Diptera Communities of Raptor (Aves) Nests in Nova Scotia, Canada
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The Canadian Entomologist (2020), page 1 of 13 doi:10.4039/tce.2020.26 ARTICLE Diptera communities of raptor (Aves) nests in Nova Scotia, Canada Valerie Levesque-Beaudin1* , Bradley J. Sinclair2, Stephen A. Marshall3, and Randolph F. Lauff4 1Centre for Biodiversity Genomics, University of Guelph, 50 Stone Road E, Guelph, Ontario, N1G 2W1, Canada, 2Canadian National Collection of Insects and Canadian Food Inspection Agency, Ottawa Plant Laboratory – Entomology, Central Experimental Farm, 960 Carling Avenue, Ottawa, Ontario, K1A 0C6, Canada, 3School of Environmental Sciences, University of Guelph, 50 Stone Road E, Guelph, Ontario, N1G 2W1, Canada and 4Department of Biology, St. Francis Xavier University, 4130 University Avenue, Antigonish, Nova Scotia, B2G 2W5, Canada *Corresponding author. Email: [email protected] (Received 3 December 2019; accepted 9 March 2020; first published online 27 April 2020) Abstract The identity, richness, and abundance of true flies (Diptera) from the nests of three cavity-nesting raptors (Aves) were investigated in northern Nova Scotia, Canada. After fledging, flies were extracted from the nest mate- rial using Berlese funnels within an emergence chamber. Thirty-one species/morphospecies from 14 families were collected, including eight new records for Nova Scotia and two new records for eastern North America. Introduction Bird nests are micro-ecosystems with diverse communities of invertebrates, from ectoparasites to commensal species. Most studies of the arthropods in bird nests have focussed on the presence and impact of ectoparasites (Møller et al. 1990; Loye and Zuk 1991; Krištofík et al. 2001, 2002, 2003, 2007; Fairn et al. 2014), including fleas (Siphonaptera) (Phipps and Bennett 1974); mites (Acari) (Wasylik 1971); and nest-associated Diptera in the families Muscidae (Lowenberg-Neto 2008), Calliphoridae (Bennett and Whitworth 1991; Whitworth and Bennett 1992), and Carnidae (Cannings 1986a, 1986b; Dawson and Bortolotti 1997). However, nests also support diverse com- munities of commensal arthropods, including mites, flies, moths (Lepidoptera), beetles (Coleoptera), and various other Insecta. The first significant publications documenting the general fauna associated with bird nests were by Hicks (1959, 1962, 1971), who started building a checklist of arthropod species occurrence and their associated bird species. Since then, several studies have documented the Arthropoda communities associated with passerine (Passeriformes) birds, but relatively few have treated the communities associated with birds of prey. Some of the raptors for which associated insect communities have been documented include Eurasian griffon vulture (Gyps fulvus (Hablitz); Aves: Accipitridae) (Dražina and Špoljar 2009), boreal owl (Aegolius funereus (Bonaparte); Aves: Strigidae) (Krištofík et al. 2003; Majka et al. 2006), lesser spotted eagle (Aquila pomarina Brehm; Aves: Accipitridae) (Krištofík et al. 2009), American kestrel (Falco sparverius Linnaeus; Aves: Falconidae) (Philips and Dindal 1990; Neubig and Smallwood 1999), northern saw-whet owl (Aegolius acadicus (Gmelin); Aves: Strigidae) (Philips et al. 1983; Majka et al. 2006), red-footed falcon (Falco vespertinus Linnaeus; Aves: Falconidae) (Soltész et al. 2018), saker falcon (Falco cherrug Gray; Aves: Falconidae) (Merkl et al. 2004), and screech owl (Megascops asio (Linnaeus); Aves: Strigidae) (Philips and Dindal 1990). Subject editor: Rayda Krell © The Author(s), 2020. Published by The Entomological Society of Canada and Cambridge University Press Downloaded from https://www.cambridge.org/core. University of Guelph Library, on 27 Apr 2020 at 12:24:31, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2020.26 2 Levesque-Beaudin et al. Fig. 1. A, Inside the nest box with young chicks, feathers, guano, and prey; B, emergence trap with Berlese funnel inside and lamp on the outside. Here, we document the Diptera species found associated with three species of raptors occurring in Nova Scotia, Canada: American kestrel (Falco sparverius), boreal owl (Aegolius funereus), and northern saw-whet owl (Aegolius acadicus). This follows the confirmation that the boreal owl now has a breeding population in Nova Scotia (Lauff 2009), where it is now known to be sympatric with the northern saw-whet owl. This could lead to competition for available nesting area and resources, so it is important to fully understand the nesting environment. Majka et al. (2006) did preliminary work on the Coleoptera communities associated with raptor nests in an earlier stage of this study, while the work reported here