Ashdin Publishing Ecological Parasitology and Immunology ASHDIN Vol. 4 (2015), Article ID 235907, 7 pages publishing doi:10.4303/epi/235907

Research Article Can a Blood-Feeding Ectoparasitic Fly Affect Songbird Migration? Examining Body Condition and Fat Reserves of Five Bird Species in Relation to Hippoboscid Fly Parasitism

Andrew K. Davis Odum School of Ecology, University of Georgia, Athens, GA 30602, USA Address correspondence to Andrew K. Davis, [email protected]

Received 12 February 2015; Revised 26 May 2015; Accepted 30 May 2015

Copyright © 2015 Andrew K. Davis. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract Background. Migratory birds are often faced with the chal- and are routinely observed by ornithologists during bird- lenge of undertaking long-distance journeys while harboring parasites. trapping activities [7,8,9]. Sometimes called “flatflies” Objective. I investigated the possibility that Hippoboscid flies (Diptera, because of their flattened body (see Figure 1(b)), these Hippoboscidae), blood-feeding ectoparasites, would be associated with reduced body condition or fat reserves of migratory songbirds. Meth- obligate, blood-sucking flies live in the spaces between ods. I mist-netted songbirds on an island off the southern coast of Nova the feathers and skin of birds [10]. Since they feed on the Scotia, Canada during fall 1996 and noted the presence of hippoboscid blood of the host, this makes them important as potential flies on five focal species. Of 731 individuals, 60 (8.2%) had flies. vectors of disease; hippoboscids are now recognized Results. In statistical models that considered species and parasitism, I found no effect of flies on body condition, but birds with flies had as potential vectors of West Nile virus [11,12] and significantly reduced fat reserves. This pattern was found in all species hemosporidian parasites [13,14]. Hippoboscids parasitize to varying degrees. Conclusions. While these results do not confirm many bird species, including migratory passerines [15,16, causality, they are consistent with the idea that parasitized birds suffer 17]. Importantly, the life cycle of this parasite is closely tied a cost to their migratory preparations. It is unclear whether the birds were in a premigratory stage or actually migrating, although reductions to the biology of the host, such that their reproductive season in fat in either case would be costly. This study highlights how host- coincides with that of their host [18]. Therefore hippoboscid parasite interactions must be studied in multiple life stages to gain a flies appear to be most prevalent in bird populations at complete understanding of their nature. the end of the summer and in early fall [8,16,17,18,19, Keywords birds; migration; parasites; Hippoboscid flies; Hippobosci- 20,21]. This period is a critical time for migratory birds, dae; fat reserves when individuals become hyperphagic and fat stores must be deposited for the fall migration. If hippoboscid flies 1. Introduction pose any problems for their hosts in terms of reductions in Parasites, by definition, subsist off of the resources of their energy or vigor (either from direct loss of blood or from host, thereby draining potential energy reserves, or reducing hosts reallocating energy into immunity), this in theory overall performance. The question of how parasites might could translate into difficulties in procuring food and/or fat influence animals during their migration has recently deposition in preparation for migration. received a high degree of scientific scrutiny [1,2,3,4,5]. In a previous study, I documented the host range For animals that migrate long distances on an annual basis, of hippoboscid flies on a small island on the eastern these journeys can be extremely taxing to begin with, and shore of Canada, which serves as fat-deposition and anything that remotely limits their performance could mean stopover site for many migratory species of songbirds the difference between success and failure on the journey. during their southward, fall migration [20]. At this site, With this in mind, interest is growing in how parasites hippoboscid flies were found on 24 species of birds, with could affect migratory performance in a variety of animals, prevalence levels between 1% and 22%, though there including migratory songbirds [1,6]. were five species in particular that were parasitized most One parasite of birds that has not previously been frequently: yellow warbler (Dendroica petechial; Figure considered as significant to migration is the Hippoboscid fly 1(c)), common yellowthroat (Geothlypis trichas; Figure (Diptera, Hippoboscidae; Figure 1). These flies (hereafter 1(d)), Swainson’s thrush (Catharus ustulatus;Figure1(e)), called hippoboscids) are common ectoparasites of birds, song sparrow (Melospiza melodia; Figure 1(f)), and fox 2 Ecological Parasitology and Immunology

