Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa

Abstract

Populations of large wildlife are declining on local and global scales. The impacts of this pulse of size-selective defaunation include cascading changes to smaller animals, particularly rodents, and alteration of many ecosystem processes and services, potentially involving changes to prevalence and transmission of zoonotic disease. Understanding linkages between biodiversity loss and zoonotic disease is important for both public health and nature conservation programs, and has been a source of much recent scientific debate. In the case of rodent-borne zoonoses, there is strong conceptual support, but limited empirical evidence, for the hypothesis that defaunation, the loss of large wildlife, increases zoonotic disease risk by directly or indirectly releasing controls on rodent density. We tested this hypothesis by experimentally excluding large wildlife from a savanna ecosystem in East Africa, and examining changes in prevalence and abundance of Bartonella spp. infection in rodents and their flea vectors. We found no effect of wildlife removal on per capita prevalence of Bartonella infection in either rodents or fleas. However, because rodent and, consequently, flea abundance doubled following experimental defaunation, the density of infected hosts and infected fleas was roughly twofold higher in sites where large wildlife was absent. Thus, defaunation represents an elevated risk in Bartonella transmission to humans (bartonellosis). Our results (i) provide experimental evidence of large wildlife defaunation increasing landscape-level disease prevalence, (ii) highlight the importance of susceptible host regulation pathways and host/vector density responses in biodiversity-disease relationships, and (iii) suggest that rodent-borne disease responses to large wildlife loss may represent an important context where this relationship is largely negative.

Keywords: Kenya; dilution effect.

Fig. 1.

Working in the KLEE, which examines the effect of large wildlife (e.g., zebra, giraffe, elephant, gazelle) removal (A), we found that S. mearnsi abundance was significantly higher (roughly double on average) in plots where large mammals had been removed compared with open plots (B) despite strong seasonal variability. (C) There was no significant difference in the intensity of infestation of fleas per rodent between treatments. (D) As a result, the density of fleas per hectare is significantly higher (roughly double) in plots without large wildlife. Error lines represent 1 SE, based on three replicate blocks. Data for all rodents are shown in Fig. S1. Photography credits: A, KLEE exclosure, D. Kimuyu (Equus quagga, Nanyuki, Kenya); Inset of flea in C and D X. sarodes sarodes (male), M. Hastriter and Michael Whiting, Monte L. Bean Museum, Brigham Young University, Provo, UT.

Fig. 2.

(A) Rodent diversity (Shannon diversity index ± SE, across plots within a season) was not significantly different between treatments with and without large mammalian wildlife. (B) There were also no significant differences in community similarity between experimental plots (animals pooled across sampling seasons). Species codes are as follows: ACKE, Acomys kempi; AEKA, Aethomys kaiseri Arvicanthis niloticus; DEME, Dendromus melanotis; MANA, Mastomys natalensis; MUAC, Mus cf. acholi; MUMI, Mus minutoides; MUSO, Mus sorella; MUTE, Mus tenellus; SAME, S. mearnsi; ZEHI, Zelotomys hildegardeae.

Fig. 3.

There was no significant overall difference in the prevalence of Bartonella spp. infection either in the dominant rodent S. mearnsi or in the fleas of S. mearnsi (A) between control and large wildlife removal treatments. However, because of increased abundance of S. mearnsi in sites without large wildlife, there was a significant increase in the abundance of infected S. mearnsi (B) and infected vectors (C) in these simulated large wildlife loss treatments. Error lines represent 1 SE, based on three replicate blocks. Data is qualitatively similar when considering all rodents (Fig. S3).