Miscel.lania Zoologica 23.2 (2000) 93 Lice and ticks parasitizing Audouin's Larus audouinii Payraudeau, 1826 (Aves, ) in the Chafarinas lslands (W Mediterranean)

M. Lafuente, V. Roca, Ma P. Martín-Mateo, E. Carbonell & A. Estrada

Lafuente, M., Roca, V., Martín-Mateo, Ma P., Carbonell, E. & Estrada, A,, 2000. Lice and ticks parasitizing Audouin's Gull Larus audouinii Payraudeau, 1826 (Aves, Laridae) in the Chafarinas lslands (W Mediterranean). Misc. Zool., 23.2: 93-102.

Lice and ticks parasitizing Audouin's Gull Larus audouinii Payraudeau, 7826 (Aves, Laridae) in the Chafarinas lslands (W Mediterranean).- Data on lice and ticks parasitizing are scarce. Here data on 58 adult and 10 young Audouin's gulls from the Chafarinas lslands are provided. Three species of chewing lice Austromenopon transversum (prevalencelmean intensity: 20%-2), Koeniginirmus punctatus (1 00%-15.5). and Saemundssonia lari (1 0%-3.2) and one tick Ornithodoros maritimus (100%-18) were found. A. transversum, S. lari, and 0. maritimus are recorded for the first time for L. audouinii

Key words: Chewing lice, Ticks, Larus audouinii.

(Rebut: 10 1 0 1; Acceptació condicional: 28 V 0 1; Acc. definitiva: 20 VI 01)

Mario Lafuente, Vicente Roca & Enrique Carbonell, Dept. de Biologia (Parasitologia Animal), Fac. de Ciencies Biologiques, Univ. de Valencia, cl Dr. Moliner 50, 46100-Burjasot, Valencia, Espanya (Spain).- M" Paz Martín-Mateo, Museo Nacional de Ciencias Naturales, cl José Gutiérrez Abascal2, 28006-Madrid, EspaRa (Spain).-Agustín Estrada, Dept. de Patología, Fac. de Veterinaria, Univ de Zaragoza, cl Miguel Servet 177, 50013-Zaragoza, EspaRa (Spain).

The taxonomic study of Mallophaga was financed by the Research Project "Fauna Ibérica IV" (DGICYT PB-95-0235).

O 2000 Museu de Zoologia 94 Lafuente et al. lntroduction The aim of this work was to provide data on ectoparasites of Audouin's gull from the Audouin's gull, Larus audouinii Payraudeau Chafarinas Islands. 1826, is an endemic species in the western Mediterranean during its breeding period, having its most numerous breeding colonies Materials and methods in Spain (more than 90% of the breeding population in the world, see PEDROCCHI& Of the Spanish breeding colonies of Larus RUIZ, 1995). audouinii, one of the most important is lnformation about the ectoparasites of that on the Chafarinas lslands (ÁLVAREZ, Larus audouinii is very scarce, the only data 1992). From 1993 to 1995, the ectoparasite available to date being the study by fauna in this colony of Audouin's gulls was TIMMERMANN(1952) on ectoparasites of some studied. The Chafarinas lslands are located specimens. There is also little information in the West Mediterranean at 35" 11' N, available on the ectoparasites of other 2" 26' W (fig. 1). The archipelago is formed species of gulls (TIMMERMANN,1952; CASADO by three volcanic islands covered by ESCRIBANOet al., 1985; GUIGUENet al., 1986; xerophytic scrub. Mean annual temperature CHASTELet al., 1987; GUIGUENet a1.,1989; is around 18"C, and mean annual rainfall is MART~N-MATEO,1989). 360mm (ÁLVAREZ,1992).

1 fl Mediterranean Sea

Chafarinas :i;;:

