DOI: 10.7589/2015-01-025 Journal of Wildlife Diseases, 51(4), 2015, pp. 907–910 # Wildlife Disease Association 2015

Interactions between the Avian Parasite, downsi (Diptera: ) and the Galapagos Flycatcher, Myiarchus magnirostris Gould (Passeriformes: Tyrannidae)

Piedad Lincango,1,3 Charlotte Causton,1 Daniel Ceden˜o,1 Johanna Castan˜ eda,1 Alexandra Hillstrom,2 and Deborah Freund21Charles Darwin Foundation, Puerto Ayora, Santa Cruz Island, Galapagos Islands, Ecuador 200350; 2Biology Department, University of Wisconsin–Eau Claire, 342 Phillips Hall, Eau Claire, Wisconsin 54702-4004, USA; 3Corresponding author (email: [email protected]) Downloaded from http://meridian.allenpress.com/jwd/article-pdf/51/4/907/2240813/2015-01-025.pdf by guest on 30 September 2021

ABSTRACT: An incidental observation of the 16 Galapagos-endemic passerines (Fessl Philornis downsi parasitizing a Galapagos Fly- and Tebbich 2002; Causton et al. 2013). catcher (Myiarchus magnirostris)nesthas Research to understand the ecology of revealed new insights into the searching behavior P. downsi and to develop methods for and biology of this invasive fly parasite and its interactions with endemic landbirds in the mitigating its impacts on Galapagos land- Galapagos Islands. Observations suggest that birds is in process and is a priority for P. downsi relies on olfactory cues, or olfactory Galapagos conservation organizations cues combined with the activity of adult birds, to (Causton et al. 2013). locate nests and that continue to visit nests The Galapagos Flycatcher, Myiarchus . when chicks are 3 d old. At least 200 eggs were magnirostris Gould, is endemic to the laid by P. downsi in different parts of the nest and .40 early-instar larvae were found inside the Galapagos and is thought to have arrived head of one chick, with additional larvae found in less than one million years ago through the base of the nest. was the likely a single colonization event (Sari and Parker cause of mortality of both chicks found in or near 2012). This flycatcher is the smallest bird in the nest. This description of P. downsi parasit- the genus Myiarchus, approximately 15 cm izing chicks of M. magnirostris highlights the long, and is the only representative of this vulnerability of this endemic bird to this invasive fly. genus in the Galapagos (Wiedenfeld 2011). Key words: Galapagos Flycatcher, invasive This species is the only hole-breeding species, landbird conservation, Myiarchus, landbird in the archipelago and occupies parasite, Philornis. a wide range of elevations and habitat types. It is found on all of the main islands Recent reports of population declines of including Espan˜ ola, Fernandina, Floreana, 11 passerine species endemic to the Isabela, Santiago, Santa Cruz, and San Galapagos Islands have alerted conserva- Cristobal (Wiedenfeld 2011). Although it is tion practitioners to the need to better one of the most common landbirds on the understand the ecology of landbirds and Galapagos Islands, it is one of the least their principal threats (Cunninghame studied, and little is known about its et al. 2012; Dvorak et al. 2012). Landbird biology and ecology and whether breeding species declines are thought to be mainly success has been affected by the increased attributable to introduced species, in abundance of introduced species over the particular the invasive parasitic fly Philor- last decades (Ervin 1992; Wiedenfeld nis downsi Dodge & Aitken (Kleindorfer 2011). Philornis downsi was first observed et al. 2014, and references therein). Fly on Galapagos Flycatcher chicks in 2004 parasitism in the Galapagos was first and again in 2008 (B. Fessl pers. comm.). reported in 1997 in Woodpecker Finch Although the flycatcher is named as a host (Camarhynchus pallidus Sclater and Sal- (Fessl et al. 2006), nothing was known vin) nestlings, and since then has become about the impacts of P. downsi on this the main threat to the survival of at least endemic species.

907 908 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/51/4/907/2240813/2015-01-025.pdf by guest on 30 September 2021

FIGURE 1. Parasitism by Philornis downsi in the Galapagos Flycatcher (Myiarchus magnirostris) in the Galapagos Islands, Ecuador. (A) Adult flycatcher exiting nest constructed inside a bamboo pole. (B) 3–4-d-old chick with flesh wound caused by feeding of P. downsi larvae. (C) One of 44 late first-instar and early second- instar P. downsi larvae extracted from 3–4-d-old chick. (D) P. downsi eggs deposited on nest material.

