance to the nearest tar road appeared to be the
most important variable separating the dens in the National Park from those outside of
lodge environments in human transformed landscapes. Den type was the most predictive
of den sites located in human-modified environments. Sites that had the longest use were
dominantly anthropogenic in nature (94% ± 6%, n= 67, used in 2008-2010 and 2016-
2017). Natural dens, in contrast, appeared to be more vulnerable to destruction and
36
shorter-lived. Only anthropogenic dens were used by troops other than the resident troop
(6%, n=19/308). These space-sharing behaviors in a territorial species may have
important influences on pathogen transmission dynamics allowing pathogen exposure
and transmission potential to increase between territorial groups. Anthropogenic land
areas appear to exert an important influence on denning behaviors in the banded
mongoose, which is information beneficial for researchers and managers as numerous
species readily adapt to novel opportunities provided by human-land transformation.
Introduction
The majority of mammalian species use some form of shelter on a daily basis (Reichman
and Smith 1990). These can vary widely from simple bedding near coniferous trees
during the night (e.g., white-tailed deer, Odocoileus virginianus (Armstrong et al. 1983)),
to the more intricate construction of lodges by beavers (Castor canadensis) (Collen and
Gibson 2000). Burrowing mammals require access to in-ground shelter and the
availability of these sites can have important influences on species reproductive success
and survival (Reichman and Smith 1990). Dens act as a place to reside when these
species are not engaging in other fitness-promoting activities (e.g. foraging, searching for
mates) and also offer critical protection from harsh, fluctuating environments, and
predation (Reichman and Smith 1990). Denning behavior is a critical element of a species
natural history (Reichman and Smith 1990) and a central element of a species
conservation management.
Den sites can be a limiting resource in a landscape and may be used by more than one
social group, exerting critical influences on contact networks and intra-and inter-specific
37
pathogen transmission potential for vector, environmentally and directly transmitted
pathogens. Particular landscape features then provide a connection through space sharing
(active or delayed) among infected and susceptible hosts, elements that may change
pathogen transmission potential across a population and landscape. For example, den
sharing was identified as a primary risk for Mycobacterium bovis infection in brushtail
possums (Trichosurus vulpecula) (Corner et al. 2003). Subadult rabbits (Oryctolagus)
move between warrens of different groups and therefore play a role in transmission of
rabbit hemorrhagic disease and myxomatosis (Jennings and Mutze 2018).
Banded mongooses are small, burrowing species, which are group living and den
communally (Rood 1975, Cant 2000). This population is infected with a novel
Mycobacterium tuberculosis complex pathogen, M. mungi that is transmitted through
olfactory communication networks and infected scent marks that allow the pathogen to
move through the population through both direct and environmental transmission routes
(Alexander et al. 2016). For banded mongooses, natural dens tend to consist of excavated
holes in the ground and termite mounds, but troops may also make use of man-made den
sites (Rood 1975, Laver and Alexander 2017). Den use is central to banded mongoose
breeding success and survival across landscape type. Multiple females will produce litters
at the same time and the young will stay in the natal den for about four to five weeks,
with one or two adults staying to guard the young while the rest of the troop forages
(Rood 1975, Cant 2003). Pups emerge from the den and start to accompany the rest of the
troop on foraging bouts at around four weeks of age, with both sexes helping to provision
the pups for up to eight weeks after emergence (Cant 2000). After foraging bouts, troop
38
members often reconvene around the den site entrance to rest, groom, scent mark, and
nurse the pups, while others engage in play behaviors (camera trap observations). Troops
relocate den sites every two to three days (Hiscocks and Perrin 1991), but have been
known to stay at the same den for longer periods (54 days in Rwenzori National Park,
Uganda (Rood 1975) and over two months in Queens Elizabeth National Park, Uganda
(Neal 1970)). Banded mongooses will often reuse den sites within their home range, with
our study troops in Northern Botswana averaging 30 unique dens sites (Laver and
Alexander 2017). Once a troop leaves one of their known den sites, they return to the
same den after a median of 106 days.
Understanding the impacts of anthropogenic change on banded mongoose ecology is
central to their management and can provide insight into the influence of land
transformation on wildlife behavior, space use, and disease transmission. We evaluate
banded mongoose den site use and attributes across anthropogenic and natural landscapes
and discuss implications to disease transmission in changing landscapes.
Methods
Study Site
Our study population is located in Chobe District, Northern Botswana (17.828°S and
25.163°E; See Figure 1). The human population for this area was estimated to be 13,141
in 2011 (2011 Botswana Population Census (Botswana Government 2015)). The urban
center of Kasane and the urban-transitioning village of Kazungula are experiencing
significant growth and development related to a growing tourism market. The urban
center of Kasane has a variety of hotels, lodges and camps, and an international airport.
