Chewing Lice in Azorean Blackcaps (Sylvia atricapilla): A Contribution to Parasite Island Syndromes Author(s): Ivan Literák, Oldřich Sychra, Roberto Resendes, and Pedro Rodrígues Source: Journal of Parasitology, 101(2):252-254. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/14-601.1 URL: http://www.bioone.org/doi/full/10.1645/14-601.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
J. Parasitol., 101(2), 2015, pp. 252–254 Ó American Society of Parasitologists 2015
Chewing Lice in Azorean Blackcaps (Sylvia atricapilla): A Contribution to Parasite Island Syndromes Ivan Litera´k, Oldˇrich Sychra, Roberto Resendes*, and Pedro Rodr´ıgues*, Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Palack´eho tˇr. 1/3, 61242 Brno, Czech Republic; *CIBIO, Centro de Investiga¸c˜ao em Biodiversidade e Recursos Gen´eticos, InBIO Laborat´ orio Associado, Polo dos A¸cores, Universidade dos A¸cores, 9501-801 Ponta Delgada, Portugal. Correspondence should be sent to: [email protected]
clearly impoverished to about 10% of the parasite diversity known for mainland blackcaps; all parasites shared between insular and continental blackcaps had lower prevalence in the island populations; and the island parasite assemblage was composed of parasites that were not specific to blackcaps, despite the fact that most parasites infesting continental blackcaps are host specific. This should have supported the idea that the mainland host–parasite associations are compromised on islands. Barrientos et al. (2014) studied both haemosporidians and ectoparasites of trumpeter finches (Bucanetes githagineus) from the Canary Islands, Iberian Peninsula, and northwestern Africa. They found the prevalence of haemosporidians to be higher in mainland populations even as ectoparasites, including chewing lice, had lower prevalence compared to those in the Canary Islands. We were focused upon chewing lice of blackcaps on the Azores. The Macaronesian archipelago of the Azores is situated in the Atlantic between 36855 0 and 39843 0 N and 25801 0 and 31807 0 W and is comprised of 9 islands. Their total surface area is about 2,250 km2, and the islands stretch more than 600 km from east to west. The nearest point on the mainland is Cabo Roca in Portugal, which is 1,408 km east of Santa Maria. In 2013, a total of 46 blackcaps were mist-netted on the Azores. Birds were captured at various sites on each of the 3 islands explored. Blackcaps were individualized with a metal ring. Totals of 17, 24, and 5 blackcaps from Sa˜o Miguel, Santa Maria, and Graciosa, respectively, were examined. Lice were collected using the fumigation chamber method (Clayton and Drown, 2001), and birds were released after examination. The lice samples were fixed in 96% ethanol and determined microscopically in the laboratory to species level. The chewing louse assemblage on blackcaps was characterized by louse species spectrum, prevalence as the percentage of blackcaps infested with parasites, mean intensity as the number of individuals of a particular chewing louse species on infested hosts, and mean abundance as the number of individuals of a particular chewing louse species on the examined birds (Bush et al., 1997). For comparing these parameters in Macaronesian blackcaps to European mainland blackcaps, we used the results from examining 240 blackcaps in the Czech Republic. We had examined blackcaps at various sites in the Czech Republic during 2004–2008. Blackcaps are commonly nesting and obligatory migrating birds in the Czech Republic. For statistical analyses, ´ we used Quantitative Parasitology 3.0 (Rozsa et al., 2000). We found 2 and 5 species of chewing lice in the Azores and in the Czech Republic, respectively (Table I). The lower number of species found in the Azores compared to the Czech Republic supports the idea that mainland host–parasite associations are compromised on islands and result in lower numbers of species on islands (Paterson et al., 2002). This is in accord with the results from studies of blackcap and trumpeter finch haemosporidians ´ ´ıguez et al., 2013; Barrientos et al., 2014). in Macaronesia (Perez-Rodr Only chewing louse species host specific to blackcaps (B. tovornikae and M. sylviae) were found on blackcaps in the Azores (Table I). Hence, we did not confirm that the island parasite assemblage was composed of parasites not specific to blackcaps, an idea postulated on the basis of a ´ ´ıguez et al., 2013). study of blackcap haemosporidians (Perez-Rodr Moreover, we found 2 chewing louse species not specific to blackcaps (M. curuccae and M. eurysternus) on blackcaps examined on the mainland.
