Diversity and Abundance of Ectoparasitic Blow Flies Protocalliphora (Diptera: Calliphoridae) and Their Nasonia (Hymenoptera
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ARTHROPOD BIOLOGY Diversity and Abundance of Ectoparasitic Blow Flies Protocalliphora (Diptera: Calliphoridae) and Their Nasonia (Hymenoptera: Pteromalidae) Parasitoids in Tree Swallow Nests Within Agricultural Lands of Southern Que´bec, Canada 1,2 3 4 5 1 S. P. DAOUST, J. SAVAGE, T. L. WHITWORTH, M. BE´ LISLE, AND J. BRODEUR Ann. Entomol. Soc. Am. 105(3): 471Ð478 (2012); DOI: http://dx.doi.org/10.1603/AN11155 ABSTRACT We described the community composition of the ectoparasitic ßies Protocalliphora Hough (Diptera: Calliphoridae) and their Nasonia (Ashmead) (Hymenoptera: Pteromalidae) para- sitoids collected from tree swallow, Tachycineta bicolor (Vieillot), nests in southern Que´bec, Canada, Downloaded from in 2008 and 2009. The prevalence of nest infestation by Protocalliphora was 70.8% in 2008 and 34.6% in 2009. The average parasitic burden of Protocalliphora spp. was estimated at 5.53 (Ϯ5.61 SD) pupae per nestling for 2008 and 4.66 (Ϯ9.31 SD) pupae per nestling for 2009. The percentage of nests containing Protocalliphora pupae parasitized by Nasonia spp. was of 85.3% in 2008 and 67.2% in 2009. Three species of Protocalliphora were collectedÑProtocalliphora sialia Shannon & Dobroscky, Pro- tocalliphora bennetti Whitworth, and Protocalliphora metallica (Townsend)Ñand two species of http://aesa.oxfordjournals.org/ Nasonia, Nasonia vitripennis (Walker) and Nasonia giraulti Darling. This is the Þrst record of P. bennetti and N. giraulti in the province of Que´bec. Our Þndings provide further evidence for observation made previously that altricial bird nests are more frequently and more heavily infested by blow ßies in western than in eastern North America. Our data also suggest that more than a quarter of the tree swallow within the study area are exposed to high levels of ectoparasitism that could negatively affect their health. KEY WORDS Protocalliphora, Nasonia, agricultural landscape, parasitism at Don Thomson on April 14, 2016 Larvae of Holarctic bird blow f1ies in the genera terials. There is a paucity of information on the life Protocalliphora Hough and Trypocalliphora Peus history of these bird ectoparasites; most of the liter- (Diptera: Calliphoridae) are obligate blood-feeding ature on Protocalliphora focuses on taxonomy, host parasites of nestling birds, a unique life history among records, and host Þtness costs after parasitism (Daw- the Calliphoridae. To date, 28 species of Protocalli- son et al. 2005, Simon et al. 2005, Hannam 2006). phora and one species of Trypocalliphora parasitizing Generally, both male and female Protocalliphora over- 139 bird species have been recorded from the Nearctic winter as adults, and females lay their eggs as soon as region (Sabrosky et al. 1989, Whitworth 2003). Birds nestlings hatch (T.L.W., personal observation). De- with the highest infestation rates are those that nest velopment from egg to adult takes on average 23Ð38 d, repeatedly in a given habitat and build large nests, and although most Protocalliphora species are univol- such as hawks (Acipiter and Buteo spp.), magpies (Pica tine, some are capable having more than one breeding spp.), crows (Corvus spp.), and cavity-nest breeders cycle per season by parasitizing the second brood of such as European starlings (Sturnus vulgaris L.) and the bird species within their habitat (Bennett and tree swallows (Tachycineta bicolor Vieillot) (Bennett Whitworth 1991). and Whitworth 1992). Blow ßy larvae are typically anchored to the most Adult Protocalliphora are rarely collected in the accessible part of the nestling (feet, legs and belly); Þeld but immatures (larvae and pupae) are typically some species also can be found in the auditory and found after close examination of nestlings or nest ma- nasal cavities (Whitworth and Bennett 1992). Proto- calliphora larvae must take two to three bloodmeals to complete their development (Sabrosky et al. 1989). 1 Institut de recherche en biologie ve´ge´tale, Universite´ de Mon- Amounts of blood ingested vary according to species, tre´al, 4101 Sherbrooke Est, Montre´al, QC, Canada, H1X 2B2. 2 Corresponding author, e-mail: [email protected]. reaching on average 0.08 g in the large Protocalliphora 3 Department of biological sciences, BishopÕs University, 2600 Col- rognesi Thompson & Pont (Bennett and Whitworth lege St., Sherbrooke, QC, Canada, J1M 1Z7. 1991). In the most extreme scenario, Þve or six of the 4 Washington State University, 2533 Inter Ave., Puyallup, WA largest P. rognesi larvae, capable of each ingesting 0.2 g 98372. 