39
Expansion and development has resulted in a loss of forest land, with around 3,060
hectares of the Kasane Forest Reserve degazetted for residential and developmental
purposes (Lepetu et al. 2010).
Figure 1: The study site in Chobe District, Northern Botswana with active banded
mongoose (Mungos mungo) den sites.
Banded Mongoose
We obtained den site characteristics from study troops across land use type (n=24, 2008-
2010 and 2016-2017, see below). Due to group fusion, extinction events, and other
influences, seven troops observed from 2008-2010 are not included in the 2016-2017 data
capture period. Briefly, within each troop, one or two banded mongooses were trapped
and fitted with radio collars, allowing troops to be located through the use of radio
telemetry. All methods were carried out in compliance with Virginia Tech IACUC
40
procedures (IACUC 13-164-FIW) and under a permit from the Botswana Ministry of
Environment, Natural Resources Conservation and Tourism (EWT 8/36/4 XXVI). Radio
collared troops were tracked five days a week, alternating seven troops on the first day
and the other eight troops the following, resulting in each troop being observed two to
three times a week (see Table 1). Once the den site was located, the GPS location,
mongoose troop, and den site characteristics were recorded and a remote sensing camera
was placed at the site (2016-2017 only).
41
Table 1: Study banded mongoose (Mungos mungo) troops used multiple land types
within their home ranges in Chobe District, Northern Botswana.
*Indicates the troops that were tracked during the 2008-2010 data period only.
42
Den sites were characterized by landscape features and mongoose troop characteristics
that were comprised of ten variables: land use, habitat, GIS land cover classification
building density, den type, level of land transformation, seasonal use, mortality density,
multiple troop use, and distance to road (Table 2). Land use was designated into five
different categories related to the nature of human influence on landscape structure:
urban, undeveloped/unprotected land areas, residential, lodge, and the national park.
Within each land class, the dominant habitat type and cover classes were identified as
previously described (See Table 2 for classifications (Child 1968, Weare and Yalala
1971, Mosugelo et al. 2002, Wolf 2009, Alexander and Vandewalle 2014, Fox et al.
2017)). Digitized data on building locations (2008, n = 5,641) was used to create a point
density surface using the density function in ArcGIS Spatial Analyst. The density
gradient raster values were classified into four categories with one being the lowest and
four the highest. This procedure calculates the density of point features around each
output raster cell. A circular neighborhood was defined around each raster cell center and
the number of points that fall within the neighborhood were totaled and divided by the
area of the neighborhood. To generate the distance between the den sites and the nearest
tar road, we used remote imagery for the area to digitize roads and used the proximity
analysis tool to obtain a distance measurement. Den structure was characterized by the
type as natural (termite mounds, bushes, hollow logs) or anthropogenic (slash piles,
buildings, building materials, concrete paths, drains, natural holes in the ground, rocks
and scrap heaps).
43
Table 2: The den site variables used to characterize banded mongoose den sites in
Northern Botswana.
Mongoose group size was excluded from the analysis as it varied considerably over the
study period by troop and was often unavailable by den night. Dens sites were
characterized by use (single or multiple troops) and by season (dry season, April-
October; wet season, November-March, or both). Mortality data were incorporated in a
similar manner as the building data above with the density gradient raster value classified
as low, medium, and high based on the standard deviation. This classification method
places class breaks around the mean based on the standard deviation.
44
Den Occupancy Assessment
To investigate the number of days a troop would occupy a den before relocating to a new
den site, we limited our evaluation to the data obtained from camera traps (2016-2017) as
this data set provided more robust information on nightly den use. Den occupancy data
was derived from camera traps as previously described in Chapter 2. Briefly, once a den
site was located, camera traps were placed in an optimal position to capture photographs
of banded mongooses at the den site. In the event that a troop relocated in the middle of
the night, if the departure was after midnight then that den night was still included in the
total den nights for that denning event.
Statistical Analysis
All statistical analyses were conducted in the open source integrated programming
environment RStudio Version 1.1.383. Fisher’s exact tests were used to test the
differences between anthropogenic and natural den structures and the period of their use
across study periods.
Exploratory data analysis: Cluster and CART:
Exploratory data analysis provides an opportunity to uncover underlying structure in a
data set and identify the most influential variables. Cluster analysis is a type of
exploratory data mining that attempts to group data in such a way that objects in the same
group (i.e. a cluster) are more similar to each other than other groups (clusters). The
package Cluster and specifically the Daisy algorithm were used for hierarchical cluster
analysis and creation of cluster dendrograms of den site variables (Table 2). The Gower’s
distance dissimilarity method was used as the linkage approach (Gower 1971). This
linkage method is able to handle different data types in the analysis (nominal, ordinal,
asymmetric binary, and interval scaled). We assessed several distance measures (i.e.