ABSTRACT: Focusing upon chewing lice (Phthiraptera: Amblycera, Ischnocera) parasitizing blackcaps (Sylvia atricapilla) in the Azores (Portugal), we found a lower number of louse species in the Azores compared to mainland Europe. Only chewing lice host specific to blackcaps were found in the Azores. Louse prevalences were much higher in blackcaps from the Azores compared to those of various mainland populations. Chewing lice are permanent parasites of birds, and for such parasites the parasite island syndrome could be characterized by higher parasite prevalence on the islands compared to the mainland.
The aim of this paper is to characterize the chewing louse assemblage on blackcaps (Sylvia atricapilla) from the Azores while comparing this assemblage to that on blackcaps from mainland Europe to elucidate parasite island syndromes (Nieberding et al., 2006) regarding these permanent ectoparasites of birds. A comparison of parasite assemblages in hosts originating from the islands and the mainland is a key element to analyzing evolutionary changes of host–parasite interactions supposedly different in these 2 environments. Until now, parasite (chewing louse) island syndromes have been exceptionally studied in a bird species inhabiting both islands and the continental mainland (Barrientos et al., 2014). More such studies are needed for an understanding of parasite island syndromes. Blackcap is a common sedentary bird on all islands of the Azores. It comprises a monophyletic group including both island and mainland populations (Dietzen et al., 2008). An isolation between contemporary blackcap populations in mainland Europe and the Atlantic islands is of relatively recent origin, because blackcaps colonized the Macaronesian Islands probably during the past 4,000–40,000 yr through several ´ migration events from mainland Europe (Perez-Tris et al., 2004; Dietzen et al., 2008). Resident populations of blackcaps in Madeira and the Canary Islands coexist, with a regular annual influx of migrating and overwintering mainland blackcaps. The closer an island is to the continent, the greater the migrating contingent (Shirihai et al., 2001). To our knowledge, there is no record of mainland blackcaps overwintering in the Azores (Portugal). Hence, there is no presumed recent transport of mainland blackcap parasites to these islands. Chewing lice (Phthiraptera: Amblycera, Ischnocera) are ectoparasites of mammals and birds, living mainly on skin, feathers, or fur. Lice influence major avian life history traits, such as flight performance, host condition, reproductive success, survival, and sexual selection (Barbosa et al., 2002; Price et al., 2003). To date, 6 species of chewing lice have been documented as parasites in blackcaps: Brueelia neoatricapillae Price, Helenthal & Palma, 2003; Brueelia paratricapillae Price, Helenthal & Palma, 2003; Brueelia tovornikae (Bala´t, 1981); Menacanthus curuccae (Schrank, 1776); Menacanthus eurysternus (Burmeister, 1838); and Myrsidea sylviae Sychra & Litera´k, 2008 (Price et al., 2003; Sychra and Litera´k, 2008). ´ ´ıguez et al. (2013) studied the haemosporidian parasites of Perez-Rodr blackcaps on the Macaronesian archipelagos of Madeira and the Canary Islands. They found that the insular haemosporidian assemblage was DOI: 10.1645/14-601.1 252
SHORT COMMUNICATIONS
253
TABLE I. Chewing lice on blackcaps in the Azores (Sa˜o Miguel, Santa Maria, and Graciosa islands) and Czech Republic. Fisher’s exact test (for ´ prevalences) and bootstrap 2-sample t-test (for intensities and abundances) were used. Calculations were made in Quantitative Parasitology 3.0 (Rozsa et al., 2000).
Species Brueelia neoatricapillae
B. tovornikae
Menacanthus curuccae
M. eurysternus
Myrsidea sylviae
Chewing lice total
Characteristics of chewing louse assemblage Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance
Sa˜o Miguel (nblackcaps ¼ 17)
Santa Maria (n ¼ 24)
0 0 0 0 70.6* 13.9 6 7.3 1–89 9.8 6 5.4* 0 0 0 0 0 0 0 0 64.7* 3.7 6 0.9* 1–10 2.4 6 0.7* 82.4* 14.9 6 6.6* 1–89 12.2 6 5.4*
0 0 0 0 20.8* 7.6 6 2–17 1.6 6 0 0 0 0 0 0 0 0 45.8* 2.1 6 1–5 1.0 6 54.2* 4.7 6 2–18 2.5 6
2.3 0.8†
0.3* 0.3* 1.2* 0.8*
Graciosa (n ¼ 5) 0 0 0 0 60.0* 4.7 6 1–11 2.8 6 0 0 0 0 0 0 0 0 40.0* 2.0 6 1–3 0.8 6 60.0* 6.0 6 2–11 3.6 6
2.6 1.9†
0.7† 0.5† 2.2† 1.8†
Czech Republic (n ¼ 240) 0.4 —‡ 1 0.004 6 0.004 0.4 —‡ 1 0.004 6 0.004 0.4 —‡ 1 0.004 6 0.004 1.3 2 6 0.5 1–3 0.025 6 0.015 0.8 1.0 6 0.0 1 0.008 6 0.005 3.3 1.4 6 0.2 1–3 0.05 6 0.02
* Significant. † Not significant statistical differences between data from the Azores and data from the Czech Republic. ‡ Only 1 bird was parasitized.