5 De´partement de biologie, Universite´ de Sherbrooke, 2500 boule- of blood, could exsanguinate an 18-d-old bank swallow vard de lÕUniversite´, Sherbrooke, QC, Canada, J1K 2R1. [Riparia riparia (L.)] in a single day (Whitworth and 0013-8746/12/0471Ð0478$04.00/0 ᭧ 2012 Entomological Society of America 472 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 105, no. 3 Bennett 1992). However, most instances of nestling known in eastern Canada where tree swallows are mortality have been associated with organ damage experiencing important population decline (Nebel et because of parasitism by obligate subcutaneous larvae al. 2010). The objectives of this study were to 1) of Trypocalliphora braueri Hendel (Sabrosky et al. describe the assemblages of Protocalliphora and Na- 1989, Howe 1992, Matsuoka et al. 1997). sonia species found in tree swallow nests in 40 farms At the upper trophic level, puparia of Protocalli- in southern Que´bec, Canada; 2) estimate the parasitic phora are often found parasitized by small, gregarious load of Protocalliphora on their bird hosts; and 3) “jewel wasps” of the genus Nasonia (Ashmead) (Hy- establish levels of parasitism by Nasonia. menoptera: Pteromalidae). All four known species of Nasonia are found in the Nearctic region, and only Materials and Methods Nasonia vitripennis (Walker), a generalist that devel- ops in the pupae of a variety of calyptrate Diptera Study Area and Nest Box Network. The 10 200-km2 species (Whiting 1967), also is found in the Palaearctic study areas included a network of 400 bird nest boxes region. The three other Nasonia species only parasitize distributed among 40 farms within the Monte´re´gie and Protocalliphora pupae and are restricted to eastern Estrie regions in southern Que´bec (Fig. 1). The area (Nasonia giraulti Darling, Nasonia oneida Raychoud- is characterized by an eastÐwest gradient of agricul- hury & Desjardins) and western North America (Na- tural intensiÞcation where dairy farming and small- sonia longicornis Darling) (Darling and Werren 1990, scale, familial farms are replaced by large-scale, con- Downloaded from Raychoudhury et al. 2010). For the past 40 yr, Nasonia tinuous row cropping with full mechanization and parasitoids, especially N. vitripennis, have been exten- high input of pesticides as well as of organic and sively used as model organisms for studies investigat- chemical fertilizers (Be´langer and Grenier 2002, Jobin ing mating behavior, genomics, speciation and espe- et al. 2003; Fig. 1). Nest boxes were built according to cially sex allocation and sex ratio distorters (Werren North American Bluebird SocietyÕs speciÞcations (i.e., and Loehlin 2009, Godfray 2010). However, very little eastern/western bluebird model) and were erected in http://aesa.oxfordjournals.org/ is actually known of their ecology and behavior in winter 2004. Ten nest boxes per farm were placed 50 m their natural habitat (Grillenberger et al. 2008). apart along drainage ditches or fence lines that bor- Although the literature has been divided with re- dered agricultural Þelds or pastures. All boxes were gard to the impact of Protocalliphora larvae on their mounted on a metal post 1.5 m above the ground and bird hosts, it now seems clear that they can negatively with the opening facing southeast. See Ghilain and inßuence health and survivorship of nestlings and Be´lisle (2008) for the detailed farm selection protocol. ßedglings by exacerbating effects of unfavorable en- Specimen Collection and Identification. Before vironmental conditions (e.g., low food abundance). their fall migration, tree swallows typically visit nests Such negative impacts are more likely to occur in that were used during the breeding season, probably at Don Thomson on April 14, 2016 species that can be frequently afßicted by high loads to ascertain the quality of potential future breeding of Protocalliphora larvae, such as the tree swallow sites (Bent 1963, Doligez et al. 2004, Ghilain and Be´- (Bennett and Whitworth 1992, Hannam 2006, Thomas lisle 2008, Winkler et al. 2011). To avoid interference et al. 2007). Indeed, tree swallows renest in the same with the birdÕs habitat quality assessment, insect spec- habitat each year; conditions conducive to mainte- imens were collected from the Þeld using two proto- nance of large Protocalliphora populations (Bent 1963, cols. First, two of the 10 available tree swallow nests Bennett and Whitworth 1992). To date, 11 species of in each of the 40 farms were examined for Protocal- Protocalliphora have been recorded parasitizing tree liphora pupae immediately upon ßedging, i.e., be- swallow nestlings, six of which occur in the Eastern tween 25 June and 16 July in both 2008 and 2009. The Nearctic (Sabrosky et al. 1989; Whitworth 2002, 2003). nest was carefully removed from the box, and all pupae Moreover, the population of this bird species, like that in nest material and in the nest box were collected. of most aerial insectivores found in North America and The nest was put back into the box upon completion Europe, has been decreasing over most of its range of sampling. Pupae were individually placed into during the past 30 yr (Benton et al. 2002, Nebel et al. meshed capped plastic bottles (4 cm in length by 7 cm 2010). This generalized population decline of aerial in height) for rearing. They were maintained in a insectivores is hypothesized to be linked to a decrease mixture of sawdust and 1% boric acid at room tem- in ßying insect abundance caused by large-scale eco- perature (Ϸ22ЊC) until the emergence of the adult system modiÞcations, notably agricultural intensiÞca- ßies or their parasitoids (5Ð12 d).