45
ward, single, average, complete, centroid, and mcquitty) and compared goodness of the
dendrogram fit with the dissimilarity matrix using both the Gower Distance Assessment
and Cophenitic Correlation (Borcard et al. 2011). The average distance measure provided
the best fit and the dendrogram was pruned using a clustering heat map (Pacheco 2015).
Further, using the sil_width function, the entire clustering was displayed by combining
the silhouettes (silhouette represents a cluster) into a single plot and the average
silhouette width provided a means to select the appropriate number of clusters
(Rousseeuw 1987). We used the rafalib package in R and the myplclust function to plot
the final dendrogram.
Recursive partitioning is a statistical approach for multivariable analysis used to create a
decision tree that splits objects into similar groups based on dichotomous independent
variables (Lemon et al. 2003). For this, we used classification and regression tree
(CART) analysis, a nonparametric decision tree method to evaluate associations between
land use and banded mongoose den sites. We used the rpart Package and the “class”
method to create the decision trees (Plaat et al.). Land use was set as the dependent
variable and we selected the lowest xerror (estimate of the cross-validation prediction
error) and the corresponding conditional probability (cp) in the rpart object to identify
the optimal level for pruning the resulting tree. The function as.party in the partykit
package in R were used to plot the final decision tree.
Results
Den site characteristics across the land use areas are provided in Table 3. The den types
were dominantly anthropogenic in nature in the human-modified land use areas (i.e.
46
buildings and scrap heaps) and natural structures in the remote national park (i.e. termite
mounds). The lodge land use areas provided pristine environments with intact gallery
forests. The urban, residential, and national park land use areas were slightly degraded
and the undeveloped areas were heavily degraded. Degraded riparian forests were
dominant in the urban, park, and undeveloped areas. Scrub savanna was prominent in
residential areas. Land cover for designated land areas is provided in Table 3. Mortality
was high in all of the land use areas with the exception of the National Park, however,
surveillance bias likely influenced this observation. Buildings were the highest in the
urban and residential areas and lowest in the National Park.
Table 3: Den site characteristics for study banded mongoose (Mungos mungo) troops in
Northern Botswana.
We also found that 6% (n=308) of mongoose den sites were used by multiple troops. All
of these dens were anthropogenic in nature with these dens more commonly found in the
urban and lodge land use designations. Communal dens were used on average for one to
three days and this pattern remained across the land use areas, between the wet and dry
seasons, and when pups were at the dens (see den occupancy, Table 2). When pups are
47
still too young to emerge from the den, adult mongooses carry the pups to the next den
site (camera trap observations).
Den site persistence
A total of 308 den sites were identified in the study site, of which 139 were in use during
2008-2010 (Laver 2013b), and 67 den sites were used repeatedly throughout both time
periods. Of those dens still in use by the 2016-2017 study period, the greater proportion
were anthropogenic in nature (94%, n= 67, p < 0.0001 by Fisher's exact test).
Cluster and classification and regression trees
The average distance metric provided the best fit to the dissimilarity matrix on both the
Gower Distance Assessment and Cophenetic Correlation. The cluster analysis of den site
characteristics identified four primary clusters (Figure 2). Den sites clustered according to
land type with the exception of the residential den sites, which grouped with the urban
dens.
48
Figure 2: Dendrogram of cluster analysis of den site data collected for study population
with clusters noted in color. The analysis identified four clusters: (1) national park, (2)
urban, (3) undeveloped, and (4) lodge areas. The residential dens group with the urban
dens.
CART analysis included all 308 den sites and identified three splits in the classification
tree (cp = 0.02) and was pruned accordingly (Figure 3). The classification tree indicated
that habitat, distance from tarred roads, and the type of den were the key variables
predicting banded mongoose den site by land use designation (Figure 3).
49
Figure 3: Decision tree from the CART analysis of cluster assignments.
Discussion
In our study, banded mongooses appear to be exceptionally plastic in their use of
communal den sites across land type, adapting to opportunities to maximize fitness needs
according to the land area and its characteristics (Table 3). Anthropogenic den structures
were commonly observed in human-modified landscapes (e.g. buildings, scrap heaps,
cement paths). In more natural settings, troops often utilized holes in the ground, termite
mounds, or snags, but these structures tended to degrade and disappear over the study
period.