considers the Diptera in a larger number of nests. Diptera are diverse and abundant in nests (Rotheray 1991; Iwasa et al. 1995; Gatt 2001) and include a large number of commensal species. It is not currently known whether these nest- associated fly communities differ between the nest boxes of different raptor species. Materials and methods Following the discovery of boreal owls breeding in Nova Scotia in 2004, nest boxes were installed in habitat suitable for the species to provide additional nesting sites for breeding pairs (Lauff 2009). The nest boxes followed the design of Korpimaki (1985) and were built from rough- cut pine lumber. Wood shavings were placed in the box to a depth of approximately 5 cm. Nest boxes were mounted 3–4 m high on living trees, with the entrance hole typically facing between south and east. Active nests were periodically visited to verify if the nest was still active, to ascertain when nestlings (Fig. 1A) would be ready to leave the nest and to record some other details including clutch size, abundance, and type of stored prey. Once the young owls had fledged, the nest mate- rial was transferred into wooden or plastic totes for transport to the laboratory where it was then placed into Berlese funnels inside emergence chambers; a 60-W incandescent bulb, approximately 50 cm from the funnel and set outside the chamber, was used to drive the funnel (Fig. 1B). The funnels collected arthropods crawling downwards, while insects flying upwards were retained in the emergence traps; collections ceased when a week went by with no further captures. The insects extracted were preserved in 70% isopropyl alcohol except for the specimens from two nests collected in 2018, which were placed in 95% ethanol to allow better DNA extraction. All adult dipterans were dried using a critical-point-dryer prior to mounting on paper points. In total, 28 nests were collected: two American kestrel, two boreal owl, and 24 northern saw- whet owl, all located in northern Cape Breton Island and the northern mainland of Nova Scotia, Canada (Fig. 2). The fly communities associated with each raptor species were assessed for Downloaded from https://www.cambridge.org/core. University of Guelph Library, on 27 Apr 2020 at 12:24:31, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2020.26 The Canadian Entomologist 3 Fig. 2. Location of the 28 nests in Nova Scotia for each bird species. richness, abundance, and trophic guild. Dominance was calculated as the percentage abundance of each species in comparison to the total number of specimens collected across all nests, regardless of the bird species. Constancy of occurrence was given as the number of nests where the species occurred compared to the total number of nests collected. These measures provided some indi- cation of whether the presence of certain species was expected in the nests or accidental. Measures of richness and abundance of flies were compared to the number of fledglings per nests to see if there was any correlation. A microplate of 95 specimens, including all apparent morphospecies, was sequenced for cyto- chrome c oxidase I (COI) prior to detailed examination of the material by specialists. This yielded sequences corresponding to most of the species later recognised by Diptera taxonomists involved with the project. All the sequences were uploaded to the Barcode of Life Database System (BOLD: http://boldsystems.org) (Ratnasingham and Hebert 2007). Most species met the requirements to be successfully assigned to a barcode index number (BIN), which is considered a good proxy for species for most groups (Ratnasingham and Hebert 2013). A maximum likelihood tree was gen- erated with Mega X using general time reversible model with gamma distributed with invariant sites to show the molecular diversity of the nests. For the species not represented among the successful sequences, a public sequence was included for representations when available (except for Ornithomyia bequaerti Maa (Diptera: Hippoboscidae) and unidentified morphospecies, e.g., Chironomidae (Diptera) species). All of these are released publicly through BOLD (https://doi.org/10.5883/DS-OWLNS) and GenBank (www.ncbi.nlm.nih.gov/genbank/). All vouchers are split among these institutions: Centre for Biodiversity Genomics (Guelph, Ontario, Canada), Canadian National Collection of Insects, Arachnids, and Nematodes (Ottawa, Ontario, Canada), University of Guelph Insect Collection (Guelph, Ontario, Canada), Downloaded from https://www.cambridge.org/core. University of Guelph Library, on 27 Apr 2020 at 12:24:31, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2020.26 4 Levesque-Beaudin et al. Nova Scotia Museum (Halifax, Nova Scotia, Canada), Department of Lands