According to the geographical range hypothesis, we can predict that the number of parasite species per host should be positively correlated with host range (Gregory, 1990; Price et al., 2003). Our finding of a larger number of species of chewing lice on mainland blackcaps corroborates this hypothesis. The question remains whether mainland blackcaps acquired unspecific lice species through host-switching events between unrelated hosts or whether island blackcaps lost these lice through a so-called ‘‘missed the boat’’ event (Paterson et al., 2002). Our results revealed no significant differences in observed parasitological parameters among island populations. This is in accordance with Santiago-Alarcon et al. (2008) and Barrientos et al. (2014), who found the same pattern for chewing lice in the Galapagos Islands and Canary Islands, respectively. The observed chewing louse prevalences were much higher in blackcaps from the Azores compared to those observed in mainland Czech populations (Table I). This corresponds with findings from other parts of mainland Europe, where prevalences similar to those in the Czech ´ Republic were found: 9.5% in Spain, n ¼ 179 (Perez-Tris et al., 2002); 4.9% in Germany, n ¼ 61 (Frenzel, 2006); 4.0% in Hungary, n ¼ 25 (Z. Vas, pers. comm.); 3.8% in Romania, n ¼ 26 (C. Adam, pers. comm.); 3.3% in Greece, n ¼ 30 (A. Diakou, pers. comm.); 1.6% in Slovenia, n ¼ 62 (C. Adam, pers. comm.); and 1.5% in Sweden, n ¼ 131 (D. Gustafsson, pers. comm.). No lice were found on blackcaps in Bulgaria (n ¼ 69, M. Ilieva, pers. comm.) and Russia (n ¼ 88, O. Tolstenkov, pers. comm.). Our results are comparable with these data, because most of the aforementioned authors use the same fumigation chamber method for collecting lice. Moreover, mean intensities and mean abundances of parasites were higher in the Azores than on the mainland (Table I). The statistically
verified differences were striking in all cases of parasite prevalences and quite the opposite from the results for haemosporidians, where all parasites shared between insular and continental blackcaps had lower ´ ´ıguez et al., 2013). A prevalence in the island populations (Perez-Rodr reduced availability of appropriate vectors for haemosporidians had been offered as the explanation for the low number of parasite species and ´ ´ıguez et al., 2013). altered prevalence patterns on islands (Perez-Rodr Formerly, we had predicted significant differences in occurrence of chewing lice on migrating and resident birds (Sychra et al., 2011). An important aspect of migration’s evolution is that hosts may obtain an advantage in terms of reduced risks of parasitism by moving to areas that harbor lower densities of conspecifics. The risk of parasite infestation is usually density dependent (e.g., Begon et al., 1986), and a lower abundance of hosts in migratory as compared to resident populations may result in altered parasite–host dynamics. This effect may provide migrants with an initial benefit during the early stages of migration’s evolution (Møller and Erritzøe, 1998). Moreover, migratory bird species have more developed immune defence than do closely related resident species. This results from the exposure of migrants to a more diverse parasite fauna than that experienced by residents (Møller and Erritzøe, 1998). High parasite loads can be linked to increased thermoregulation costs and therefore lower fat stores. That, in turn, leads to less energy that can be devoted to flying (Barrientos et al., 2014). This can be important in the case of migratory birds. Because the life cycle of chewing lice occurs entirely on the host, environmental variability likely has less effect on the transmission dynamic of parasites. This suggests that their parasitological parameters—intensity, prevalence, and abundance—are equally variable (Santiago-Alarcon et al., 2008). We propose that differences of parasitological
254
THE JOURNAL OF PARASITOLOGY, VOL. 101, NO. 2, APRIL 2015
parameters between island and mainland populations of blackcaps found in this study can be correlated with migratory and ecological traits. This is in accordance with Teller ´ıa and Carbonell (1999), who had demonstrated that mainly these traits could explain morphological differences between the described subspecies of blackcap. Our results indicate that ectoparasites, including chewing lice, may play a role in bird migration and especially among small transcontinental passerine birds. Chewing lice are permanent parasites of birds, and for such parasites the parasite island syndrome could be characterized by higher parasite prevalence, mean intensity, and mean abundance on the islands compared to the mainland, as we demonstrated in blackcaps from the Azores compared to blackcaps from mainland Europe.