A subset of den sites was regularly used by multiple troops, all of which were
anthropogenic in nature. These dens sites were dominantly located in the urban and lodge
land use areas. Banded mongooses are territorial and are known to defend their home
ranges vigorously, where intergroup encounters can result in mortalities (Cant et al. 2002,
50
Otali and Gilchrist 2004). Thus, these findings are particularly interesting and suggest
that anthropogenic landscapes may relax or reduce territorial defense or drive troops to
risk aggressive encounters in order to enter and stay within another troops territory to
access associated resource opportunities. Den sharing can have important implications for
pathogen transmission in this species allowing infected/susceptible individuals to have
indirect contact with environments that have potentially high levels of pathogen related to
marking behavior. The frequency of marking behaviors varies across the landscape but is
higher in the urban and lodge settings (Chapter 2). We do not currently know how long
M. mungi might survive in the environment, but M. bovis in environmental samples was
detected four to 21 months after possible contamination (Young et al. 2005). The anal
gland secretions fundamental in the transmission of M. mungi are highly lipid in nature
and depending on the den site, can be protected from desiccation for a considerable
period of time (Alexander et al. 2016). Deposition within the den would provide further
protection from pathogen degrading environmental forces (wind, rain, sunlight). Previous
studies in this system found that banded mongoose space use was strongly associated
with the degree of overlap with humans (Laver and Alexander 2017); as association with
humans increased, home range, core range, and space use dispersion decreased. Resource
acquisition (i.e. food, water) from the subsidized resources around the human settlements
might motivate different troops to utilize the same den sites in the urban and lodge areas,
amplifying disease transmission potential.
Across land type, den sites were consistently used for one to three nights before
mongoose relocated to another den. Relocating dens sites may decrease infestations by
51
ectoparasites, but it is unlikely that build up occurs within one to three days (Boydston et
al. 2006). Other social, diurnal Herpestidae species are known to relocate dens along a
similar time frame; dwarf mongooses (Helogale parvula) predominantly use a den for a
single night, moving to another den the following day (Hiscocks 1999). Meerkats
(Suricata suricatta) change burrows every two to three days, except when young are at
the dens (Clutton-Brock and Manser 2016). This is a short relocation time compared to
other larger communally denning species and may be related to forage limitations for
these smaller fossorial species. For example, clans of spotted hyenas (Crocuta crocuta)
can use a communal den for over a month (Périquet et al. 2016). However, aardwolves
(Proteles cristatus), an insectivorous Hyaenidae, relocates dens several times within a
month (Kotze et al. 2012).
Urban landscapes present novel predation risks and we recorded mortalities in our study
troops from a variety of human-mediated sources including vehicles, human conflict, and
predation by domestic animals. Direct eradication efforts from humans have been
observed when banded mongooses are perceived as pests (e.g., hot oil being poured into
active den sites, razor-wire placed in the entrance to den sites, shooting with a weapon,
and stoning). Research in Uganda also reported humans throwing rocks and adult
mongooses being killed by human inflicted burns (Otali and Gilchrist 2004). Domestic
dogs in our system commonly pursued and engage in aggressive interactions with study
banded mongoose troops, often resulting in mongoose fatalities (11%, n=188 deaths
recorded from 2008-2016).
52
Cluster and CART analysis of den sites
Cluster analysis identified land use type (national park, lodge, urban, and the
undeveloped areas) as the primary variable grouping communal den sites. This was not
true for den sites in residential areas, however, these sites appeared to share features
common across human modified land categories (Figure 3). CART analysis identified
three primary nodes: habitat, distance to the nearest tar road, and den type as the most
important predictors of den sites by land type (Figure 3).
The presence of gallery forests/riparian woodlands was most predictive of dens at lodge
facilities as compared to dens sites located in other land use types. Loss of riparian
ecosystems has been an in issue of increasing concern across Africa and the globe with
pressures that include invasive species (Holmes et al 2005), wood extraction, fire, and
increasingly in Southern Africa, complex interactions between elephant damage, lack of
recruitment, and declining water tables (Skarpe et al. 2004, Alexander and Vandewalle
2014, Nichols et al. 2017). Banded mongooses are not known to have an ecological
requirement for gallery forests and this association may simply be a characteristic of
lodge sites rather than a habitat feature important to banded mongoose fitness. These
riparian woodlands provide critical habitat to other species such as the Chobe bushbuck
(Tragelaphus scriptus ornatus) that has declined since the 1970s but populations still
persist in preserved habitat found at lodge sites (Addy 2016). While gallery forests are
under threat across the globe (Palmer et al. 2000), certain human transformed landscapes
may provide greater protection for these plant communities allowing them to persist
where they might otherwise be lost.
53
The distance from the tar road was the variable most predictive of den sites located
within the national park where infrastructural development is limited and only one tar
road traverses the region. Wildlife viewing from safari vehicles is common, but tracks are
not paved. The mongooses in this system den along the floodplains, which further
increases their distance from tar roads. Subsequently, the wildlife within this land use
area experiences the least exposure to human influences.
For undeveloped and urban land use areas, den site type (e.g. bush, hole in the ground,
building material) appeared to be the most important variable differentiating these land
areas. This tendency likely follows den site opportunities where natural den sites would
be more frequently found in the undeveloped land type and anthropogenic opportunities
provided in the urban landscape (See Figure 4 anthropogenic and natural den site
example).