de 30 km

Congreso Isabel II lsland lsland0 %Francisco

137 m Mediterranean Sea @ 500 m Miscel.lania Zoologica 23.2 (2000) 9 5

Two of the three islands, Rey lsland and 1954; CLAY,1959; ZLOTORZYCKA,1968). Congreso lsland, are uninhabited and harbour Table 1 shows the measurements of the colonies of Audouin's gull. Isabel II lsland is specimens found in L. audouinii. inhabited by scientists and military personnel, and no breeding colonies have settled there. Koeniginirmus punctatus (fig. 3) The sampling was done during the breeding seasonsfrom 1993 to 1995: ¡"total, Examined material: 558, 71? 10 young were caught by hand and 58 Prevalence: 100% adult gulls were caught during the incubation Mean intensity: 15.5 season. Adult birds were captured by means The body, practically colourless, shows a of nest traps (LAFUENTE,1997). After capture, series of pigmented black marks with were given an overdose of chloro- characteristic arrangement. These marks form and examined in situ. show slight differences between dorsal and Feathers from the head, wings, body and ventral sides in both sexes (fig. 3). tail were examined for ectoparasites. We Measurements are indicated in table 2. used visual examination for both lice and ticks, standardizing the examination by Saemundssonia lari (fia. 4) searching defined areas of the host for a constant amount of time (CLAYTON& WALTHER, Examined material: 68, 59 1997). A total of 22 nests for ticks were Prevalence: 10% sampled in situ also by visual examination, Mean intensity: 3.2 ¡.e. counting the number of individuals visible The morphological features, measurements in the nest (LEE& CLAYTON,1995). Some authors (table 3) and chaetotaxy agree with the (see CLAYTON& WALTHER, 1997) found that the descriptions of the species (TIMMERMANN,1951; number of ectoparasites visible in the nests is highly correlated with the total collected by subsequent destruction and sifting of nests. Ornithodoros maritimus The collected specimens were isolated and conserved in 70% alcohol. For taxonomic study, Examined material: 58, 59, 5 larvae they were clarified and mounted in Hoyer Prevalence: 100% (in young birds) medium (KRANTZ,1978). Prevalence and mean Mean intensity: 18 (in young birds) intensity were calculated according to BUSHet This is a common species whose detailed al. (1997). although the value of mean intensity morphology is described in VERMEIL& should only be considered as indicative. MARGUET(1 967) and HOOGSTRAALet al. (1 976). The specimens studied agree with these descriptions. Results Among the 22 examined nests, we found a mean number of 7.2 ticks (mainly adults) Four ectoparasitespecies were found on Larus per nest. Among the 10 young birds audouinii: the chewing lice Austromenopon (unfledged gulls), we found mainly larvae (a transversum (Denny, 1842) (Mallophaga, maximum of 49 on one ). Three adult Menoponidae), Koeniginirmus punctatus ticks were recovered from the nasal cavities (Timmermann, 1952). Saemundssonia lari of two young hosts. No ticks were found on (Fabricius, 1870) (Mallophaga, Philopteridae), adult gulls. and the tick Ornithodoros maritimus (Vermeil et Marguet, 1967) (Acarina, Argasidae). Discussion ~u;tromeno~on transversum (fig. 2) TIMMERMANN(1954) considered al1 the described Examined material: 18. 29 species of Austromenopon (Denny, 1842) from Prevalence: 20% gulls (Larinae) belonging to A. transversum Mean intensity: 2 species, the nominal subspecies being A. t. These specimens show the main mor- transversum. This opinion is accepted by most phological features of the species (TIMMERMAN,authors. In fact, ZLOTORZYCKA(1968) studied 96 Lafuente et al:

-Irnrn

100 pm 200 prn Miscel.lania Zoologica 23.2 (2000) 97

Fig. 3. Koeniginirmus punctatus: A. Q dorsal view. B. Q ventral view; C. a" dorsal view; D. a" ventral view; E. 8 posterior end, dorsal view; F. a" posterior end, ventral view; G. Egg attached to a feather; H. Genitalia. Koeniginirmus punctatus:A. Q vista dorsal. B. 9 vista ventral; C. a" vista dorsal; D. d vista ventral; E. a" parte trasera posterior; vista dorsal; E a" parte trasera posterior, vista ventral; G. Huevo unido a una pluma; H. Genitalia. 98 Lafuente et al.