Figure 1: Dorsal (a) and lateral (b) photographs of a hippoboscid fly (Ornithomya anchineuria), which is a blood-feeding ectoparasite of birds, plus photos of each of the focal bird species in this study, including (c) yellow warbler, (d) common yellowthroat, (e) Swainson’s thrush, (f) song sparrow, and (g) fox sparrow. The hippoboscid specimen was 6.75 mm in length, including wings. Hippoboscid photos were taken by Tyler Christensen, and all bird photos were taken by Richard Hall. sparrow (Passerella iliaca; Figure 1(g)). Because of their island off the southern coast of Nova Scotia, Canada large sample sizes, I focused the current project on these (43¡28 N, 65¡44 W; Figure 2). The site is now the Atlantic five species. Each of these species is classified as migratory, Bird Observatory, a Canadian Migration Monitoring though their journeys vary in length; yellow warblers, Network station [27,28]. The island is mostly composed of common yellowthroats, and Swainson’s thrushes are long- Maritime forest habitat (spruce, birch, maples), with some distance migrants, with wintering grounds in Central and marsh/bog habitat [29]. Birds were captured with standard South America [22,23,24], while song sparrows and fox ornithological mist nets (12 m length, 3 m tall) that were set sparrows are temperate migrants and winter in the southern up in wooded and shrubby areas where birds were known to United States [25,26]. Here, I used previously unpublished forage. Mist nets were usually set up from dawn to noon and data from the original study (from the fall migration season were checked every 30 min [29,30]. After net extraction, in 1996) to examine the effect of hippoboscid fly infection all captured birds were transported to a central processing on two key measures of bird performance during migration: station in cloth bags. their overall body condition as well as the degree of fat deposition. To my knowledge, this paper represents the 2.2. Hippoboscid parasitism first investigation into hippoboscid fly effects within the Any hippoboscid flies that flew from the bird during the net migratory stage of songbirds, and the results should prove extraction and/or banding procedures were recorded [20]. useful for comparisons with other life stages. If no hippoboscid flies were observed it was assumed that the bird was not parasitized. While it is possible that flies 2. Methods could have flown from birds prior to net extraction, in reality, there is no recourse for addressing this problem, since birds 2.1. Capturing birds cannot be extracted immediately when multiple nets need From August through October of 1996, I captured migrating to be checked. For the purposes of the current project, the landbirds on Bon Portage Island, which is a small (∼ 150 ha) species-level identification of these flies was not important; Ecological Parasitology and Immunology 3

regressions were significantly positive (P<.05 for all) and resulted in a score for each individual that was on the same scale (centered around zero) regardless of species. This body condition score was the response variable in an ANOVA model that included hippoboscid fly parasitism (infected, not infected), and bird species as categorical predictors. I also included a month variable to account for variation in condition over the season. The two-way interaction term, species*parasitism, was included to account for the possibility of differences among species in the effects of the parasite, and a month*parasitism term was also included. I did not include age as an independent variable because of the difficulties in assigning age to all individuals. A second analysis examined fat scores of the birds in relation to hippoboscid fly presence. Since fat scores in this study were limited to 5 discrete values (i.e., 0Ð4 on the Helms and Drury scale), I used a Poisson regression model [33] with fat score as the dependent variable and using the same predictors and interaction effects as in the previous analysis Figure 2: Location of the study site for this project, Bon (i.e., bird species, month, parasitism, month*parasitism, ∼ Portage Island (marked by arrow). It is a 150 ha island species*parasitism). All statistical analyses in this study situated approximately 3 km off the southwestern tip of were conducted using the Statistica 12.0 software package. Nova Scotia, Canada. 3. Results the prior study [20] showed that there were only two species 3.1. General of hippoboscid flies observed on passerines at this site— Ornithomya anchineuria (Figure 1) and Ornithoica vicina, I captured a total of 731 individual birds of the five focal based on taxonomic keys established by Maa and Peterson species (yellow warbler, common yellowthroat, song spar- [10], but 92% of all flies were O. anchineuria. row, Swainson’s thrush, and fox sparrow) during fall 1996 on Bon Portage Island. I made 60 observations of hippo- 2.3. Bird measurements boscid flies on these birds (Table 1). Hippoboscid preva- Each bird was processed following established procedures lence within species ranged from 4.5% to 15.8% and there at this site and other migration monitoring or bird banding appeared to be a general association with body size; larger stations [29,30]. Each bird was weighed using a portable bodied species tended to have higher rates of hippoboscid electronic balance and its wing length (a standard measure fly parasitism, which is a pattern that has been shown in of body size in birds) was measured to the nearest millimeter other investigations as well [18]. Of the known-aged birds, using an ornithologist’s wing ruler. I attempted to assign an hippoboscid flies were observed on 7 adult birds out of 54 age to each bird (adult or young-of-the-year) based on skull total (13%). Forty-five (8%) of the 586 young birds were ossification and plumage characteristics [31], though not all infected. These frequencies were not significantly different birds could be reliably aged. I then assessed the amount of (χ2 = 1.85, P = .174). visible subcutaneous fat in the furcular hollow of each bird following Helms and Drury [32]. In this system, the level 3.2. Effects of hippoboscids on body condition and fat of subcutaneous fat was subjectively scored on a 0Ð5 scale Hippoboscid fly parasitism was not a significant predictor so that birds with no visible fat are classified as “0”, a bird of body condition score of any of the birds I examined. In is “3” if the fat was just at the level of the furcular hollow, the ANOVA model examining predictors of body condition, and birds with fat overflowing the furcular hollow are a “5” there was no significant main effect of parasitism nor any (although no birds with 5 were recorded during this study). two-way interactions that involved parasitism (P>.7 Finally, all birds were banded with a numbered aluminum for all; Table 2(a)). However, the Poisson regression leg band (USFWS) for later identification and released. model of fat scores did show evidence of variation due to hippoboscid parasitism (df = 1, χ2 = 17.32, P<.001; 2.4. Data analysis Table 2(b)). Other significant predictors in the fat score I first obtained a “body condition” score for each bird by model included species (df = 4, χ2 = 82.44, P<.001) retaining the residual mass from a linear regression of and month (df = 2, χ2 = 162.45, P<.001). To visualize mass versus wing length, using each species separately. All the effect of hippoboscids across species, Figure 3 shows 4 Ecological Parasitology and Immunology