54
Figure 4: Photograph of an anthropogenic and a natural den site utilized by banded
mongooses (Mungos mungo) in Northern Botswana. The photo on the left (A) is a drain
used by a study troop in the urban land use area. The photo on the right (B) is a termite
mound used by a study troop in an undeveloped area.
As human populations increase worldwide, the resulting habitat loss and degradation
often force animals to live in close proximity to humans (Woodroffe 2000). Banded
mongooses appear to be able to access suitable den sites across landscape type and
display behavioral flexibility in den site use, successfully taking advantage of
anthropogenically derived opportunities where these arise (Herr et al. 2010). The ability
to adapt to urban landscapes is variable among vertebrate species and predictive of urban
establishment. Some species, “urban avoiders” (Blair 2001), cannot adapt and persist
only in more natural settings. These species deliberately avoid areas near humans and
select shelter or den sites far from human influences (Theuerkauf et al. 2003, Elfström et
al. 2008). In contrast, “urban adapters” (Blair 2001) are able to live in close human
proximity exploiting non-seasonal food resources (e.g. waste, cultivated plants) and other
considerable behavioral plasticity, exploiting man-made structures for denning (Hwang et
al. 2007, Herr et al. 2010), many in close proximity to humans (Hwang et al. 2007,
Baldwin and Bender 2008). Banded mongooses should be considered urban adapters, as
they are able to take advantage of novel urban denning opportunities.
Though there are numerous species that thrive in urban environments, the wildlife in
these areas face novel selection pressures (Ditchkoff et al. 2006). The banded mongooses
in human-mediated areas have access to non-seasonal resources, but drawbacks such as
increased pathogen transmission associated with injury while foraging and invasion of
the novel pathogen M. mungi is presented in these environments (Flint et al. 2016). Here,
sharing of dens sites may also increase pathogen transmission in these same landscapes.
As urbanization pressures continue, it is clear that land use can have an important
influence on denning behavior in those species that can adapt to urban environments. The
use of these landscapes may have important implications for disease transmission and
pathogen persistence, and potentially, human and animal health.
Acknowledgments
We are grateful to Dr. Mark Vandewalle for logistical assistance and Dr. Claire
Sanderson for comments on earlier drafts. We would like to thank the dedicated
CARACAL team members and volunteers that contributed to data collection.
56
This project was supported by the National Science Foundation Ecology and Evolution of
Infectious Diseases (#1518663) and Morris Animal Foundation (#D14ZO- 083).
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Creeping in the night: what might ecologists be missing?
C.A. Nichols12¶ and K.A. Alexander12¶*
1 Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA, United
States of America
2 Centre for Conservation of African Resources, Animals, Communities, and Land use
This manuscript was formatted for and submitted to PLOS ONE
61
Abstract
Wildlife activity patterns tend to be defined by terms such as diurnal and nocturnal that
might not fully depict the complexity of a species’ life history strategy and behavior in a
given system. These activity pattern categories often influence the methodological
approaches employed, including the temporal period of study (daylight or nighttime). We
evaluated banded mongoose (Mungos mungo) behavior in Northern Botswana through
the use of remote sensing cameras at active den sites in order to characterize early
morning fear behavior for this diurnal species. Our approach, however, provided the
facility to capture unexpected nocturnal activity in a species that had otherwise only been
studied during daylight hours. Camera traps were deployed 215 trap days (24 hour data
capture period) at den sites, capturing 5,472 photos over all events. Nocturnal activity
was identified in 3% of trap days at study den sites. There was no association between the
occurrence of nocturnal activity and light availability from lunar phases (Fisher’s exact
test, n=215, p = 0.638) and thus, increased moonlight was not identified as a factor
influencing nocturnal space use. Nearly a third of nocturnal events were characterized as
fear behaviors (fleeing the den, relocation events, n=2/7). Drivers of nocturnal activity in
mongoose are uncertain but captured events have important implications for fear
behavior and space use during this activity period. Our findings highlight the need for
ecological studies to more explicitly address and evaluate the potential for temporal
variability in activity periods. Modifying our approach and embracing variation in
wildlife activity patterns might provide new insights into the interaction between
ecological phenomenon and species biology that spans the diurnal – nocturnal spectrum.
62
Introduction
The categorization of wildlife activity tends to be constrained to traditional day-night
niches, strictly classifying species as diurnal or nocturnal (Tattersall 1987, Curtis and
Rasmussen 2002, Hill 2006). Less frequently, the term crepuscular is used, since many
diurnal species are active at dawn and dusk as well as in full daylight (Ashby 1972).
Identification of more distinct adaptations to either a diurnal or nocturnal life history
strategy (e.g. larger orbits in nocturnal primate species improving night vision (Kay and
Kirk 2000)) may contribute to the tendency to strictly view species’ activity patterns as a
binary trait, rather than extending across a spectrum of temporal activity types (Tattersall
1987, Bearder et al. 2006). The characterization of a species to an activity pattern may
translate into a methodological approach where evaluation extending beyond the
dominant activity period is never attempted.
