The belted kingfisher, Megaceryle alcyon (Linnaeus) (Coraciiformes: Alcedinidae), is distributed widely in North America and is the only coraciiform bird in Canada (Kelly et al. Reference Kelly, Bridge, Hamas and Rodewald2009). It is one of about 117 species of kingfishers worldwide (Catanache et al. Reference Catanache, Johnson, Marks, Moyle, Valim and Weckstein2019) and a member of the least diverse subfamily, Cerylinae (Moyle Reference Moyle2006). It breeds throughout the forested regions of Canada, including Manitoba, especially along waterways and lakes where food (fish, crayfish, invertebrates) is abundant and where there are suitable banks in which to excavate burrows for nesting (Godfrey Reference Godfrey1986). Belted kingfishers are not particularly common in Manitoba (Holland and Taylor Reference Holland and Taylor2003), but many people might recognise their familiar call and perhaps even recall their appearance on the Canadian five-dollar bill in the Birds of Canada Series that ran from 1986 to 2002.
A number of studies have investigated internal parasites of belted kingfishers (e.g., Zeliff Reference Zeliff1941; Preble and Harwood Reference Preble and Harwood1944; Anderson Reference Anderson1959; Boyd Reference Boyd1966; Boyd and Fry Reference Boyd and Fry1971; Scott Reference Scott1984; Muzzall et al. Reference Muzzall, Cook and Sweet2011; Bronson et al. Reference Bronson, Kelly and Hoberg2014), but records for ectoparasites are largely taxonomic or anecdotal and generally lacking in significant ecological context (e.g., Peters Reference Peters1936; Stirrett Reference Stirrett1952; Judd Reference Judd1953; Whitehead Reference Whitehead1954; Carriker Reference Carriker1959; Keirans Reference Keirans1967; Boyd and Fry Reference Boyd and Fry1971; Emerson Reference Emerson1972; Pence and Gray Reference Pence and Gray1996; Galloway et al. Reference Galloway, Proctor and Mironov2014). As part of a long-term study on ectoparasites infesting wildlife in Manitoba, an opportunity arose to examine a sample of 41 belted kingfishers. The objectives are to provide an assessment of infestation parameters for the one species of chewing louse that infests kingfishers in the province, Alcedoffula alcyonae Carriker (Phthiraptera: Ischnocera: Philopteridae), and to determine other ectosymbionts infesting this host.
Kingfishers were obtained from wildlife hospitals (Wildlife Haven, Ⓘle-des-Chênes, and Prairie Wildlife Rehabilitation Centre, Winnipeg and St. Adolphe, Manitoba, Canada), from Manitoba Sustainable Development, and from Oak Hammock Marsh Interpretive Centre (near Stonewall, Manitoba). All birds had been euthanised or died from their injuries and were frozen individually in plastic bags for at least 48 hours to kill all ectoparasites. Birds were lightly thawed and then washed twice in warm, soapy water, then once in warm water to collect lice as described by Mironov and Galloway (Reference Mironov and Galloway2002). This method removes virtually all the chewing lice, except most of the eggs (Clayton and Drown Reference Clayton and Drown2001; Galloway, personal observation). Lice were collected onto a 90-μ screen and then preserved in 70% or 95% ethanol. Specimens were sorted using a stereomicroscope, counted, and enumerated according to sex and stage of development (adult versus nymph). Representative specimens were prepared onto microscope slides as per Richards (Reference Richards1964). Vouchers were deposited in the J.B. Wallis/R.E. Roughley Museum of Entomology (Department of Entomology, University of Manitoba, Winnipeg, Manitoba). After birds had been washed, the nasal passages were flushed through each nostril and out through the mouth with a solution of warm soapy water, using a 12-mL Monojet® 412 curved-tip plastic orthodontic syringe to collect nasal mites. Primary and secondary feathers were removed from the wings of 19 birds and were examined under a stereomicroscope for quill mites.
