Can Darwin's Finches and Their Native Ectoparasites Survive the Control of Th

Home , Coextinction, Conservation genetics, Mangrove finch, Medium ground finch, Medium tree finch, Philornis downsi

Insect Conservation and Diversity (2017) 10, 193–199 doi: 10.1111/icad.12219

FORUM & POLICY Coextinction dilemma in the Galapagos Islands: Can Darwin’s ﬁnches and their native ectoparasites survive the control of the introduced ﬂy Philornis downsi?

1 2 MARIANA BULGARELLA and RICARDO L. PALMA 1School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand and 2Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand

Abstract. 1. The survival of parasites is threatened directly by environmental alteration and indirectly by all the threats acting upon their hosts, facing coextinction. 2. The fate of Darwin’s finches and their native ectoparasites in the Galapagos Islands is uncertain because of an introduced avian parasitic fly, Philornis downsi, which could potentially drive them to extinction. 3. We documented all known native ectoparasites of Darwin’s finches. Thir- teen species have been found: nine feather mites, three feather lice and one nest mite. No ticks or fleas have been recorded from them yet. 4. Management options being considered to control P. downsi include the use of the insecticide permethrin in bird nests which would not only kill the invasive fly larvae but the birds’ native ectoparasites too. 5. Parasites should be targeted for conservation in a manner equal to that of their hosts. We recommend steps to consider if permethrin-treated cotton stations are to be deployed in the Galapagos archipelago to manage P. downsi. Key words. Chewing lice, coextinction, Darwin’s finches, dilemma, ectoparasites, feather mites, Galapagos Islands, permethrin, Philornis downsi.

Introduction species have closely associated species which are also endangered (Dunn et al., 2009). The same threats affecting Coextinction refers to the loss of one species as the result of free-living species such as global warming and ecosystem the extinction of another species it depends on (Stork & disturbance, reduce the abundance and diversity of parasites Lyal, 1993). This is a process with cascading effects across as well (Bradley & Altizer, 2007; Bush et al., 2013). Thus, trophic levels (Dunn et al., 2009); losing one species from parasites are directly threatened by environmental alteration the ecosystem may imply losing others consequently and indirectly by all the threats acting upon their hosts (Col- because organisms are interconnected (Koh et al., 2004). well et al., 2012; Gomez & Nichols, 2013). A compounded Coextinctions represent a loss of evolutionary history (Pur- effect of the threats experienced by avian hosts, for example, vis et al., 2000), and they might be the most common form would mean that climate change poses a serious threat to the of biodiversity loss, according to different mathematical smaller parasite fauna on polar and temperate regions, while models (Koh et al., 2004; Dunn, 2005, 2009). Documented habitat destruction would be the main threat to parasites in cases of coextinction are, however, extremely scarce (Dunn tropical regions (Dobson et al., 2008). et al., 2009). Either coextinctions are common but happen Until recently, the idea of protecting parasites has not undetected or, they are rare because parasites adapt quickly been a priority for conservation efforts (Durden & Keir- and are more plastic than it is thought (Dunn et al., 2009). ans, 1996) because there is a bias towards conserving free- Tens of thousands of parasites are likely to have disap- living species (Windsor, 1990, 1995) to whom humans can peared due to coextinction and many endangered host put an emotional or recreational value. As an example, the IUCN Red List of Threatened Species only includes one parasite species as endangered (Whiteman & Parker, Correspondence: Mariana Bulgarella, School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington 2005; Dunn et al., 2009). Parasitic organisms form great 6140, New Zealand. E-mail: [email protected] part of biodiversity (Price, 1980). Besides having

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Table 1. List of ectoparasites recorded from Darwin’s ﬁnches in the Galapagos Islands (Records due to natural straggling or contamination by human agency have not been included).

