Urbanization and translocation disrupt the relationship between host density and parasite abundance

Abstract

The species interactions that structure natural communities are increasingly disrupted by radical habitat change resulting from the widespread processes of urbanization and species translocations. Although many species are disadvantaged by these changes, others thrive in these new environments, achieving densities that exceed those in natural habitats. Often the same species that benefit from urbanization are successful invaders in introduced habitats, suggesting that similar processes promote these species in both environments. Both processes may especially benefit certain species by modifying their interactions with harmful parasites (‘enemy release’). To detect such modifications, we first need to identify the mechanisms underlying host–parasite associations in natural populations, then test whether they are disrupted in cities and introduced habitats. We studied the interaction between the cane toad Rhinella marina, a globally invasive species native to South America, and its Amblyomma ticks. Our field study of 642 cane toads across 46 sites within their native range in French Guiana revealed that 56% of toads carried ticks, and that toads with ticks were in poor body condition relative to uninfected conspecifics. Across natural and disturbed habitats tick prevalence and abundance increased with toad density, but this association was disrupted in the urban environment, where tick abundance remained low even where toad densities were high, and prevalence decreased with density. Reductions in the abundance of ticks in urban habitats may be attributable to pesticides (which are sprayed for mosquito control but are also lethal to ticks), and our literature review shows that tick abundance is generally lower in cane toads from urban habitats across South America. In the invasive range, ticks were either absent (in 1,960 toads from Puerto Rico, Hawai'i, Japan and Australia) or less abundant (in Florida and the Caribbean; literature review). The positive relationship between host density and parasite abundance is thought to be a key mechanism through which parasites regulate host populations; anthropogenic processes that disrupt this relationship may allow populations in urban and introduced habitats to persist at densities that would otherwise lead to severe impacts from parasites.

Spatial ecology of cane toads (Rhinella marina) in their native range: a radiotelemetric study from French Guiana

“…In addition, although breeding occurs year-round, influxes of toads to French Guiana breeding sites occurred in December, indicating that toads may be more mobile during the wet season. This reliance on limited freshwater resources during the drier months may also explain why toads lived at such high densities at coastal sites, despite the fact that these dense populations suffered from high levels of parasitism as a result 40 . Limited rainfall during the tracking period may therefore have restricted toad movements, especially at coastal sites, where seasonality is more pronounced and water availability was limited.…”

“…Our study of native-range toads has shown great flexibility in movement patterns in response to local conditions. Toads in the native range exploit a wide range of habitats, including beach and rainforest sites otherwise typified by profoundly disparate faunal groups, exhibiting a level of habitat generalism that likely facilitated this toad’s success and subsequent colonization of a wide range of habitats in their introduced range 40 , 62 , 64 . Native-range toads also exhibited strong behavioural plasticity in response to environmental conditions and utilized different strategies to exploit available resources in different habitats; such plasticity may also increase performance in species invading novel environments 65 , 66 .…”

“…In French Guiana > 95% of the land area is forested, but cane toads occupy a range of habitat types from dense rainforest to coastal beaches 40 . To include that variation, we tracked toads at two sites in coastal beach habitats (Fig.…”

“…Behaviour can also be state-dependent; for example, body condition can influence foraging decisions 43 . To calculate the body condition of the tracked toads we obtained body mass (g) and SVL (mm) data from 142 male and 98 female toads from across northern French Guiana 40 . Using these data we calculated sex-specific relationships between mass and SVL by plotting ln(mass) against ln(SVL).…”

Discovery of Novel Viruses Associated With the Invasive Cane Toad (Rhinella marina) in Its Native and Introduced Ranges

“…Collection of Australian cane toads took place between May 2014 and December 2018 in the Northern Territory (NT; n =7 toads), Queensland (QLD; n =51), and Western Australia (WA; n =49; Supplementary Table S1 ). Between August and November 2017, French Guianese toads were collected near Regina and St. George ( Supplementary Table S1 ; DeVore et al, 2020 ). Hawai’ian cane toads ( n =10) were collected from two regions on the island of O’ahu in June 2015 ( Supplementary Table S1 ).…”