Behavior of the Avian Parasite Philornis downsi (Diptera: Muscidae) in and Near Host Nests in the Galapagos Islands

J Insect Behav https://doi.org/10.1007/s10905-021-09789-7 Behavior of the Avian Parasite Philornis downsi (Diptera: Muscidae) in and Near Host Nests in the Galapagos Islands Courtney L. Pike · Ismael E. Ramirez · David J. Anchundia · Birgit Fessl · George E. Heimpel · Charlotte E. Causton Received: 6 January 2021 / Revised: 22 October 2021 / Accepted: 29 October 2021 © The Author(s) 2021 Abstract The Avian Vampire Fly, Philornis downsi, has invaded the Galapagos Islands, where it causes high mortality of endemic and native landbird species, including most species of Darwin’s finches. Control methods are under development, but key information is missing about the reproductive biology of P. downsi and the behavior of flies in and near nests of their hosts. We used external and internal nest cameras to record the behavior of P. downsi adults within and outside nests of the Galapagos Flycatcher, Myiarchus magnirostris, throughout all stages of the nesting cycle. These recordings showed that P. downsi visited flycatcher nests throughout the day with higher fly activity during the nestling phase during vespertine hours. The observations also revealed that multiple P. downsi individuals can visit nests concurrently, and that there are some interactions among these flies Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s10905-021-09789-7. C. L. Pike · D. J. Anchundia · B. Fessl · C. E. Causton Charles Darwin Research Station, Charles Darwin Foundation, Puerto Ayora, Santa Cruz, Ecuador C. L. Pike (*) · D. J. Anchundia Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Vienna, Austria e-mail: I. E. Ramirez · G. E. Heimpel Department of Entomology, University of Minnesota, St. Paul, MN, USA within the nest. Fly visitation to nests occurred significantly more often while parent birds were away from the nest than in the nest, and this timing appears to be a strategy to avoid predation by parent birds. We report fly mating behavior outside the nest but not in the nest cavity. We discuss the relevance of these findings for the adaptive forces shaping P. downsi life history strategies as well as rearing and control measures. Keywords Insect behavior · Ectoparasite · Invasive species · Nest visitation · Life history · Host-parasite interactions Introduction Island ecosystems are increasingly challenged by invasive species that have been introduced by humans (Simberloff 2010; Bellard et al. 2017; Spatz et al. 2017; Lenzner et al. 2020). These invasive species threaten the health and survival of often naïve endemic species through interactions such as predation, competition, parasitism, or as vectors of parasites and pathogens (Causton et al. 2006; Reaser et al. 2007; Blackburn and Ewen 2016; Russel et al. 2017). While there is extensive research on the impacts attributed to alien plants and vertebrates (Medina et al. 2011; Pyšek et al. 2012; Spatz et al. 2017), less is known about introduced parasites and how they interact with biodiversity in these novel environments Vol.:(0123456789) 13 J Insect Behav and what makes them successful invaders (Poulin 2017). At least 499 species of insects have been introduced to and established in the Galapagos Islands, including 35 species that are parasitic on animals or plants, and additional surveys will likely reveal more (Toral-Granda et al. 2017). One of the most devastating introduced insects is the Avian Vampire Fly, Philornis downsi, a muscid whose larvae are ectoparasites of nestling birds (Fessl and Tebbich 2002). While the first report of P. downsi in bird nests occurred in 1997 (Fessl et al. 2001), records in museums date back to the 1960 s (Causton et al. 2006; Fessl et al. 2018). This fly is native to mainland South America and Trinidad (Bulgarella et al. 2015; Fessl et al. 2018; Koop et al. 2020), but it now also has a widespread distribution and broad host range in Galapagos, infesting nests of at least 21 small landbird species (Fessl, et al. 2018; Anchundia and Fessl 2020; Coloma et al. 2020). The introduction of this parasite has been highly detrimental to the reproductive success of small Galapagos landbirds, including various species of Darwin’s finches (Kleindorfer and Dudaniec 2016; Koop et al. 2016; Fessl et al. 2018; McNew and Clayton 2018). Indeed, P. downsi is now regarded as a leading causal factor in the observed population declines of passerine species in Galapagos, and, as such, it is a priority for conservation organizations to develop tools for its management (Cunninghame et al. 2012; Causton et al. 2013). Control options that are being evaluated include insecticidal treatment of nests and trapping as stop-gap methods and biological control and the Sterile Insect Technique as long-term options (Knutie et al. 2014; Heimpel 2017; Bulgarella et al. 2017; Fessl et al. 2018; Boulton et al. 2019; Bulgarella et al. 2020; Ramirez et al. Accepted). The behaviors exhibited by P. downsi in and around nests of its hosts have implications for the development of control strategies for this fly and prior studies have provided information on nest-associated behaviors and interactions. Video recordings from within the nests of three species of Darwin’s finches from 2008 revealed that adult P. downsi visit nests during the incubation and nestling phases of bird development (both during the day and night), and may typically occur when adult birds are absent (O’Connor et al. 2010). These observations also revealed that adult P. downsi tend to oviposit on nest 13 material near nestlings and that larval feeding is primarily nocturnal. Other observations of P. downsi behavior outside of an active nest of the Galapagos Flycatcher, Myiarchus magnirostris, showed that adult flies landed outside the nest and walked into it once a parent flycatcher had exited the nest (Lincango et al. 2015). Some use of defense strategies by parents or nestlings against P. downsi has been documented in Darwin’s finches, including preening of P. downsi larvae by nestlings or female parents, and antibody production against P. downsi by female parents (Huber et al. 2010). However, these appear to do little to protect nestlings from larval feeding by this parasite (O’Connor et al. 2010; Koop et al. 2013). Despite these advances, there are still considerable gaps in our knowledge about how and when P. downsi adults locate and interact with their bird hosts. Furthermore, nothing is known about the courtship and mating behavior of P. downsi. In this study, we observed active nests of the Galapagos Flycatcher in artificial structures as a means of obtaining additional information on the behavior of P. downsi and its host inside and outside host nests. We also provide the first data on the interactions between P. downsi and its host over the entire bird developmental cycle – from incubation to fledging. Our main aims were to determine (i) if P. downsi preferentially v (...truncated)