Common name Order Family Species Host species References

Feather Sarcoptiformes Psoroptoididae Mesalgoides geospizae Geospiza conirostris Mironov and Perez (2002) mite Geospiza fortis O’Connor et al. (2005) Geospiza fuliginosa Villa et al. (2013) Geospiza magnirostris Geospiza scandens Camarhynchus parvulus Camarhynchus pallidus Camarhynchus psittacula Platyspiza crassirostris Certhidea olivacea Feather Sarcoptiformes Xolalgidae Xolalgoides palmai Geospiza fortis Mironov and Perez (2002) mite Geospiza fuliginosa O’Connor et al. (2005) Geospiza magnirostris Villa et al. (2013) Geospiza scandens Camarhynchus parvulus Camarhynchus psittacula Platyspiza crassirostris Certhidea olivacea Feather Sarcoptiformes Trouessartiidae Trouessartia geospiza Geospiza fortis O’Connor et al. (2005) mite Geospiza fuliginosa Lindstrom€ et al. (2009) Geospiza magnirostris Villa et al. (2013) Geospiza scandens Camarhynchus parvulus Camarhynchus pallidus Camarhynchus psittacula Platyspiza crassirostris Certhidea olivacea Feather Sarcoptiformes Proctophyllodidae Proctophyllodes darwini Geospiza fortis O’Connor et al. (2005) mite Geospiza fuliginosa Villa et al. (2013) Geospiza magnirostris Geospiza scandens Camarhynchus parvulus Camarhynchus pallidus Camarhynchus psittacula Platyspiza crassirostris Certhidea olivacea Feather Sarcoptiformes Proctophyllodidae Amerodectes atyeoi Geospiza difﬁcilis O’Connor et al. mite Geospiza fortis (2005, as Pterodectes) Geospiza fuliginosa Villa et al. (2013) Geospiza magnirostris Geospiza scandens Camarhynchus parvulus Camarhynchus pallidus Camarhynchus psittacula Platyspiza crassirostris Certhidea olivacea Feather Sarcoptiformes Analgidae Strelkoviacarus sp. Geospiza fortis O’Connor et al. (2005) mite Geospiza fuliginosa Villa et al. (2013) Camarhynchus parvulus Certhidea olivacea Feather Sarcoptiformes Analgidae Analges sp. Certhidea olivacea Villa et al. (2013) mite Feather Sarcoptiformes Dermoglyphidae Dermoglyphus sp. Geospiza fortis O’Connor et al. (2005) mite Geospiza fuliginosa Villa et al. (2013) Geospiza scandens

(continued)

Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 10, 193–199 Conserving native ectoparasites of Darwin’s ﬁnches 195

Table 1. (continued)

Common name Order Family Species Host species References

Camarhynchus pallidus Platyspiza crassirostris Nest Parasitiformes Dermanyssidae Dermanyssus sp. Geospiza fuliginosa O’Connor et al. (2005) mite Feather Phthiraptera Menoponidae Myrsidea darwini Geospiza fuliginosa Palma and Price (2010) louse Geospiza magnirostris Palma and Peck (2013) Camarhynchus psittacula Feather Phthiraptera Philopteridae Brueelia chelydensis Geospiza conirostris Palma and Peck (2013) louse Geospiza difﬁcilis Geospiza fortis Geospiza fuliginosa Geospiza magnirostris Camarhynchus pallidus Camarhynchus parvulus Camarhynchus psittacula Certhidea olivacea Feather Phthiraptera Philopteridae Brueelia interposita Geospiza difﬁcilis Palma and Peck (2013) louse Geospiza fortis Geospiza fuliginosa Geospiza magnirostris Camarhynchus psittacula Platyspiza crassirostris Feather Phthiraptera Philopteridae Philopterus insulicola Certhidea olivacea Palma and Peck (2013) louse