LITERATURE CITED BARBOSA, A., S. MERINO, F. DE LOPE, AND A. P. MØLLER. 2002. Effects of feather lice on flight behavior of male barn swallows. Auk 119: 213– 216. BARRIENTOS, R., F. VALERA, A. BARBOSA, C. M. CARILLO, AND E. MORENO. 2014. Biogeography of haemo- and ectoparasites of an arid-land bird, the trumpeter finch. Journal of Arid Environments 106: 11–17. BEGON, M., J. L. HARPER, AND C. R. TOWNSEND. 1986. Ecology: Individuals, populations and communities. Blackwell Scientific Publications, Oxford, U.K., 876 p. BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ, AND A. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583. CLAYTON, D. H., AND D. M. DROWN. 2001. Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). Journal of Parasitology 87: 1291–1300. ´ -DEL-REY, G. D. CASTRO, AND M. WINK. 2008. DIETZEN, C., E. GARCIA Phylogenetic differentiation of Sylvia species (Aves: Passeriformes) of the Atlantic islands (Macaronesia) based on mitochondrial DNA sequence data and morphometrics. Biological Journal of the Linnaean Society 95: 157–174. FRENZEL, K. 2006. Die Federlinge (Insecta: Phthiraptera: Ischnocera) durchziehender Singvoegel (Oscines) auf der Greifswalder Oie. Seevoegel 27: 2–6. GREGORY, R. D. 1990. Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4: 645–654. MØLLER, A. P., AND J. ERRITZØE. 1998. Host immune defence and migration in birds. Evolution and Ecology 12: 945–953.
NIEBERDING, C., S. MORAND, R. LIBOIS, AND J. R. MICHAUX. 2006. Parasites and the island syndrome: The colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33: 1212–1222. PATERSON, A. M., R. L. PALMA, AND R. D. GRAY. 2002. Drowning on arrival, missing the boat, and x-events: How likely are sorting events? In Tangled trees. Phylogeny, cospeciation, and coevolution, R. D. M. Page (ed.). University of Chicago Press, Chicago, Illinois, p. 287–309. ´ RAMIREZ ´ -RODRIGUEZ ´ ´ , A., A. , D. S. RICHARDSON, AND J. PE´REZ-TRIS. PEREZ 2013. Evolution of parasite island syndromes without long-term host population isolation: Parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography 22: 1272–1281. PE´REZ-TRIS, J., S. BENSCH, R. CARBONELL, A. J. HELBIG, AND J. L. ´ . 2004. Historical diversification of migration patterns in a TELLERIA passerine bird. Evolution 58: 1819–1832. ´ . 2002. Parasites and the ———, R. CARBONELL, AND J. L. TELLERIA blackcap’s tail: Implications for the evolution of feather ornaments. Biological Journal of the Linnaean Society 6: 481–492. PRICE, R. D., R. A. HELLENTHAL, R. L. PALMA, K. P. JOHNSON, AND D. H. CLAYTON. 2003. The chewing lice: World checklist and biological overview. Illinois Natural History Survey Special Publication 24, 501 p. RO´ZSA, L., J. REICZIGEL, AND G. MAJOROS. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86: 228–232. SANTIAGO-ALARCON, D., N. K. WHITEMAN, P. G. PARKER, R. E. RICKLEFS, AND G. VALKIUNAS. 2008. Patterns of parasite abundance and distribution in island populations of Galapagos endemic birds. Journal of Parasitology 94: 584–590. SHIRIHAI, H., G. GARGALLO, AND A. J. HELBIG. 2001. Sylvia warblers. Identification, taxonomy and phylogeography of the genus Sylvia. Princeton University Press, Princeton, New Jersey, 576 p. SYCHRA, O., AND I. LITERA´K. 2008. Myrsidea sylviae (Phthiraptera, Menoponidae), a new species of chewing louse from Sylvia atricapilla (Passeriformes, Sylviidae). Deutsche Entomologische Zeitschrift 55: 241–243. ———, ———, P. PODZEMNY´ , P. HARMAT, AND R. HRABA´K. 2011. Insect ectoparasites on wild birds in the Czech Republic during the prebreeding period. Parasite 18: 13–19. ´ , J. L., AND R. CARBONELL. 1999. Morphometric variation of five TELLERIA Iberian Blackcap Sylvia atricapilla populations. Journal of Avian Biology 30: 63–71.