This more simplistic approach, however, was questioned in the 1970s with the
characterization of the activity patterns of the presumed diurnal Mayotte lemur (Lemur
fluvus mayottensis). This species was observed to apportion it’s behavior equally between
day and night periods (Tattersall 1979). As a consequence, the term cathemerality was
developed to capture this temporal activity type, adding to the previously established, and
mutually exclusive categories of nocturnal and diurnal. As a behavioral strategy,
cathemerality is thought to allow considerable advantages, identifying the ability for the
species to engage in diurnal and/or nocturnal activity periods in response to varying
ecological conditions (Hill 2006). Factors such as temperature, access to food resources,
and predation risk are all thought to be important in promoting cathemerality (Hill 2006).
63
At least eight species of Madagascar lemur exhibit cathemeral activity patterns (Schaik
and Kappeler 1996, Wright 1999, Curtis and Rasmussen 2002). This new term was
initially met with skepticism and even rejected by a reviewer in the peer review process
as it was considered to be “unnecessary new jargon” (Tattersall 1987). This initial
rejection illustrates the commitment to the notion that animal activity cycles can be
viewed as if they are a binary trait, rather than extending across a spectrum of temporal
activity types.
For the animals that restrict activity to day or night periods, the rare occurrences of
behavior ongoing in the other phases are considered unusual circumstances. Since these
events are considered unusual, the additional time and effort required to gain an
understanding of these occurrences are often disregarded. Regardless, it is evident that
expansion of activity into the night occurs in a number of species that are classified as
diurnal (e.g. over 70% of nocturnally vocalizing avian species were diurnal (La 2012),
nine West Indian diurnal lizards and one species of diurnal snake extending their activity
into the night around lights (Henderson and Powell 2001)). A prominent hypothesis for
diurnal species expanding activity into the night is that nighttime activity occurs due to
elevated light levels. Singing at night was typical of unmated northern mockingbirds
(Mimus polyglottos) and regularly occurred during full moon periods and less frequently
during other lunar phases (Derrickson 1988). For carnivores, more recent studies reveal
that nocturnal activity may be more pronounced than previously thought for traditionally
perceived diurnal species such as the African wild dog (Lycaon pictus (Cozzi et al. 2012,
Rasmussen and Macdonald 2012)) and cheetahs (Acinonyx jubatus (Cozzi et al. 2012)),
64
with nocturnal activity for both species comprising roughly 25% of their overall activity
budget (Cozzi et al. 2012). African wild dogs and cheetahs diurnal activities are thought
to arise as a temporal avoidance of stronger competitors, the lions (Panthera leo) and
hyenas (Crocuta crocuta), which are active at night (Cozzi et al. 2012). However,
nocturnal activity of both wild dogs and cheetahs fluctuated with the lunar cycle,
constrained to the brighter nights, suggesting that brighter moon phases might offset or
reduce potential costs of encountering stronger competitors and predators (Cozzi et al.
2012).
We used camera traps to systematically study fear behavior among banded mongooses
(Mungos mungo), a diurnal mesocarnivore (Rood 1975), at den sites in Northern
Botswana. Systematic studies of banded mongoose ecology and behavior had only been
undertaken during daylight hours (e.g. (Rood 1975, Cant et al. 2002, Jordan et al. 2010,
Jordan et al. 2011a, Jordan et al. 2011b, Jordan et al. 2011c, Fairbanks 2013a)). Here, we
report nocturnal activity for this presumed exclusively diurnal species. We aim to test
whether the detection of nocturnal activity patterns can be attributed to brighter lunar
phases and discuss our findings in the light of our current approach to activity pattern
classification and methodological approaches for ecological studies of wildlife.
Methods
Field methods
Remote sensing camera traps were deployed from January 4 to November 9, 2016, in
order to study banded mongoose behavior at the den sites of 17 troops located in our
long-term study site in Northern Botswana (Table 1). The study area covered the urban
65
areas of Kasane and Kazungula (defined as town e.g., tourist lodges, residential areas,
camp kitchens, farm land, and garbage sites) as well as natural habitats (defined as park
e.g., forest reserves and Chobe National Park). Animals were tracked through the
deployment of radio collars as previously described (Laver 2013b). Each radio collared
troop (n=15) was tracked five days a week alternating eight one day and seven the next.
Once the den site was located, camera traps were mounted on nearby fence posts, trees,
poles, and occasionally man-made stake mounts to obtain the optimal position for
photographing movement and behavior at the den site. While tracking the marked troops,
we also opportunistically placed cameras at den sites (n=2) that were identified but the
troops had not been fitted with a radio collar. A trap day was defined as a 24-hour
monitoring period of banded mongoose activity at the den site.