Table 1: Summary of birds captured and hippoboscid fly parasitism rates during the period AugÐOct 1996 on Bon Portage Island, NS, Canada. Birds are listed in order of increasing body mass (average of all individuals of each species). Standard deviations of weight means are indicated in parentheses. Species Ave. weight (g) Total captured # with hippoboscids % with hippoboscids Yellow warbler (YWAR) 9.8 (1.4) 286 13 4.5 Common yellowthroat (COYE) 10.0 (1.4) 174 9 5.2 Song sparrow (SOSP) 20.6 (1.5) 69 9 13.0 Swainson’s thrush (SWTH) 30.6 (1.7) 76 12 15.8 Fox sparrow (FOSP) 38.2 (2.8) 126 17 13.5 Total 731 60 8.2

Table 2: Summary of statistical analyses that examined the effects of bird species and hippoboscid fly parasitism on body condition (a) and fat scores (b) of songbirds on Bon Portage Island. Body condition scores were examined using analyses-of-variance, while fat scores were examined using a Poisson regression model. Predictor df MS FP Month 2 1.05 0.41 .666 Species 4 0.81 0.31 .869 Parasitism (0/1) 1 0.35 0.14 .713 Species*parasitism 4 1.25 0.49 .745 Month*parasitism 2 0.20 0.08 .926 Error 717 2.57 (a) Response variable: body condition. Figure 3: Average fat scores of five species of passerines, 2 Predictor df Log-likelihood χ P separated by hippoboscid fly presence. Species abbrevia- − . <. Month 2 754 106 162.45 001 tions are as follows: yellow warbler (YWAR), common − . <. Species 4 835 334 82.44 001 yellowthroat (COYE), song sparrow (SOSP), Swainson’s Parasitism (0/1) 1 −745.446 17.32 <.001 − . thrush (SWTH), and fox sparrow (FOSP). Species are listed Species*parasitism 3 741 477 7.94 .047 X Month*parasitism 1 −739.441 4.07 .044 on the -axis in order of increasing body size. All birds were captured from August through October, 1996, on Bon (b) Response variable: fat scores. Portage Island. Whiskers represent standard errors. average fat scores of each of the five study species. There were clear differences in the magnitude of the effect, which is also evidenced by the significant interaction of species*parasitism in the Poisson regression model (df = 3, χ2 = 7.94, P = .047; Table 2(b)); the largest effects of hippoboscid flies were in the three smallest species examined (Figure 3). An alternative depiction of the parasite effects on fat deposition is to compare mean fat scores across all species combined during each month; see Figure 4. In this figure, average fat scores of nonparasitized birds tended to increase throughout the season (the effect of month was significant in the Poisson model; Table 2(b)), but birds with hippoboscids tended to have lower fat scores in each month. To put the parasite-related variation in fat scores into Figure 4: Average fat scores of all five bird species perspective, it is important to know how much fat, in terms combined, separated by hippoboscid presence, across the of weight, is typical for each of the categories. To get at this, three months of trapping at Bon Portage Island. Only one I selected two of the species with similar body sizes, yellow hippoboscid fly was found in October. Whiskers represent warblers and common yellowthroats (∼ 9Ð10 g each), and standard errors. Ecological Parasitology and Immunology 5