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
J. Parasitol., 101(2), 2015, pp. 252–254 Ó American Society of Parasitologists 2015
Chewing Lice in Azorean Blackcaps (Sylvia atricapilla): A Contribution to Parasite Island Syndromes Ivan Litera´k, Oldˇrich Sychra, Roberto Resendes*, and Pedro Rodr´ıgues*, Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Palack´eho tˇr. 1/3, 61242 Brno, Czech Republic; *CIBIO, Centro de Investiga¸c˜ao em Biodiversidade e Recursos Gen´eticos, InBIO Laborat´ orio Associado, Polo dos A¸cores, Universidade dos A¸cores, 9501-801 Ponta Delgada, Portugal. Correspondence should be sent to: [email protected]
clearly impoverished to about 10% of the parasite diversity known for mainland blackcaps; all parasites shared between insular and continental blackcaps had lower prevalence in the island populations; and the island parasite assemblage was composed of parasites that were not specific to blackcaps, despite the fact that most parasites infesting continental blackcaps are host specific. This should have supported the idea that the mainland host–parasite associations are compromised on islands. Barrientos et al. (2014) studied both haemosporidians and ectoparasites of trumpeter finches (Bucanetes githagineus) from the Canary Islands, Iberian Peninsula, and northwestern Africa. They found the prevalence of haemosporidians to be higher in mainland populations even as ectoparasites, including chewing lice, had lower prevalence compared to those in the Canary Islands. We were focused upon chewing lice of blackcaps on the Azores. The Macaronesian archipelago of the Azores is situated in the Atlantic between 36855 0 and 39843 0 N and 25801 0 and 31807 0 W and is comprised of 9 islands. Their total surface area is about 2,250 km2, and the islands stretch more than 600 km from east to west. The nearest point on the mainland is Cabo Roca in Portugal, which is 1,408 km east of Santa Maria. In 2013, a total of 46 blackcaps were mist-netted on the Azores. Birds were captured at various sites on each of the 3 islands explored. Blackcaps were individualized with a metal ring. Totals of 17, 24, and 5 blackcaps from Sa˜o Miguel, Santa Maria, and Graciosa, respectively, were examined. Lice were collected using the fumigation chamber method (Clayton and Drown, 2001), and birds were released after examination. The lice samples were fixed in 96% ethanol and determined microscopically in the laboratory to species level. The chewing louse assemblage on blackcaps was characterized by louse species spectrum, prevalence as the percentage of blackcaps infested with parasites, mean intensity as the number of individuals of a particular chewing louse species on infested hosts, and mean abundance as the number of individuals of a particular chewing louse species on the examined birds (Bush et al., 1997). For comparing these parameters in Macaronesian blackcaps to European mainland blackcaps, we used the results from examining 240 blackcaps in the Czech Republic. We had examined blackcaps at various sites in the Czech Republic during 2004–2008. Blackcaps are commonly nesting and obligatory migrating birds in the Czech Republic. For statistical analyses, ´ we used Quantitative Parasitology 3.0 (Rozsa et al., 2000). We found 2 and 5 species of chewing lice in the Azores and in the Czech Republic, respectively (Table I). The lower number of species found in the Azores compared to the Czech Republic supports the idea that mainland host–parasite associations are compromised on islands and result in lower numbers of species on islands (Paterson et al., 2002). This is in accord with the results from studies of blackcap and trumpeter finch haemosporidians ´ ´ıguez et al., 2013; Barrientos et al., 2014). in Macaronesia (Perez-Rodr Only chewing louse species host specific to blackcaps (B. tovornikae and M. sylviae) were found on blackcaps in the Azores (Table I). Hence, we did not confirm that the island parasite assemblage was composed of parasites not specific to blackcaps, an idea postulated on the basis of a ´ ´ıguez et al., 2013). study of blackcap haemosporidians (Perez-Rodr Moreover, we found 2 chewing louse species not specific to blackcaps (M. curuccae and M. eurysternus) on blackcaps examined on the mainland.
ABSTRACT: Focusing upon chewing lice (Phthiraptera: Amblycera, Ischnocera) parasitizing blackcaps (Sylvia atricapilla) in the Azores (Portugal), we found a lower number of louse species in the Azores compared to mainland Europe. Only chewing lice host specific to blackcaps were found in the Azores. Louse prevalences were much higher in blackcaps from the Azores compared to those of various mainland populations. Chewing lice are permanent parasites of birds, and for such parasites the parasite island syndrome could be characterized by higher parasite prevalence on the islands compared to the mainland.