On 5 August 2014, a female flycatcher larvae at the base of the beak. No other was observed on several occasions enter- lesions were observed on the hatchling. ing and exiting a 9-cm-diameter bamboo Two days after the first observation, and pole that formed part of a roof of a shade after confirming that the parents had house maintained by the Charles Darwin abandoned the nest, the nest material Research Station at Puerto Ayora, Santa was removed. At least 80% of the nest was Cruz (0u45900S, 90u1990.10W; Fig. 1A). made of feathers from other bird species, After determining that the parents were including feathers that appeared to belong not in the vicinity, a nest was found inside to feral chickens (A. Llerena pers. comm.). , the pole approximately 20 cm from the A dead chick ( 2–3 d old) was found inside the nest with large holes around its opening. Inside the bamboo pole, about beak; however, no larvae were visible on 5 cm from the opening, a moribund the chick. This chick appeared to have chick (,3–4 d old) was found. Further been dead for at least 1 d, and it is possible investigation with a 1-m wireless snake that this was not the same chick we plumbing inspection camera with an LCD observed alive in the nest 2 d earlier. monitor (distributed by Brainydeal, New Because there was no evidence of egg York, New York, USA) revealed a live shells in the nest, we could not tell if there chick inside the nest. The moribund chick had been more than two chicks in the nest; was later examined and 44 first- and Galapagos Flycatchers are thought to lay second-instar P. downsi larvae were col- 3–5 eggs (Wiedenfeld 2011). lected (Fig. 1B, C). Most of the larvae Approximately 70% of the nest material were found in a large hole made by the was inspected (some of the outer nest SHORT COMMUNICATIONS 909 material was needed for an experiment). and did not possess the typical dome Upon dismantling the nest, 42 live shape of finch nests. Philornis downsi was P. downsi larvae were found (32 second- recently recorded parasitizing chicks in instar and 10 third-instar larvae). In addi- rectangular nest boxes on mainland Ecua- tion, 203 P. downsi eggs were found in the dor (Bulgarella et al. 2015), suggesting feathers and other material used to build the that adult flies may locate nests by nest (Fig. 1D), both inside and outside of orientating to olfactory cues or to olfactory the nest. Of these, 21 eggs were unhatched cues combined with the activity of the and opaque, 30 contained fully formed adult birds. 2) Adult flies showed interest larvae, and 152 eggs were empty following in the nest when chicks were .3 d old, larval eclosion. Eighty-six of the larvae that similar to observations of O’Connor et al. Downloaded from http://meridian.allenpress.com/jwd/article-pdf/51/4/907/2240813/2015-01-025.pdf by guest on 30 September 2021 hatched were found on the chicks or in the (2010) on the interactions of P. downsi nest material, but 66 were unaccounted for and two finch species. This suggests that, and may have been inside the dead chicks, if there are olfactory cues, they are not just on the parents, or in the nest material that associated with eggs or egg hatch and that was not inspected. No pupae were found in female flies that arrive at the nest later in the nest and there was no evidence of other the reproductive phase of the birds may Diptera. The fact that no pupal exuviae be responding to cues produced by the were found eliminates the possibility that chicks, the fly larvae, or the action of the some of the fly eggs might have originated larvae feeding on the birds. 3) Flies waited from a cohort of chicks that had occupied to enter the nests until adult birds were this nest previously. absent (confirming the observations of The day the nest was discovered, two O’Connor et al. [2010]). 4) Flies did not adult female P. downsi were found resting fly directly into the nest; rather they flew on the black mesh of the shade house wall close to the nest and then walked. 5) Flies about 30–50 cm from the entrance to the entered the nest even though chicks were nest. The flies were observed for .40 min already parasitized and there were numer- at 1000 hours and did not change position ous fly larvae and eggs already present in even when they were approached to the nest. Nest infestation by multiple confirm their identity. We did not observe P. downsi females has been confirmed by any interactions between them. On check- microsatellite studies (Dudaniec et al. ing the area at 1430 hours, two female flies 2010); however, to our knowledge, this is were observed close to the bamboo pole the first record of a P. downsi female and nest. Soon after, a female flycatcher visiting a nest with a known number of emerged from the pole and one of the flies conspecific larvae and eggs. 6) Early-instar flew to the edge of the bamboo pole and P. downsi larvae can affect other areas of entered the pole walking. The fly re- the heads of the chicks in addition to the mained inside the bamboo pole for about nostrils, beak, and ears (Fessl et al. 2006), 8 min, even after the female flycatcher suggesting subcutaneous habits (M. Quir- returned to the nest. As the flycatcher oga pers. comm.). 