The following infestation parameters were calculated using Quantitative Parasitology (QPweb, Version 1.0.14; Reiczigel et al. Reference Reiczigel, Marozzi, Fabian and Rózsa2019): prevalence (proportion of birds infested; Sterne’s method for 95% confidence limits), mean intensity, and mean abundance (mean number per infested bird and mean number per sampled bird, respectively; Bootstrap BCa with 2000 bootstrap replications for 95% confidence limits for both). Measures of aggregation of infestation, including the variance–mean ratio, Poulin’s Index of Discrepancy (D; Poulin Reference Poulin1993), and the negative binomial exponent, k, were also calculated using QPweb.
From 1995 to 2020, 41 birds were examined, 27 of which were from Winnipeg. Two birds came from each of Gimli and Selkirk, and one bird came from each of Falcon Beach, Glenlea, Minnedosa, Spruce Siding, and Whiteshell. Five birds came from unknown locations in Manitoba. At least one to four kingfishers were obtained in every year of the survey, except 1997, 2007 and 2019, when none was examined. Kingfishers in Manitoba are migratory, and birds were examined during all months they are typically present in Manitoba, with the number of birds examined in each month as follows: May – 2; June – 2; July – 6; August – 7; September – 17; October – 4. No dates of collection were available for three birds.
The only chewing louse species found to be infesting belted kingfishers was A. alcyonae. It was found on 20 of the 41 birds examined, or 48.8% (95% confidence interval = 34.0–64.1) of the birds. Of the 342 lice collected, 59 were males, 80 were females, and 203 were nymphs (with a ratio of 2.6 nymphs to each female). Although females outnumbered males, the sex ratio was not significantly different from 1.0 (χ2 = 3.173, P = 0.08, df = 1). The number of lice on each infested bird ranged from 1 to 70. Mean intensity of infestation was 17.1 (95% confidence interval = 10.40–29.10), and mean abundance was 8.3 (95% confidence interval = 4.46–15.10). Distribution of infestation was highly aggregated: variance/mean = 30.7, D = 0.763 (95% confidence interval = 0.690–0.849), k = 0.184 (not significantly different from k for negative binomial, P = 0.654, based on χ2).
No nasal mites were collected from any of 32 birds examined in this study (Knee and Galloway Reference Knee and Galloway2017). The only feather mite collected was an undescribed species of Proterothrix (Acari: Astigmatina: Proctophyllodidae) (Galloway et al. Reference Galloway, Proctor and Mironov2014), which infested three of 35 birds (8.6%). No quill mites were found in the primary feathers removed from 19 birds.
Alcedoffula Clay & Meinertzhagen is a relatively small genus of chewing lice that includes 19 described species, all of which are specific ectoparasites of kingfishers (Price et al. Reference Price, Hellenthal and Palma2003). To the author’s knowledge, the present study is the first quantitative analysis of chewing lice infesting belted kingfishers. There are studies in which small numbers of other species of kingfishers have been examined for chewing lice. For example, Roda and Isidro de Farias (Reference Roda and Isidro de Farias1999) reported one louse, a Quadraceps Clay & Meinertzhagen sp. (Phthiraptera: Ischnocera: Philopteridae), from one green kingfisher, Chloroceryle americana Kaup, in Brazil, but lice in this genus typically infest charadriiform birds (this specimen is likely a straggler or a contaminant). Clayton et al. (Reference Clayton, Gregory and Price1992) examined one each of two Chloroceryle species of kingfishers from Peru, Amazon kingfisher (C. amazona (Latham)) and green kingfisher, the former of which was infested by four females of an Alcedoffula sp. Gustafsson et al. (Reference Gustafsson, Lei, Luo, Chu, Zhao, Zhang and Zou2019) examined one specimen of black-capped kingfisher, Halcyon pileata (Boddaert) from China, but found no lice. Najer et al. (Reference Najer, Sychra, Kounek, Papousek and Hung2014) collected five specimens of Alcedoecus annulatus Ansari (Phthiraptera: Ischnocera: Philopteridae) from one