66
Table 1. The banded mongoose (M. mungo) troops sampled from January 4 - November
9, 2016. The individual study troops are listed with the general land class (i.e. park or
town) that they inhabited throughout the study period. The occurrence of nighttime
activity is documented for the troops that engaged in nighttime behavior along with the
month that the event took place.
67
The study was conducted under approval and in accordance with the guidelines of the
Virginia Tech Institutional Care and Use Committee (16-217-FIW) and under permit of
the Botswana Government.
Photo classifications and moon phase
The trap events were categorized as “day” or “night” according to the time stamp on the
photographs. The hours used to classify trap events were based on astronomical twilight.
Considering Botswana’s tropical location, sunrise and sunset do not drastically change
throughout the year. The days are slightly shorter in the winter months from May to
August. During the winter, the “day” length was 0500-2000, and accordingly, the “night”
photos include the times between 2000 and 0500. During the summer, the “day” photos
were lengthened to the hours between 0400 and 2100, and the “night” photos include the
times between 2100 and 0400. A trap event that contained photographs during the
nighttime hours is categorized as a “night” trap event. The trap events were then aligned
to the concomitant lunar phase classified into four categories (i.e. full, waning, waxing,
and new).
Data analysis
The proportion of nighttime activity was calculated as the number of trap days where
nighttime activity was identified over the total number of trap days. Due to the rare
occurrence of nocturnal activity, our approach is limited to evaluating nights with activity
regardless of some nights incorporating multiple observations from different troops.
Fisher’s exact test was used in RStudio (Version 0.99.484) to evaluate associations
between the trap nights with nighttime activity and variables of interest. Moonlight was
68
available during the waxing, waning, and full moon phases, so they were grouped as the
bright nights. The new moon phases were considered the dark nights.
Results
From January to November 2016, nighttime activity was identified for 3% of the trap
days (SD= 18%, n=7/215) and across five of the 11 months of the study. The nocturnal
activity occurred between 2000 and 2400 hours. The nighttime activity was observed in
29% of the troops (n =5/17 study troops, Table 1). There was no association between land
classification of the den site (town or park) and the occurrence of night activity (Fisher’s
exact test p=1). However, the limited number of park troops might have influenced our
ability to detect an effect.
Banded mongoose nighttime activity was seen across all moon phases with no significant
difference between the nights with no light (i.e. the new moon) and the phases (i.e. wane,
wax full) that did provide moonlight (Fisher’s exact test p=0.638).
Discussion
Like other social mongooses, banded mongooses are considered diurnal species (Veron et
al. 2004), and across studies ecological and behavioral investigations have been restricted
to daylight periods (Rood 1975, Cant et al. 2002, Jordan et al. 2010, Jordan et al. 2011a,
Jordan et al. 2011b, Jordan et al. 2011c, Fairbanks 2013a). However, this limited
temporal approach may fail to capture data critical to understanding the ecology and
temporal nature of space use for a species. Here, we identify important nocturnal
behavior and movement in banded mongooses. Unlike a number of other species,
nighttime activity was seen across both the brighter and darker moon phases and thus, did
69
not appear to be influenced by sufficient light. Our evaluation of fear behavior at den
sites identified both vigilant and non-vigilant behavioral states (See Chapter 2 for
Ethogram) across both diurnal and nocturnal activity periods with nocturnal vigilance
behavior restricted to fleeing and den relocation. The occurrence of vigilance behavior
followed by fleeing and den relocation was unique to nocturnal observations. Lack of
association with moon phase suggests other important ecological factors or stimuli are
encountered at night and influence nocturnal space use, and denning behavior and site
fidelity.
Nighttime predation forces diurnal species to engage in anti-predation behaviors. For
example, snake predations on avian nests results in females leaving the nest during the
night (Reidy et al. 2009). In addition to avoiding predation, there are other fitness
advantages to diurnal species engaging in nighttime movements. Although yellow
breasted chats (Icterina virens) are diurnal, both males and females are active and foray
outside of their territories at night. Fertile females foraying at night to engage in extrapair
copulations potentially allowing them to go undetected by their social mate (Ward et al.
2014). Brown bears (Ursus arctos) are primarily diurnal but forage equally between
daylight and darkness during salmon migrations with capture success increasing during
the night (Klinka and Reimchen 2002).
Photos from the cameras did not provide information as to what caused nocturnal vigilant
behavior. Fleeing behavior had previously only been reported in this species in
association with intergroup aggression events (Thompson et al. 2017). When collecting
70
the cameras for one of the nighttime evacuation events, the residents of the house that the
den site was located under reported that they had been woken up in the middle of the
night by a disturbance involving the mongoose. Another researcher studying the same
population found that a study troop at a lodge relocated dens during the night and a staff
member reported that lions entered the property that night. These vigilant responses may
hinder our ability to understand the influence of moonlight on nocturnal behavior for this
normally diurnal species, but further research may provide better insight.