extraordinary species richness (Windsor, 1998) and biomass Thraupidae. They evolved from a single group of ances- (Kuris et al., 2008), parasites contribute to important tors that colonised the Galapagos Islands 2–3 million ecosystems functions and services as they occupy key roles years ago from Central or South America (Farrington & in food webs (Hudson et al., 2006; Strona, 2015), they may Petren, 2009). One of these, the Cocos Island finch be indicators of ecosystem health (Marcogliese, 2005), and (Pinaroloxias inornata) occurs only on Cocos Island. are relevant in increasing genetic diversity of natural popu- Therefore, the Galapagos radiation would comprise 15 lations (Coltman et al., 1999; O’Brien, 2000). In addition, finch species that include seven ground finches (Geospiza parasite population genetics is a useful tool to infer host’s spp.), five tree finches (Camarhynchus spp.), the vegetarian population history (Whiteman & Parker, 2005). finch (Platyspiza crassirostris) and two warbler finches The relevance of parasites in natural ecosystems leaves (Certhidea spp.). We follow the avian taxonomic classifi- us with an important dilemma that needs to be addressed cation of the Cornell University (2016) Neotropical Birds and dealt with: should native parasites be saved when a website (http://neotropical.birds.cornell.edu/) where the free-living species is managed for its conservation? (Perez vampire finch, Geospiza septentrionalis, is not recognised et al., 2013). The case of a host specific louse living on as a separate species. Most of Darwin’s finches occur on the Californian condor, which became extinct because of more than one island of the Galapagos archipelago but the conservation efforts to save its host, is a classic there are two species of major conservation concern. The example of that dilemma (Windsor, 1990; Stork & Lyal, mangrove finch (Camarhynchus heliobates) with <100 indi- 1993; Anonymous, 2006). Here, we are concerned viduals is restricted to Isabela Island (Lawson et al., about the fate of the Darwin’s finches and their native 2017), and the medium tree finch (Camarhynchus pauper), ectoparasites in the Galapagos Islands, especially because which is only found on Floreana Island with an estimated the birds are seriously threatened by an introduced population of approximately 1600 individuals (O’Connor parasitic fly, which could potentially drive them to et al., 2010). Both species are listed as Critically Endan- extinction. gered on the IUCN Red List of Threatened Species (Bird- Life International, 2016). The most serious threat to land birds in the Galapagos is the accidentally introduced Darwin’s finches: endangered hosts avian parasitic fly, Philornis downsi (Diptera: Muscidae). While adult flies are not parasitic, female flies lay eggs Farrington et al. (2014) recognised 16 species of Darwin’s inside bird nests and the fly larvae feed on nestlings (Fessl finches, placed by Barker et al. (2015) in the family et al., 2006). Mortality of infested nestlings is high,

Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 10, 193–199 196 Mariana Bulgarella and Ricardo L. Palma