Table 3: Average weights of birds within each fat score not yet be realized. On the other hand, given that similar category, using two species of similar body size, yellow patterns were found across multiple species, with varying warbler and common yellowthroat. The increase in weight life histories (i.e., nesting biology, migration patterns, etc.), with progressive fat scores provides an indication of fat it seems reasonable to favor the alternative—that these content. Note no birds with a fat score of 5 were observed parasites cause reductions in fat reserves of migratory within these species. songbirds. Fat score n Weight mean (g) Weight SD From the trapping data, especially for the month of 0 256 9.5 1.3 August, it is not necessarily clear whether the birds captured 1829.71.4 were local individuals that were in a premigratory state, or 2 60 10.3 1.5 if they were migrants that had recently arrived at the site. 3 44 10.8 0.8 Prior work did show that hippoboscid flies are common on 4 16 11.4 1.2 birds captured in the summer in this site [20]. However, this may not matter, since in either case, birds would be foraging calculated average body weights for all birds in each fat for food and depositing fat stores, which they would use as class (Table 3). In doing so it is clear that each fat class fuel for their migratory journeys [34]. Moreover, it is also is approximately 0.3 gÐ0.6 g heavier than the previous one. important to consider the location of this site in relation to This information is helpful for interpreting parasite-related the migratory flyways (Figure 2); all birds here would be reductions in fat reserves, as shown in Figure 3. Thus, if facing a long journey ahead of them regardless of whether hippoboscids are responsible for a reduction in fat score by they were preparing for migration or simply using this 1 (on the 0Ð5 scale), that is equivalent to a loss of between island as a stopover site. Thus, if hippoboscid flies hinder 0.3 g and 0.6 g of fat. fat deposition during either of these stages it would certainly be detrimental to overall migratory success. At a minimum, 4. Discussion it could delay their departure at the outset, or prolong their The results of this project suggest that hippoboscid flies can numerous stopovers, either of which would result in delayed negatively affect bird migrations as their occurrence was arrival to wintering grounds. A more serious possibility is associated with an individual’s ability to procure and/or that they would fail to complete the migration from the store fat. The fact that the same pattern was found in inadequate fat deposits. multiple species (Figure 3) provides the most substantial This work raises the larger question of how these evidence for this conclusion. Surprisingly, there appeared to parasites exert their influence on their hosts. In other be no evidence that body condition was affected by the par- words, why would parasitized birds suffer at all from asites [19], however, of the two variables I considered, this hippoboscids, especially if the number of parasites per one may be less important than the other to the success of the individual is usually less than 3 flies [18,20]? There is little migration. Interestingly, this investigation also revealed that knowledge concerning the physiological effects of these larger-bodied species tended to have higher prevalence of flies. Experimental work with barn swallows (Hirundo hippoboscids [18], but the negative effects of hippoboscids rustica) showed how hippoboscid flies exert much of their (on fat reserves) appear to be more pronounced in the negative effects on birds during the nestling stage, by smaller species (Figure 3). This observation is supported by reducing condition (i.e., protein levels) of chicks [35]. the significant species*parasitism interaction in the model Nestlings are known to have high rates of hippoboscid of fat scores (Table 2(b)). parasites, and in fact, some believe this is the primary mode It is important to note that while the analyses of of vertical transmission [18]. If the negative effect of the fat scores showed a significant “statistical effect” of flies carries over to the fledged stage (i.e., lower condition), hippoboscid parasitism, this does not necessarily imply such individuals may be at a disadvantage compared to causation, that is, that the flies directly led to reductions nonparasitized conspecifics, in terms of energy availability. in host fat reserves. What these data do show is that there The barn swallow study also indicated hippoboscids can is an association between hippoboscid flies and low host stimulate an immune reaction [35], which in itself can cause fat reserves. In fact, it is possible that poorly-nourished, or energy stores to be reallocated from normal activities [36]. otherwise less fit hosts would be more likely to encounter One other study has shown negative effects of hippoboscid and/or retain these parasites because of reduced activity flies on condition in adult birds [19]. Future studies may or reductions in grooming. Moreover, hippoboscid flies need to be directed at this question of how hippoboscid flies are also known to move between hosts, although not affect host physiology. often [18]. However, this fact is nonetheless relevant to the The current study adds to the small but growing list interpretation of results here, since birds with flies may have of hippoboscid fly effects by highlighting their potential only recently become parasitized, and any ill-effects would influence on a key life stage of many songbirds, their 6 Ecological Parasitology and Immunology migratory periods. This period is marked by heightened Evidence from molecular and morphological studies, with a energy demand, increased stress, and extreme physiological description of Haemoproteus iwa, Int J Parasitol, 41 (2011), changes, which means that even minor impediments to 1019Ð1027. [14] J. R. Baker, A review of the role played by the Hippoboscidae performance may become magnified during this time. That (Diptera) as vectors of endoparasites, J Parasitol, 53 (1967), a pronounced effect was found in this study, by a parasite 412Ð418. that some may consider inconsequential, is a testament [15] C. M. 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