The aim of this paper is to characterize the chewing louse assemblage on blackcaps (Sylvia atricapilla) from the Azores while comparing this assemblage to that on blackcaps from mainland Europe to elucidate parasite island syndromes (Nieberding et al., 2006) regarding these permanent ectoparasites of birds. A comparison of parasite assemblages in hosts originating from the islands and the mainland is a key element to analyzing evolutionary changes of host–parasite interactions supposedly different in these 2 environments. Until now, parasite (chewing louse) island syndromes have been exceptionally studied in a bird species inhabiting both islands and the continental mainland (Barrientos et al., 2014). More such studies are needed for an understanding of parasite island syndromes. Blackcap is a common sedentary bird on all islands of the Azores. It comprises a monophyletic group including both island and mainland populations (Dietzen et al., 2008). An isolation between contemporary blackcap populations in mainland Europe and the Atlantic islands is of relatively recent origin, because blackcaps colonized the Macaronesian Islands probably during the past 4,000–40,000 yr through several ´ migration events from mainland Europe (Perez-Tris et al., 2004; Dietzen et al., 2008). Resident populations of blackcaps in Madeira and the Canary Islands coexist, with a regular annual influx of migrating and overwintering mainland blackcaps. The closer an island is to the continent, the greater the migrating contingent (Shirihai et al., 2001). To our knowledge, there is no record of mainland blackcaps overwintering in the Azores (Portugal). Hence, there is no presumed recent transport of mainland blackcap parasites to these islands. Chewing lice (Phthiraptera: Amblycera, Ischnocera) are ectoparasites of mammals and birds, living mainly on skin, feathers, or fur. Lice influence major avian life history traits, such as flight performance, host condition, reproductive success, survival, and sexual selection (Barbosa et al., 2002; Price et al., 2003). To date, 6 species of chewing lice have been documented as parasites in blackcaps: Brueelia neoatricapillae Price, Helenthal & Palma, 2003; Brueelia paratricapillae Price, Helenthal & Palma, 2003; Brueelia tovornikae (Bala´t, 1981); Menacanthus curuccae (Schrank, 1776); Menacanthus eurysternus (Burmeister, 1838); and Myrsidea sylviae Sychra & Litera´k, 2008 (Price et al., 2003; Sychra and Litera´k, 2008). ´ ´ıguez et al. (2013) studied the haemosporidian parasites of Perez-Rodr blackcaps on the Macaronesian archipelagos of Madeira and the Canary Islands. They found that the insular haemosporidian assemblage was DOI: 10.1645/14-601.1 252
SHORT COMMUNICATIONS
253
TABLE I. Chewing lice on blackcaps in the Azores (Sa˜o Miguel, Santa Maria, and Graciosa islands) and Czech Republic. Fisher’s exact test (for ´ prevalences) and bootstrap 2-sample t-test (for intensities and abundances) were used. Calculations were made in Quantitative Parasitology 3.0 (Rozsa et al., 2000).
Species Brueelia neoatricapillae
B. tovornikae
Menacanthus curuccae
M. eurysternus
Myrsidea sylviae
Chewing lice total
Characteristics of chewing louse assemblage Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance Prevalence (%) Mean intensity Intensity range Mean abundance
Sa˜o Miguel (nblackcaps ¼ 17)
Santa Maria (n ¼ 24)
0 0 0 0 70.6* 13.9 6 7.3 1–89 9.8 6 5.4* 0 0 0 0 0 0 0 0 64.7* 3.7 6 0.9* 1–10 2.4 6 0.7* 82.4* 14.9 6 6.6* 1–89 12.2 6 5.4*
0 0 0 0 20.8* 7.6 6 2–17 1.6 6 0 0 0 0 0 0 0 0 45.8* 2.1 6 1–5 1.0 6 54.2* 4.7 6 2–18 2.5 6
2.3 0.8†
0.3* 0.3* 1.2* 0.8*
Graciosa (n ¼ 5) 0 0 0 0 60.0* 4.7 6 1–11 2.8 6 0 0 0 0 0 0 0 0 40.0* 2.0 6 1–3 0.8 6 60.0* 6.0 6 2–11 3.6 6
2.6 1.9†
0.7† 0.5† 2.2† 1.8†
Czech Republic (n ¼ 240) 0.4 —‡ 1 0.004 6 0.004 0.4 —‡ 1 0.004 6 0.004 0.4 —‡ 1 0.004 6 0.004 1.3 2 6 0.5 1–3 0.025 6 0.015 0.8 1.0 6 0.0 1 0.008 6 0.005 3.3 1.4 6 0.2 1–3 0.05 6 0.02
* Significant. † Not significant statistical differences between data from the Azores and data from the Czech Republic. ‡ Only 1 bird was parasitized.
