Ectoparasite extinction in simplified lizard assemblages during experimental island invasion

Abstract

Introduced species can become invasive, damaging ecosystems and disrupting economies through explosive population growth. One mechanism underlying population expansion in invasive populations is 'enemy release', whereby the invader experiences relaxation of agonistic interactions with other species, including parasites. However, direct observational evidence of release from parasitism during invasion is rare. We mimicked the early stages of invasion by experimentally translocating populations of mite-parasitized slender anole lizards (Anolis apletophallus) to islands that varied in the number of native anoles. Two islands were anole-free prior to the introduction, whereas a third island had a resident population of Gaige's anole (Anolis gaigei). We then characterized changes in trombiculid mite parasitism over multiple generations post-introduction. We found that mites rapidly went extinct on one-species islands, but that lizards introduced to the two-species island retained mites. After three generations, the two-species island had the highest total density and biomass of lizards, but the lowest density of the introduced species, implying that the 'invasion' had been less successful. This field-transplant study suggests that native species can be 'enemy reservoirs' that facilitate co-colonization of ectoparasites with the invasive host. Broadly, these results indicate that the presence of intact and diverse native communities may help to curb invasiveness.

Keywords: Anolis; anole; ectoparasite; enemy release hypothesis; invasion biology; invasive species.

Figure 1.

Changes in the number of mites within and among generations for populations and individual founder lizards. (a) Slender anole (Anolis apletophallus) and Gaige's anole (A. gaigei). Photos by John David Curlis. Total number of mites on slender anole lizards for the mainland (b), islands with one species (c,d) and two species (e) in the founding generation (F₀) and two successive generations (F₁ and F₂). Lines indicate medians and range. Mites disappeared from all lizards on one-species islands (a,b) but persisted for three generations on the two-species island (c). (f) Initial and final numbers of mites in individual founder lizards that persisted on islands for multiple years (each line represents an individual lizard). Founding individuals invariably lost all mites on one-species islands but retained or gained mites on the two-species island.

Figure 2.

Density and biomass of lizards on each island, as well body size and parasitism of Gaige's anoles. Density of lizards (a) and lizard biomass (b) on islands, based on mark recapture over three lizard generations. Mites persisted only on a two-species island with high total lizard density and biomass per unit area. (c) Body length and body mass of slender and Gaige's anoles on the two-species island (island D), the island where mites persisted. Symbols indicate mean ± SEM. (d) Intensity of mite infection on the source (mainland) population of slender anoles, and both slender and Gaige's anoles on island D. Lines indicate median and range. Gaige's anoles, which are longer and heavier than slender anoles, had significantly higher intensity of parasitism than slender anoles from the mainland, suggesting that they may have served as a reservoir of parasitism during the slender anole invasion.