1 mrn Miscel.lania Zoologica 23.2 (2000) 99

Pontoppidan, 1763 and L. ridibundus L. (MART~N-MATEO,1989). K. punctatus was included by some authors in the genus Nirmus Burmeister, 1838 (WATERSON 1914). EICHLER(1940) designated it as the type species of the new genus Koeniginirmus for parasites of Laridae, showing charaderistic partial chromatism in the body. Other authors do not consider this genus as valid and include K. punctatus in different genera, Degeeriella (Seguy 1944), and Quadraceps (HOPKINS& CLAY, 1953; EMERSON,1972; LEDGER,1980). ZLOTORZYCKA (1 967) considered the genus Koeniginirmus as valid and differentiated K. punctatus from two other similar species parasitizing Larus spp, K. lingulatus Waterson, 1914 and K. felix Giebel, 1874. TIMMERMANN(1952) established eight phylogenetic forms for K. punctatus that developed varying pigmentation patterns, from K. p. felix (the most pigmented form) to K. p. pallidus. Our specimens belong to K. p. regressus, the third less pigmented form, four different subspecies from four species of found by TIMMERMANN(1952) on yellow-legged Larus and concluded that there are very few gull, L. cachinnans Pallas 181 1 and also on L. differences among them and from the nominal audouinii. subspecies. Our specimens are very similar to According to LEDGER(1980), al1 descriptions those described by these authors, showing of the genus Saemundssonia may be only minor biometric differences probably considered as S. lari sensu lato, although dueto adaptation to the host. This is the first some authors (TIMMERMANN,1951; ZLOTORZYCKA, record of this chewing lice on L. audouinii, 1978) recognized several subspecies of S. previously cited in Spain on L. argentatus lari. Our specimens are very similar to those 1O0 Lafuente et al.

described by TIMMERMANN(1952) and Resumen ZLOTORZYCKA(1961) with small differences in their measurements. Although this species Ectoparásitos de la gaviota de Audouin Larus has wide holarctic distribution and a wide audouinii Payraudeau, 1826 (Aves, Laridae) range of hosts (DELHOYO et al., 1996; EMERSON, en las islas Chafarinas (Mediterráneo 1972), this constitutes its first record on L. sudoccidental) audouinii. In Spain, this species was found on L. argentatus and L. ridibundus (CASADO Se ha llevado a cabo por vez primera en España ESCRIBANOet al., 1985; MART~N-MATEO,1989). un estudio de los ectoparásitos de la gaviota O. maritimus is a member of the coniceps- de Audouin, Larus audouinii en su colonia de capensis group (MANILLA,1990) which includes cría de las Islas Chafarinas (fig. 1). Se detecta- ticks living in rocky xeric areas used as breeding ron tres especies de piojos masticadores, colonies by many marine birds. Its presence in Austromenopon transversum (fig. 2, tabla l), one of the rnost important colonies of L. Koeniginirmus punctatus (fig. 3, tabla 2) y audouinii is not therefore surprising. However, Saemundssonia lar; (fig. 4, tabla 3) y una garra- GUIGUENet al. (1986) recorded O. maritimus in pata, Ornithodoros maritimus, de todas las many species of marine birds from Corsica, cuales se ofrecen los valores de prevalencia e but not on L. audouinii. Therefore, this is the intensidad media y sus dimensiones. A. first record on L. audouinii. transversum, S. lar; y O. maritimus se citan por We have not found any quantitative data primera vez para L. audouinii. about infection of these ectoparasite species transmitted to L. audouinii or other gull species. Only for Ornithodorus marítímus Acknowledgements some data showing hyperinfection by ticks, I have been published. Thus GUIGUEN& MONAT The authors thank Enrique Rico (University (1985) found 210 individuals in a nest of the of Valencia), M" Carmen del Arco (University gull Rissa tridactyla L. Chastel et al (CHASTEL of Salamanca), Georgina Álvarez (ICONA), et al., 1987) found 759, 931 and 3,503 Jacob González-Solis, Joan Carles Abella, individuals respectively on three young birds Nuria Bertomeu, Vittorio Pedrocchi (Uni- of Rissa tridacwa. And MANILLA(1 990) found versity of Barcelona) and the personnel 900 individuals in a nest of Larus cachinnans. from GENA (Antonio Barón, Gonzalo Hyperinfection has not been found in L. Martínez) for their help in collecting audouinii of Chafarinas Islands. specimens of gulls in the field. Misce1,lania Zooloaica 23.2 (2000)