According to the geographical range hypothesis, we can predict that the number of parasite species per host should be positively correlated with host range (Gregory, 1990; Price et al., 2003). Our finding of a larger number of species of chewing lice on mainland blackcaps corroborates this hypothesis. The question remains whether mainland blackcaps acquired unspecific lice species through host-switching events between unrelated hosts or whether island blackcaps lost these lice through a so-called ‘‘missed the boat’’ event (Paterson et al., 2002). Our results revealed no significant differences in observed parasitological parameters among island populations. This is in accordance with Santiago-Alarcon et al. (2008) and Barrientos et al. (2014), who found the same pattern for chewing lice in the Galapagos Islands and Canary Islands, respectively. The observed chewing louse prevalences were much higher in blackcaps from the Azores compared to those observed in mainland Czech populations (Table I). This corresponds with findings from other parts of mainland Europe, where prevalences similar to those in the Czech ´ Republic were found: 9.5% in Spain, n ¼ 179 (Perez-Tris et al., 2002); 4.9% in Germany, n ¼ 61 (Frenzel, 2006); 4.0% in Hungary, n ¼ 25 (Z. Vas, pers. comm.); 3.8% in Romania, n ¼ 26 (C. Adam, pers. comm.); 3.3% in Greece, n ¼ 30 (A. Diakou, pers. comm.); 1.6% in Slovenia, n ¼ 62 (C. Adam, pers. comm.); and 1.5% in Sweden, n ¼ 131 (D. Gustafsson, pers. comm.). No lice were found on blackcaps in Bulgaria (n ¼ 69, M. Ilieva, pers. comm.) and Russia (n ¼ 88, O. Tolstenkov, pers. comm.). Our results are comparable with these data, because most of the aforementioned authors use the same fumigation chamber method for collecting lice. Moreover, mean intensities and mean abundances of parasites were higher in the Azores than on the mainland (Table I). The statistically
verified differences were striking in all cases of parasite prevalences and quite the opposite from the results for haemosporidians, where all parasites shared between insular and continental blackcaps had lower ´ ´ıguez et al., 2013). A prevalence in the island populations (Perez-Rodr reduced availability of appropriate vectors for haemosporidians had been offered as the explanation for the low number of parasite species and ´ ´ıguez et al., 2013). altered prevalence patterns on islands (Perez-Rodr Formerly, we had predicted significant differences in occurrence of chewing lice on migrating and resident birds (Sychra et al., 2011). An important aspect of migration’s evolution is that hosts may obtain an advantage in terms of reduced risks of parasitism by moving to areas that harbor lower densities of conspecifics. The risk of parasite infestation is usually density dependent (e.g., Begon et al., 1986), and a lower abundance of hosts in migratory as compared to resident populations may result in altered parasite–host dynamics. This effect may provide migrants with an initial benefit during the early stages of migration’s evolution (Møller and Erritzøe, 1998). Moreover, migratory bird species have more developed immune defence than do closely related resident species. This results from the exposure of migrants to a more diverse parasite fauna than that experienced by residents (Møller and Erritzøe, 1998). High parasite loads can be linked to increased thermoregulation costs and therefore lower fat stores. That, in turn, leads to less energy that can be devoted to flying (Barrientos et al., 2014). This can be important in the case of migratory birds. Because the life cycle of chewing lice occurs entirely on the host, environmental variability likely has less effect on the transmission dynamic of parasites. This suggests that their parasitological parameters—intensity, prevalence, and abundance—are equally variable (Santiago-Alarcon et al., 2008). We propose that differences of parasitological
254
THE JOURNAL OF PARASITOLOGY, VOL. 101, NO. 2, APRIL 2015
parameters between island and mainland populations of blackcaps found in this study can be correlated with migratory and ecological traits. This is in accordance with Teller ´ıa and Carbonell (1999), who had demonstrated that mainly these traits could explain morphological differences between the described subspecies of blackcap. Our results indicate that ectoparasites, including chewing lice, may play a role in bird migration and especially among small transcontinental passerine birds. Chewing lice are permanent parasites of birds, and for such parasites the parasite island syndrome could be characterized by higher parasite prevalence, mean intensity, and mean abundance on the islands compared to the mainland, as we demonstrated in blackcaps from the Azores compared to blackcaps from mainland Europe.