7) Philornis downsi lays emerged from the nest, the fly was its eggs in other parts of the nest, not just observed flying over the bird’s head. on the inner surface of the nest where the These observations provide new insights baby chicks are found or on the chicks into the behavior and ecology of P. downsi themselves (O’Connor et al. 2010). 8) The in the Galapagos Islands, and on the chicks are not necessarily dead when impacts it is having on the Galapagos the parents take them out of the nest Flycatcher, and suggest the following. 1) (Small Ground-finch [Geospiza fuliginosa Philornis downsi may not require a visual Gould] adults were filmed removing dead “nest image” cue to locate nests as we had chicks from nests by O’Connor et al. suspected—the flycatcher nest was hidden [2014]); in our study a moribund flycatcher 910 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015 chick was observed outside the nest for at 2011–2012. GNPS, GCREG, CDF, and GC, least 3 h after the nest was discovered. 9) Puerto Ayora, Galapagos, Ecuador, pp. 167–173. Cunninghame F, Ortiz-Catedral L, Fessl B. 2012. Parasite load in the Galapagos Flycatcher Landbird conservation plan: Strategies for re- can be high; .40 first- and second-instar versing the decline of passerine birds on the larvae were found on or inside the head of Galapagos Islands. Secondary report of the one of the chicks and additional larvae were workshop: Searching for solutions for the control found in the base of the nest. of the avian parasite, Philornis downsi, Puerto Ayora, Santa Cruz, Galapagos, 31 January– The impact of P. downsi larvae on 3 February; Charles Darwin Foundation and newborn Galapagos Flycatchers highlights Galapagos National Park Directorate, 26 pp. the vulnerability of these small birds and Dudaniec RY, Gardner MG, Kleindorfer S. 2010. the urgent need to find a method for Offspring genetic structure reveals mating and Downloaded from http://meridian.allenpress.com/jwd/article-pdf/51/4/907/2240813/2015-01-025.pdf by guest on 30 September 2021 controlling P. downsi. A pilot study was nest infestation behaviour of an invasive parasitic fly (Philornis downsi) of Gala´pagos birds. Biol initiated in May 2014 in the arid zone of Invasions 12:581–592. Santa Cruz Island to learn more about the Dvorak M, Fessl B, Nemeth E, Kleindorfer S, nesting and reproductive behavior of the Tebbich S. 2012. Distribution and abundance Galapagos Flycatcher and to determine of Darwin’s finches and other land birds on Santa Cruz Island, Gala´pagos: Evidence for the degree of parasitism by P. downsi. declining populations. Oryx 46:78–86. Many thanks to Francesca Cunninghame, Ervin S. 1992. Nesting behavior of the Large-billed Paul Medranda, Carolina Loyola, and Xavier Flycatcher on Isla Santa Cruz. Notı´cias de Pilataxi of the Charles Darwin Foundation Gala´pagos 51:17–19. for helping with sorting the material and to Fessl B, Kleindorfer S, Tebbich S. 2006. An experimental study on the effects of an in- Martin Quiroga, George Heimpel, Birgit troduced parasite in Darwin’s finches. Biol Fessl, and Javier Cotin for comments on this Conserv 127:55–61. note. This work was supported by funding Fessl B, Sinclair BJ, Kleindorfer S. 2006. The life from the Galapagos Conservancy and the cycle of Philornis downsi (Diptera: Muscidae) International Community Foundation (with parasitizing Darwin’s finches and its impacts on nestling survival. Parasitology 133:739–747. a grant awarded by The Leona M. and Harry Fessl B, Tebbich S. 2002. Philornis downsi—A B. Helmsley Charitable Trust) to the Charles recently discovered parasite on the Galapagos Darwin Foundation. This is contribution Archipelago—A threat for Darwin’s finches? Ibis number 2107 of the Charles Darwin Foun- 144:445–451. dation for the Galapagos Islands. Permission Kleindorfer S, Peters KJ, Custance G, Dudaniec RY, O’Connor JA. 2014. Changes in Philornis in- to conduct this study in protected areas of festation behavior threaten Darwin’s finch sur- Galapagos National Park was granted by the vival. Curr Zool 60:542–550. Galapagos National Park Directorate (Pro- O’Connor J, Robertson J, Kleindorfer S. 2010. 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