For the nighttime photographs that banded mongooses were not responding to a threat,
there are one or two individuals engaging in activity instead of the entire troop. These
active individuals tend to be walking towards an active den site, and in one situation, an
individual appears to be investigating the den site. There is no evidence of emerging from
the den, so it is unclear if these individuals belong to the troop residing in the den. It is
possible that these individuals could be from a neighboring troop or dispersing
individuals. The advantages of these nocturnal movements remains unclear.
Clearly, nocturnal and diurnal data are necessary to fully understand den selection and
fidelity across a landscape. Restricting data collection for diurnal species to expected
daytime activity periods might hinder or limit our ability to gain further insight of the
biology and ecology of wildlife species. Limiting observations may also result in
erroneous conclusions when restricting data collection to a particular activity time. For
example, non-invasive fecal glucocorticoids are used to evaluate stress responses in
wildlife (Keay et al. 2006) and results are often interpreted in conjunction with behavioral
71
data collected during the same diurnal time period of collection or the diurnal period the
day before the collection (Wielebnowski and Watters 2007). Here, stress levels are
interpreted and aligned with observed daytime movements and behaviors when, in fact,
the stress response may reflect the occurrence of unobserved nocturnal events. Failure to
account for variation in activity periods might not only undermine study objectives, but
also the veracity of our understanding of a species’ ecology and behavior.
Considering that heterogeneity is a fundamental underlying phenomenon of ecology
(Scheiner and Willig 2011), temporal variation in activity patterns should be explicitly
accounted for in methodological approaches. Our observations of banded mongooses
illustrate the importance of including observations during low activity times when
studying a wildlife species. Initially, ecology assumed spatial homogeneity for
convenience and simplicity, with heterogeneity an unwelcome but necessary
complication (Pickett and Cadenasso 1995). Study approaches and theoretical
frameworks in the field of landscape ecology that have embraced heterogeneity and
complexity have provided new and critical insights into key ecological processes (e.g.
community dynamics or succession, the role of edges, patch dynamics)(Pickett and
Cadenasso 1995). A similar inclusion of heterogeneity into our consideration of activity
periods and associated behaviors is called for and will likely lead to a new era of
ecological discovery.
Acknowledgments
We thank the Government of Botswana’s Ministry of Environment Wildlife and Tourism,
and the Department of Wildlife and National Parks for their support for this project, and
72
the residents and business owners in Kasane and Kazungula for permitting research on
their properties. We are especially thankful to Dr. Mark Vandewalle for administrative
and logistical support. We are grateful to CARACAL staff for their hard work locating
active den sites and the volunteers at Virginia Tech and CARACAL that assisted with
reviewing photographs. We thank Dr. Claire Sanderson and Kelton Verble for comments
on earlier drafts.
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Conclusions
We identified interesting implications for disease pathogen transmission across landscape
type in Northern Botswana. The assessment of den site characteristics along the human-
wildlife interface exemplified the ability of banded mongooses to locate and utilize
human-subsidized resources for denning needs. The anthropogenic den sites used by
mongooses remain intact for much longer periods of time than natural dens. We also
identified locations where den sharing is ongoing in the human-mediated landscapes.
Both the lack of natural regeneration processes and therefore, continued use for
anthropogenic dens and den sharing likely have implications for pathogen transmission
both within and between troops.
We showed that the landscape influences wildlife behaviors in complex ways that can
influence pathogen transmission. Both the land use areas, vigilance behaviors, and the
interaction between the two explained the variation in the olfactory communication
behaviors that transmit M. mungi. Vigilance appears to be a stimulant for olfactory
communication when the threat is competition related, but a reducer when the threat is
predation related. However, there are situations when predation risks are inspected or
mobbed (e.g. snakes). Vigilance is a multifaceted behavior and its influence on olfactory
communication across the landscape reflects this. The intense competition between
neighboring troops of mongooses in areas with human-subsidized resources likely
promotes between-troop transmission.
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Our use of remote sensing camera traps allowed us to study nighttime behavior, which
had not been previously documented for this species. The categorization of a species as
diurnal or nocturnal usually limits behavior observations to the hours of dominant activity
periods. However, though rare, these events can have substantial influences on ecological
interactions and should be accounted for in methodologies, especially when applicable to
study questions and objectives.
As numerous species begin to utilize anthropogenic landscapes, these fundamental
changes in behavior and life history attributes should be taken into consideration for
conservation and management purposes. We have shown the implications of behavioral
changes across the landscape on disease transmission dynamics, but it is likely that
additional interactions are affected as well. Future studies should focus on refining our
understanding of sickness behavior on pathogen shedding. Additional focus on the period
of pathogen shedding will be important as we seek to refine computational models and
outbreak prediction capacity.
Appendix
Supplementary Table 1: The wildlife species captured in camera trap photographs at