LITERATURE CITED BARBOSA, A., S. MERINO, F. DE LOPE, AND A. P. MØLLER. 2002. Effects of feather lice on flight behavior of male barn swallows. Auk 119: 213– 216. BARRIENTOS, R., F. VALERA, A. BARBOSA, C. M. CARILLO, AND E. MORENO. 2014. Biogeography of haemo- and ectoparasites of an arid-land bird, the trumpeter finch. Journal of Arid Environments 106: 11–17. BEGON, M., J. L. HARPER, AND C. R. TOWNSEND. 1986. Ecology: Individuals, populations and communities. Blackwell Scientific Publications, Oxford, U.K., 876 p. BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ, AND A. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583. CLAYTON, D. H., AND D. M. DROWN. 2001. Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). Journal of Parasitology 87: 1291–1300. ´ -DEL-REY, G. D. CASTRO, AND M. WINK. 2008. DIETZEN, C., E. GARCIA Phylogenetic differentiation of Sylvia species (Aves: Passeriformes) of the Atlantic islands (Macaronesia) based on mitochondrial DNA sequence data and morphometrics. Biological Journal of the Linnaean Society 95: 157–174. FRENZEL, K. 2006. Die Federlinge (Insecta: Phthiraptera: Ischnocera) durchziehender Singvoegel (Oscines) auf der Greifswalder Oie. Seevoegel 27: 2–6. GREGORY, R. D. 1990. Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4: 645–654. MØLLER, A. P., AND J. ERRITZØE. 1998. Host immune defence and migration in birds. Evolution and Ecology 12: 945–953.
NIEBERDING, C., S. MORAND, R. LIBOIS, AND J. R. MICHAUX. 2006. Parasites and the island syndrome: The colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33: 1212–1222. PATERSON, A. M., R. L. PALMA, AND R. D. GRAY. 2002. Drowning on arrival, missing the boat, and x-events: How likely are sorting events? In Tangled trees. Phylogeny, cospeciation, and coevolution, R. D. M. Page (ed.). University of Chicago Press, Chicago, Illinois, p. 287–309. ´ RAMIREZ ´ -RODRIGUEZ ´ ´ , A., A. , D. S. RICHARDSON, AND J. PE´REZ-TRIS. PEREZ 2013. Evolution of parasite island syndromes without long-term host population isolation: Parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography 22: 1272–1281. PE´REZ-TRIS, J., S. BENSCH, R. CARBONELL, A. J. HELBIG, AND J. L. ´ . 2004. Historical diversification of migration patterns in a TELLERIA passerine bird. Evolution 58: 1819–1832. ´ . 2002. Parasites and the ———, R. CARBONELL, AND J. L. TELLERIA blackcap’s tail: Implications for the evolution of feather ornaments. Biological Journal of the Linnaean Society 6: 481–492. PRICE, R. D., R. A. HELLENTHAL, R. L. PALMA, K. P. JOHNSON, AND D. H. CLAYTON. 2003. The chewing lice: World checklist and biological overview. Illinois Natural History Survey Special Publication 24, 501 p. RO´ZSA, L., J. REICZIGEL, AND G. MAJOROS. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86: 228–232. SANTIAGO-ALARCON, D., N. K. WHITEMAN, P. G. PARKER, R. E. RICKLEFS, AND G. VALKIUNAS. 2008. Patterns of parasite abundance and distribution in island populations of Galapagos endemic birds. Journal of Parasitology 94: 584–590. SHIRIHAI, H., G. GARGALLO, AND A. J. HELBIG. 2001. Sylvia warblers. Identification, taxonomy and phylogeography of the genus Sylvia. Princeton University Press, Princeton, New Jersey, 576 p. SYCHRA, O., AND I. LITERA´K. 2008. Myrsidea sylviae (Phthiraptera, Menoponidae), a new species of chewing louse from Sylvia atricapilla (Passeriformes, Sylviidae). Deutsche Entomologische Zeitschrift 55: 241–243. ———, ———, P. PODZEMNY´ , P. HARMAT, AND R. HRABA´K. 2011. Insect ectoparasites on wild birds in the Czech Republic during the prebreeding period. Parasite 18: 13–19. ´ , J. L., AND R. CARBONELL. 1999. Morphometric variation of five TELLERIA Iberian Blackcap Sylvia atricapilla populations. Journal of Avian Biology 30: 63–71.
