Parasite spillback: A neglected concept in invasion ecology?

Abstract

While there is good evidence linking animal introductions to impacts on native communities via disease emergence, our understanding of how such impacts occur is incomplete. Invasion ecologists have focused on the disease risks to native communities through "spillover" of infectious agents introduced with nonindigenous hosts, while overlooking a potentially more common mechanism of impact, that of "parasite spillback." We hypothesize that parasite spillback could occur when a nonindigenous species is a competent host for a native parasite, with the presence of the additional host increasing disease impacts in native species. Despite its lack of formalization in all recent reviews of the role of parasites in species introductions, aspects of the invasion process actually favor parasite spillback over spillover. We specifically review the animal-parasite literature and show that native species (arthropods, parasitoids, protozoa, and helminths) account for 67% of the parasite fauna of nonindigenous animals from a range of taxonomic groups. We show that nonindigenous species can be highly competent hosts for such parasites and provide evidence that infection by native parasites does spillback from nonindigenous species to native host species, with effects at both the host individual and population scale. We conclude by calling for greater recognition of parasite spillback as a potential threat to native species, discuss possible reasons for its neglect by invasion ecologists, and identify future research directions.

Parasite spillover: indirect effects of invasive Burmese pythons

“…This parasite is native to viperid snakes of North and South America (Riley & Self, 1979), and its presence in invasive Burmese pythons introduces the potential that pythons could negatively impact native pit vipers through parasite spillback (Kelly et al., 2009a). The intermediate hosts of P. crotali are primarily small rodents (Christoffersen & De Assis, 2013) including the hispid cotton rat ( Sigmodon hispidus ), Florida mouse ( Peromyscus floridana ), rice rat ( Oryzomys palustris ), and cotton mouse ( Peromyscus gossypinus ) (Kinsella, 1974; Layne, 1967).…”

“…Nonindigenous species may also acquire parasites from their introduced range (Cornell & Hawkins, 1993; Dobson & May, 1986; Kelly, Paterson, Townsend, Poulin, & Tompkins, 2009a; Poulin & Mouillot, 2003), and in many cases, a majority of parasites infecting NIS are native to the invaded range (Torchin & Mitchell, 2004). If NIS are competent hosts (i.e., parasites are capable of establishment, survival, and reproduction within the host) of native parasites, then NIS may serve as reservoirs of indigenous parasites and increase infection in sympatric native hosts through parasite spillback (Daszak et al., 2000; Kelly et al., 2009a; Tompkins & Poulin, 2006).…”

“…If NIS are competent hosts (i.e., parasites are capable of establishment, survival, and reproduction within the host) of native parasites, then NIS may serve as reservoirs of indigenous parasites and increase infection in sympatric native hosts through parasite spillback (Daszak et al., 2000; Kelly et al., 2009a; Tompkins & Poulin, 2006). Aside from direct effects on host mortality, increased transmission can adversely affect competitive interactions and increase vulnerability to predation, resulting in host population declines and altered community structure (Settle & Wilson, 1990; Tompkins, Draycott, & Hudson, 2000; Tompkins, Greenman, & Hudson, 2001).…”

Diversity and host specificity of coccidia (Apicomplexa: Eimeriidae) in native and introduced squirrel species

“…Parasites may play a role in biological invasions via three main mechanisms: (i) invaders may lose some of their parasites during translocation, leading to a competitive advantage (Torchin et al 2003); (ii) invaders may serve as complementary hosts for local parasites, leading to spillback process or dilution effect, depending on their competence as hosts (Kelly et al 2009); (iii) invaders may introduce with them new parasites, which may spill over to native hosts (Dubey and Shine 2008;Paterson and Gray 1997). Although majority of parasites are host-specific (Pizzatto and Shine 2011;Poulin 2007), a range of examples of successful invasion (i. a. avian malaria to Hawaii, Fascioloides magna to Europe, spreading of chytridiomycosis in amphibian populations) suggests that the interspecific transmission of parasites can be more frequent than expected (Atkinson et al 2014;Marzal et al 2015; a total of 540 faecal samples from 466 animals (S. vulgaris 206 samples/143 individuals, S. carolinensis 164/164, C. erythraeus 170/159), some individuals were screened repeatedly.…”

Recolonizing gray wolves increase parasite infection risk in their prey

“…“Wolf‐specialized” parasites should then be overrepresented in wolves and show the strongest prevalence increase in ungulate intermediate hosts in wolf‐inhabited areas, and there should be a “mismatch” in relative parasite frequencies between wolves and their prey. Under the “host flexibility” hypothesis, returning wolves serve as an additional definitive host for endemic parasites also spread by other carnivores (spillback) which had resumed the function of alternative hosts (Kelly, Paterson, Townsend, Poulin, & Tompkins, 2009; Moré, Maksimov, Conraths, & Schares, 2016). In this case, we would not expect to find Sarcocystis species that could be considered “wolf specialists”.…”