Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus)

Abstract

Hendra virus (HeV) is a lethal paramyxovirus which emerged in humans in 1994. Poor understanding of HeV dynamics in Pteropus spp. (flying fox or fruit bat) reservoir hosts has limited our ability to determine factors driving its emergence. We initiated a longitudinal field study of HeV in little red flying foxes (LRFF; Pteropus scapulatus) and examined individual and population risk factors for infection, to determine probable modes of intraspecific transmission. We also investigated whether seasonal changes in host behaviour, physiology and demography affect host-pathogen dynamics. Data showed that pregnant and lactating females had significantly higher risk of infection, which may explain previously observed temporal associations between HeV outbreaks and flying fox birthing periods. Age-specific seroprevalence curves generated from field data imply that HeV is transmitted horizontally via faeces, urine or saliva. Rapidly declining seroprevalence between two field seasons suggests that immunity wanes faster in LRFF than in other flying fox species, and highlights the potentially critical role of this species in interspecific viral persistence. The highest seroprevalence was observed when animals showed evidence of nutritional stress, suggesting that environmental processes that alter flying fox food sources, such as habitat loss and climate change, may increase HeV infection and transmission. These insights into the ecology of HeV in flying fox populations suggest causal links between anthropogenic environmental change and HeV emergence.

Figure 1

Field sites where LRFF were captured in the Northern Territory of Australia: Katherine Gorge National Park; Northern Territory (NT) Rural College; Flora River Nature Park; Elsey National Park; Litchfield National Park; and Katherine River.

Figure 2

Patterns of HeV seroprevalence in relation to age and size. (a) Age-specific HeV seroprevalence as determined by criteria in table 1: animals less than one month old were all seropositive (n=8), reflecting the serostatus of their mothers, which were also all seropositive. Error bars represent 95% binomial CIs. (b) Relationship between forearm length (for animals with forearm length≥124 mm) and HeV seroprevalence. The risk of HeV infection increases with body size. Animals with a forearm length of above 130 mm were all mature animals. Error bars represent 95% binomial CIs. A, 125–130; B, 131–135; C, 136–140; D, 141–145; E, 146–150; F, 151–155; G, 156–160. (c) Age distribution of animals from which teeth were analysed.

Figure 3

HeV seroprevalence as a function of reproductive status and season. (a) Seroprevalence across reproductive classes in autumn 2005 (preg, pregnant; lact, lactating; not preg/lact, not pregnant or lactating). (b) Overall seroprevalence across seasons (Spr04, spring 2004; Aut05, autumn 2005; Win05, winter 2005; Spr05, spring 2005; Aut06, autumn 2006). Error bars represent 95% binomial CIs.

Figure 4

Relationship between seroprevalence and body condition (weight/forearm ratio). Points represent mean seroprevalence per field season as a function of mean body weight/forearm ratio for adult non-pregnant females (squares and solid line) and adult males (diamonds and dashed line). Dividing body weight by forearm measurement accounts for body size and therefore gives a crude measurement of body condition. 1, spring 2004; 2, autumn 2005; 3, winter 2005; 4, spring 2005; 5, autumn 2006.

Figure 5

Variance in HeV seroprevalence over five field seasons in LRFF compared with variance in HeV seroprevalence over five field seasons in a Northern Queensland population of spectacled flying foxes (A. C. Breed 2005–2006, unpublished data).