This study is part of a project financed by Oiseaux marins nicheurs du midi et de la the DGCONA (Spain) which also provided Corse. Ann. du C.R.O.P., 2: 23-26, Aix en the capture licences for birds. The Ministry Provence. of Defence provided al1 licences for non- GUIGUEN,C., MONNAT,J. Y. & THIBAULT,J. C., military personnel movements and helped 1986. Apports a la connaissance des tiques with the transport of material to the islands. (Ixodoidea) d'oiseaux marins en France continentale et en Corse. Bull. Soc. Fr. Parasitol., 4: 267-272. References GUIGUEN,C., TEIXEIRA,A. M., & MONNAT,J. Y., 1989. Xenopsylla gra tiosa (Siphonaptera, ÁLVAREZ,C., 1992. Conservation programme Pulicidae) y Ornithodoros maritimus for Audouin's Gull in the Chafarinas (Acarina, Ixodoidae, Argasidae), ecto- Islands. Avocetta, 16: 63-66. parásitos hematófagos de aves marinas, BUSH,A. O., LAFFERTY,K. D., LOR, J. M. & nuevos para Portugal. Rev. Ibér. Parasitol., SHOSTAK, A. W., 1997. Parasitology meets 49: 177. ecology on its own terms: Margolis et al. HOOGSTRAAL,H., CLIFFORD,C. M., KEIRANS,J. E., revisited. J. Parasitol., 83: 575-583. KAISER,M. N., & EVANS,D. E., 1976. The CASADOESCRIBANO, N., JIMÉNEZ GONZALEZ,A., Ornithodoros (Alectorobius) capensis CRIADOFORNELIO, A. & RODR~GUEZCAABEIRO, F., group (Acarina: lxodoidea: Argasidae) of 1985. Estudio comparativo de los maló- the Palearctic and Oriental Regions: O. fagos parásitos de Larus argentatus (A,) maritimus. J. Parasitol., 62: 799-81 0. Pontoppidan y Larus ridibundus L. IV HOPKINS,G. H. E., & CLAY,T., 1953. Additions Congr. Nac. Parasitol., Tenerife: 74. and corrections to the check list of CLAY, T., 1959. Key to the species of Mallophaga. Ann. Mag. Nat. Hist. (ser. Austromenopon Bedford (Mallophaga) 12), 6: 434-448. parasitic on the . Proc. R. KRANTZ,G. W., 1978. A Manual ofAcarology. Ent. Soc. London (Ser. B), 28: 11-1 2. Second edition. Oregon State University CLAYTON,D. H. & WALTER,B.A., 1997. Collection Book Stores, Inc., Corvallis (OR). and quantification of arthropod parasites LAFUENTE,M., 1997. Estudio parasitológico de of birds. In: Host-parasite evolutíon. la gaviota de Audouin, Larus audouinii, General principies and avian models: 41 9- en su colonia de cría de las islas Chafarinas 440. (D. H. Clayton & J. Moore, Eds.). (Mediterráneo sudoccidental). Tesis Oxford University Press, Oxford. Doctoral, Universitat de Valencia. CHASTEL,C., MONNAT,J. Y., LELAY, C., & BALOUET, LEDGER,J. A., 1980. The arthropod parasites C., 1987. lnfestation et hyperinfestation of vertebrates in Africa. South of the de la mouette tridactyle, Rissa tridactyla Sahara. Vol. IV. Phthiraptera. Publ. South L., par des tiques lxodes (Ceratixodes) Afr. Inst. Med. Res., 56: 1-327. uriae, Ornithodoros (Alectorobius) LEE,P. L. M. & CLAYTON,D. H., 1995. Population maritimus; consequences pathologiques. biology of swift (Apus apus) ectoparasites Ann. Parasitol. Hum. Comp., 62: 492-504. in relation to host reproductive succes. DELHOYO, J., ELLIOT,A. & SARGATAL, J. (Eds.), Ecological Entomology, 20: 43-50. 1996. Handbook ofthe Birds of the World. MANILLA,C., 1990. Ornithodoros (Alectorobius) Vol. 3. Hoatzin to . Lynx, Barcelona. maritimus (Ixodoidea: Argasidae) specie EICHLER,W. D., 1940. Notulae mallopha- nuova in Italia e osservazioni su1 gruppo gologicae IV. Neue Gattungen und hohere coniceps-capensis. Parassitologia, 32: 265-274. Einheiten von Kletterfederlingen. Zoolo- MARTIN-MATEO,M. P., 1989. Estado actual del gischer. Anzeiger, 130: 97-1 03. conocimiento sobre los malófagos (Insecta) EMERSON,K. C., 1972. Ckeck list of the parásitos de aves y mamíferos en España. Mallophaga of north America (north of Rev. Ibér. Parasitol., 49: 387-41 0. Mexico) Part l. Ischnocera. Deseret Test PEDROCCHI,V. & RUIZ, X., 1995. On the current Center, Dugway. status of Audouin's Gull (Larus audouini~)in GUIGUEN,C. & MONNAT,J. Y., 1985. Facteurs the Mediterranean. In: Threats to : influencant I'évolution des effectifs Proceedings ofthe 5th Interna tional d'oiseaux marins: les ectoparasites. In: Group Conference: 1-38 (M. L. Tasker, Ed.). 102 Lafuente et al.

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