of three white-throated kingfishers, Halcyon smyrnensis (Linnaeus), in southern Vietnam. When Saxena et al. (Reference Saxena, Kumar, Gupta, Mitra, Ali and Srivastava2007) examined 30 white-throated kingfishers in India, they recorded 40% to be infested with a species of Meropoecus Eichler (Phthiraptera: Ischnocera: Philopteridae), a genus typically infesting bee-eaters, Merops Linnaeus spp. (Coraciiformes: Meropidae). This genus of louse has not otherwise been recorded from this host (Price et al. Reference Price, Hellenthal and Palma2003; perhaps a misidentification). Saxena et al. (Reference Saxena, Kumar, Gupta, Mitra, Ali and Srivastava2007) reported a mean intensity of 17.75, similar to infestation parameters in the present study. Intensity of infestation reported in the present study is higher than in either Roda and Isidro Farias (Reference Roda and Isidro de Farias1999) or Najer et al. (Reference Najer, Sychra, Kounek, Papousek and Hung2014), perhaps because numbers of host specimens examined in their studies are very small, but differences in efficiency of collecting methods may have also contributed to the differences found in infestation intensity.
No conclusions about seasonal patterns in infestation can be reached because of the small numbers of kingfishers obtained for study in each month. Greatest numbers were available for study in August and September (65.7% of birds for which collection dates were available), likely because of the greater proportion of migrating juveniles in the population. No attempt was made to age birds in this study.
Because the belted kingfisher is widely distributed in North America and is closely associated with aquatic systems (Baron et al. Reference Baron, Ashwood, Sample and Welsh1997), it has become an important indicator for environmental contaminants, including heavy metals, PCBs, and pesticides, acquired through its predominately piscivorous feeding habits (Moore et al. Reference Moore, Sample, Suter, Parkhurst and Teed1999; Blocksom et al. Reference Blocksom, Walters, Jicha, Lazorchak, Angradi and Bolgrien2010; Flanagan Pritz et al. Reference Flanagan Pritz, Schrlau, Massey Simonich and Blett2014; Jackson et al. Reference Jackson, Evers, Eagles-Smith, Ackerman, Willacker and Elliott2016). This species seems to be less affected than other piscivorous species of birds by some contaminants in aquatic systems because of the small size of their prey (Jackson et al. Reference Jackson, Evers, Eagles-Smith, Ackerman, Willacker and Elliott2016). Human activities that affect water quality and food availability, cover, and nesting habitat can impact populations of belted kingfisher (Kelly et al. Reference Kelly, Bridge, Hamas and Rodewald2009). The conservation status of belted kingfisher at this time is of Least Concern (BirdLife International 2016), but any major decline in belted kingfisher populations in the future may also affect populations of the monoxenic chewing louse, A. alcyonae.
Acknowledgements
The author extends special thanks to the staff of Wildlife Haven and Prairie Wildlife Rehabilitation Centre for the care with which they handled the birds for this study, to Paula Grieef who kindly allowed access to belted kingfishers submitted at the Oak Hammock Marsh Interpretive Centre and to the Canadian Wildlife Service for issuing scientific permits over the duration of this study. The author thanks to Dave Holder and the many students who helped by washing birds. Robert J. Lamb (Department of Entomology, University of Manitoba, Winnipeg, Manitoba), Dale H. Clayton (School of Biological Sciences, University of Utah, Salt Lake City, Utah, United States of America), Carol A. Galloway, and two anonymous reviewers provided valuable comments on the manuscript. This research was funded in part by Discovery Grants from the National Sciences and Engineering Council of Canada and by Manitoba Conservation (Sustainable Development Initiatives Fund). The author is grateful for the continued support of the Department of Entomology and the Faculty of Agricultural and Food Sciences at the University of Manitoba.