Introduction and purpose
Growing concern about the
emergence of zoonotic infectious diseases has stimulated research into
the dynamics and drivers of infection in wildlife reservoir hosts (Patz
et al. 2004; Jones et al. 2008). Understanding factors that drive the
magnitude and timing of epidemics – and which allow for the long-term
persistence of pathogens – in animal host populations is of particular
importance to the prediction and prevention of zoonotic spillover into
humans (Plowright and Hudson 2021). Investigations into how ecological
features shape infection is achieved through empirical and theoretical
research at the interface of ecology and wildlife epidemiology (e.g.,
Peel et al. 2014; Lunn et al. 2021; Mancy et al. 2022). The availability
of key ecological information on wildlife reservoir hosts is fundamental
to these research efforts, yet even basic information is lacking for
many wildlife species in global hotspots of infectious disease emergence
(Kuzmin et al. 2011).
Seasonal birthing is a common ecological feature of wildlife species,
and is thought to play a key role in the infection dynamics of
populations via the addition of susceptible individuals (Peel et al.
2014; Plowright et al. 2016; Baker et al. 2020). At its simplest, the
seasonal addition of naïve juveniles increases the proportion of
contacts between susceptible and infected individuals, increasing the
rate of transmission during and following the birthing period, thereby
driving seasonal epidemic cycles (Peel et al. 2014). Ecological
attributes of seasonal birthing, as well as other host and pathogen
features such as population size and infectious period, shape variation
in this dynamic host-pathogen relationship.
Synchronicity of birthing (the time period over which birthing occurs),
and the number of birth pulses per year, are key drivers for the
magnitude of epidemic cycles and contribute to the probability of
pathogen extinction from a population. More synchronous birth pulses
(the same number of births over a shorter time) can drive pathogen
extinction by creating large amplitude oscillations in epidemics (i.e.,
high peaks, low troughs), which increase the probability of
stochastic fade-out during
troughs in the epidemic cycle (Peel et al. 2014). This is exacerbated by
short infectious periods and high demographic turnover, and increases
the population size required for pathogen persistence (Peel et al. 2014;
Hayman 2015). Meanwhile, having more birth pulses per year can increase
the likelihood of pathogen persistence by decreasing the amplitude of
oscillations (i.e., lower peaks, higher troughs), meaning the number of
infected individuals does not drop as low between birth pulses, and the
risk of pathogen extinction via stochastic fade-out is reduced (Hayman
2015).
Modelling has shown that bi-annual birth pulses may be needed for the
persistence of filoviruses (including Ebolavirus sp. andMarburgvirus sp.) in bat populations, and that persistence –
even with bi-annual birthing – is sensitive to birth synchrony and
host/virus attributes (Hayman 2015). Persistence of filoviruses is more
likely when birth synchronicity is low, when the incubation or
infectious periods are long, and when population sizes are large (Hayman
2015). These findings highlight ecological conditions under which
sustained transmission of ebola- and marburgviruses may be possible and
identify key traits of reservoir hosts. However, these results pertain
to generic bat populations with fruit bat-like ecological traits (based
on the African fruit bats, Eidolon helvum and Rousettus
aegyptiacus ), and are not necessarily applicable to other possible
hosts of ebolaviruses, including insectivorous bats (Hayman 2015;
Leendertz et al. 2016). Species-specific investigations into plausible
reservoir hosts, especially for ebolaviruses, remain limited by deficits
in information on bat ecology. The synchronicity of birthing – in
particular – is unknown for most bat species and warrants further
attention (Kuzmin et al. 2011; Hayman 2015).
The Angolan free-tailed bat (Molossidae: Mops condylurus ) has
been implicated as a reservoir host for ebolaviruses. Wild-caughtM. condylurus have tested positive for ebolavirus antibodies (De
Nys et al. 2018), and demonstrate the ability to replicate and shed
ebolaviruses following experimental inoculation, with little evidence of
virus-induced morbidity (Swanepoel et al. 1996; Edenborough et al.
2019). More recently, this species has been associated with a new
ebolavirus, Bombali virus, with detection of viral RNA in wild-caught
bats from five distinct locations across their range (Sierra Leone,
Guinea, two locations in Kenya, and Mozambique) (Goldstein et al. 2018;
Forbes et al. 2019; Karan et al. 2019; Kareinen et al. 2020;
Lebarbenchon et al. 2022). Bombali virus RNA has also been detected from
a closely related co-roosting species, Mops pumilus (Goldstein et
al. 2018).
Birth-pulse synchronicity and magnitude have not been estimated forM. condylurus or M. pumilus , despite the pertinence of
this information to understanding infection dynamics. The temporal
resolution of existing research – at best, singular capture events once
per month – is insufficient to accurately estimate the spans of most
reproductive states (Mutere 1973; O’Shea and Vaughan 1980; Happold and
Happold 1989; Vivier and Van Der Merwe 1996; Vivier and Merwe 1997).
Gestation and lactation periods have been estimated from patchy data, at
roughly 85 days and 50-60 days respectively for M. condylurus ,
and 67-72 days and 21-28 days for M. pumilus (McWilliam 1976;
Happold and Happold 1989; Vivier and Merwe 1997). Female M.
condylurus show bi-annual birthing across their range, and M.
pumilus up to penta-annual birthing depending on latitude (Happold and
Happold 1989). Both species have a post-partum oestrus, where bats can
be detected lactating and gestating simultaneously (Happold and Happold
1989).
Given current gaps in knowledge, and the importance of detailed
reproductive information for investigating viral maintenance, the
purpose of this study was to empirically characterise key parameters of
the birth pulse in M. condylurus and M. pumilus bats.
Specifically, we investigated the timing, synchronicity, and magnitude
of the birth pulse in south-eastern Kenya where Bombali virus has
previously been detected (Forbes et al. 2019; Kareinen et al. 2020).