Table 2. List of Darwin’s finches with their recorded ectopara- Table 2. (continued) sites in the Galapagos Islands (Records due to natural straggling or contamination by human agency have not been included). Common Host species names Ectoparasite species Common Host species names Ectoparasite species Feather lice Brueelia chelydensis Medium tree finch Feather mites No record Large cactus finch Feather mites Mesalgoides geospizae Camarhynchus Feather lice No record Geospiza conirostris Feather lice Brueelia chelydensis pauper Sharp-beaked ground Feather mites Amerodectes atyeoi Large tree finch Feather mites Amerodectes atyeoi finch Feather lice Brueelia chelydensis Camarhynchus Mesalgoides geospizae Geospiza difficilis Brueelia interposita psittacula Proctophyllodes darwini Medium ground finch Feather mites Amerodectes atyeoi Trouessartia geospiza Geospiza fortis Dermoglyphus sp. Xolalgoides palmai Mesalgoides geospizae Feather lice Brueelia chelydensis Proctophyllodes darwini Brueelia interposita Strelkoviacarus sp. Myrsidea darwini Trouessartia geospiza Vegetarian finch Feather mites Amerodectes atyeoi Xolalgoides palmai Platyspiza Dermoglyphus sp. Feather lice Brueelia chelydensis crassirostris Mesalgoides geospizae Brueelia interposita Proctophyllodes darwini Small ground finch Feather mites Amerodectes atyeoi Trouessartia geospiza Geospiza fuliginosa Dermoglyphus sp. Xolalgoides palmai Mesalgoides geospizae Feather lice Brueelia interposita Proctophyllodes darwini Grey warbler finch Feather mites No record Strelkoviacarus sp. Certhidea fusca Feather lice No record Trouessartia geospiza Green warbler finch Feather mites Amerodectes atyeoi Xolalgoides palmai Certhidea olivacea Analges sp. Nest mites Dermanyssus sp. Mesalgoides geospizae Feather lice Brueelia chelydensis Proctophyllodes darwini Brueelia interposita Strelkoviacarus sp. Myrsidea darwini Trouessartia geospiza Large ground finch Feather mites Amerodectes atyeoi Xolalgoides palmai Geospiza Mesalgoides geospizae Feather lice Brueelia chelydensis magnirostris Proctophyllodes darwini Philopterus insulicola Trouessartia geospiza Xolalgoides palmai Feather lice Brueelia chelydensis Brueelia interposita Myrsidea darwini leading to concerns about population declines and poten- Common cactus finch Feather mites Amerodectes atyeoi tial extinction of some species of Darwin’s finches (Huber, Geospiza scandens Dermoglyphus sp. 2008; O’Connor et al., 2010; Koop et al., 2011, 2013, Mesalgoides geospizae 2016; Cimadom et al., 2014; Kleindorfer et al., 2014; Proctophyllodes darwini Heimpel et al., in press). Up to now, P. downsi has been Trouessartia geospiza reported parasitising 11 of the 14 species of Darwin’s Xolalgoides palmai finches (Causton et al., 2013; Heimpel et al., in press). Feather lice No record The large cactus finch (Geospiza conirostris), the sharp- Mangrove finch Feather mites No record beaked ground finch (Geospiza difficilis) and the grey Camarhynchus Feather lice No record heliobates warbler finch (Certhidea fusca) are not known to be para- Woodpecker finch Feather mites Amerodectes atyeoi sitised because nests of these three species have not yet Camarhynchus Dermoglyphus sp. been sampled for P. downsi. pallidus Mesalgoides geospizae The detrimental effects of P. downsi parasitism on nest- Proctophyllodes darwini lings of the two critically endangered Darwin’s finch spe- Trouessartia geospiza cies are well studied (O’Connor et al., 2010; Lawson Feather lice Brueelia chelydensis et al., 2017). Mangrove finch nests are heavily infested Small tree finch Feather mites Amerodectes atyeoi with P. downsi resulting in 70% nestling mortality (Law- Camarhynchus Mesalgoides geospizae son et al., 2017) and medium tree finch nests presented parvulus Proctophyllodes darwini the highest recorded parasite load per nest of any finch Strelkoviacarus sp. Trouessartia geospiza species on Floreana Island with a mean of 52 parasites Xolalgoides palmai per nest (O’Connor et al., 2010). An international team of scientists is working together with the Charles Darwin (continued) Foundation and the Galapagos National Park Directorate Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 10, 193–199 Conserving native ectoparasites of Darwin’s finches 197 to find potential methods to control P. downsi (Causton has not been considered (Causton & Lincango, 2014). If et al., 2013). the birds sit on a nest built with permethrin-treated cotton, some of their ectoparasites may die, in particular those inhabiting the ventral side of the birds, but those Darwin’s finches: Ectoparasites living on the dorsal side of the body may not be affected as much. Darwin’s finches and their native ectoparasites have coe- Furthermore, considering that, with very few excep- volved for millions of years in the Galapagos Islands. The tions, the same native ectoparasite species have been ectoparasites’ dependence on avian hosts implies that they found on most of the finch species (see Tables 1 and 2), are also coendangered and risk going extinct together with and that not all islands or finch species will be targeted them. In addition, sustained parasite transmission requires with the permethrin-treated cotton method, some popula- a threshold host population size, meaning that some of tions of ectoparasites should survive, as long as their host Darwin’s finch ectoparasite species might be already species do. We believe that precautions should be taken extinct, as parasite extinction could precede that of the when deploying the cotton-treated stations. If they were hosts (Gompper & Williams, 1998; Altizer et al., 2007; to be installed, we urge scientists, in particular those deal- Powell, 2011; Bush et al., 2013; Rosza & Vas, 2015). The ing with the mangrove and medium tree finch, to collect coextinction threat of a host-parasite system should be native ectoparasites from a series of adult individuals assessed on a case by case basis (Gomez & Nichols, 2013) before the installation occurs, so that their ectoparasitic as it will depend on the host and the parasite ecology, associations can be recorded and described. We advocate phylogeny, and the parasite’s host range and life cycle that parasites should be targeted for conservation in a (Gomez et al., 2012). manner equal to that of their hosts. If the aim is main- We use the term ‘ectoparasite’ to include feather lice taining biodiversity, it is first necessary to research it in (Phthiraptera), fleas (Siphonaptera), mites and ticks order to know what there is to conserve, and then to do (Acari). A list of ectoparasites known from Darwin’s it in its entirety (Wilson, 2000). finches is given in Table 1. We documented a total of 13 ectoparasite species on 11 Darwin’s finch species in the Galapagos Islands. There may be still more unnamed Acknowledgements ectoparasitic species to be discovered, especially feather mites, whereas fleas and ticks have not been recorded We thank two anonymous reviewers for their useful com- from them yet. Knowledge of the biology and ecology of ments that improved our original manuscript. those species is almost nil. Further study of the ectoparasites living on these iconic birds should take place before it is too late. References

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