Data on lice and ticks parasitizing gulls 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 (100%-15.5). and Saemundssonia lari (10%-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.Data on lice and ticks parasitizing gulls 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 (100%-15.5). and Saemundssonia lari (10%-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.Data on lice and ticks parasitizing gulls 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 (100%-15.5). and Saemundssonia lari (10%-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

Carbonell, E.

Estrada, A.

Lafuente, M.

Martín-Mateo, María Paz

Roca, V.

Revistes Catalanes amb Accés Obert

Miscel.lania Zoologica 23.2 (2000) 93 
Lice and ticks parasitizing 
Audouin's Gull Larus audouinii 
Payraudeau, 1826 (Aves, Laridae) 
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 gulls 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 t ime 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 Animal (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, c l  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 
Audouin's gull, Larus audouinii Payraudeau 
1826, is an endemic species in the western 
Mediterranean during its breeding period, 
having i t s  most numerous breeding colonies 
in Spain (more than 90% of the breeding 
population in the world, see PEDROCCHI & 
RUIZ, 1995). 
lnformation about the ectoparasites of 
Larus audouinii is very scarce, the only data 
available t o  date being the study by 
TIMMERMANN (1952) on ectoparasites of some 
specimens. There is also little information 
available on the ectoparasites of other 
species of gulls (TIMMERMANN, 1952; CASADO 
ESCRIBANO et al., 1985; GUIGUEN et al., 1986; 
CHASTEL et al., 1987; GUIGUEN et a1.,1989; 
MART~N-MATEO, 1989). 
The aim of this work was to  provide data 
on ectoparasites of Audouin's gull from the 
Chafarinas Islands. 
Materials and methods 
Of the Spanish breeding colonies of Larus 
audouinii, one of the most important is 
that on the Chafarinas lslands (ÁLVAREZ, 
1992). From 1993 t o  1995, the ectoparasite 
fauna in this colony of Audouin's gulls was 
studied. The Chafarinas lslands are located 
in the West Mediterranean at 35" 11' N, 
2" 26' W (fig. 1). The archipelago is formed 
by three volcanic islands covered by 
xerophytic scrub. Mean annual temperature 
is around 18"C, and mean annual rainfall is 
360mm (ÁLVAREZ, 1992). 
1 f l  Mediterranean Sea 
Chafarinas 
: i;;: 
30 km de 
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 birds 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 wi th  
animals were given an overdose of chloro- characteristic arrangement. These marks 
form and examined in  situ. 
Feathers from the head, wings, body and 
tail were examined for ectoparasites. We 
used visual examination for both lice and 
ticks, standardizing the examination by 
searching defined areas of the host for a 
constant amount of  time (CLAYTON & WALTHER, 
1997). A total of 22 nests for ticks were 
sampled in  situ also by visual examination, 
¡.e. counting the number of individuals visible 
in the nest (LEE & CLAYTON, 1995). Some authors 
(see CLAYTON & WALTHER, 1997) found that the 
number of ectoparasites visible in the nests 
is highly correlated with the total collected 
by subsequent destruction and sifting of nests. 
The collected specimens were isolated and 
conserved in 70% alcohol. For taxonomic study, 
they were clarified and mounted in Hoyer 
medium (KRANTZ, 1978). Prevalence and mean 
intensity were calculated according to  BUSH et 
al. (1997). although the value of mean intensity 
should only be considered as indicative. 
Results 
show slight differences between dorsal and 
ventral sides in both sexes (fig. 3). 
Measurements are indicated in table 2. 
Saemundssonia lari (f ia. 4) 
Examined material: 68, 59 
Prevalence: 10% 
Mean intensity: 3.2 
The morphological features, measurements 
(table 3) and chaetotaxy agree with the 
descriptions of the species (TIMMERMANN, 1951; 
Ornithodoros maritimus 
Examined material: 58, 59, 5 larvae 
Prevalence: 100% (in young birds) 
Mean intensity: 18 (in young birds) 
This is a common species whose detailed 
morphology is described in VERMEIL & 
MARGUET (1 967) and HOOGSTRAAL et al. (1 976). 
The specimens studied agree with these 
descriptions. 
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 bird). 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 
Prevalence: 20% 
Mean intensity: 2 
species of Austromenopon (Denny, 1842) from 
gulls (Larinae) belonging to A. transversum 
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 e t  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 t o  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 e t  al. 
1 mrn 
Miscel.lania Zoologica 23.2 (2000) 99 
four different subspecies from four species of 
Larus and concluded that there are very few 
differences among them and from the nominal 
subspecies. Our specimens are very similar to 
those described by these authors, showing 
only minor biometric differences probably 
dueto adaptation to  the host. This is the first 
record of this chewing lice on L. audouinii, 
previously cited in Spain on L. argentatus 
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, 
1 953; 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) 
t o  K. p. pallidus. Our specimens belong to  K. 
p. regressus, the third less pigmented form, 
found by TIMMERMANN (1952) on yellow-legged 
gull, L. cachinnans Pallas 181 1 and also on L. 
audouinii. 
According to  LEDGER (1980), al1 descriptions 
o f  the genus Saemundssonia may be 
considered as S. lari sensu lato, although 
some authors (TIMMERMANN, 1951; ZLOTORZYCKA, 
1978) recognized several subspecies of S. 
lari. Our specimens are very similar t o  those 
1 O0 Lafuente et al. 
described by  TIMMERMANN (1952) and 
ZLOTORZYCKA (1961) w i th  small differences in  
their measurements. Although this species 
has wide holarctic distribution and a wide 
range o f  hosts (DEL HOYO et al., 1996; EMERSON, 
1972), this constitutes i t s  first record on L. 
audouinii. In Spain, this species was found 
on L. argentatus and L. ridibundus (CASADO 
ESCRIBANO et  al., 1985; MART~N-MATEO, 1989). 
O. maritimus is a member o f  the coniceps- 
capensis group (MANILLA, 1990) which includes 
ticks living in rocky xeric areas used as breeding 
colonies by many marine birds. Its presence in 
one of the rnost important colonies of L. 
audouinii is not therefore surprising. However, 
GUIGUEN et al. (1986) recorded O. maritimus in 
many species of marine birds from Corsica, 
but not on L. audouinii. Therefore, this is the 
first record on L. audouinii. 
We have not  found any quantitative data 
about infection o f  these ectoparasite species 
transmitted t o  L. audouinii or other gull 
species. Only for Ornithodorus marítímus 
some data showing hyperinfection by ticks, 
have been published. Thus GUIGUEN & MONAT 
(1985) found 210 individuals in a nest o f  the 
gull Rissa tridactyla L. Chastel et al (CHASTEL 
et al., 1987) found 759, 931 and 3,503 
individuals respectively on  three young birds 
o f  Rissa tridacwa. And MANILLA (1 990) found 
900 individuals in a nest o f  Larus cachinnans. 
Hyperinfection has not  been found in  L. 
audouinii o f  Chafarinas Islands. 
Resumen 
Ectoparásitos de la gaviota de Audouin Larus 
audouinii Payraudeau, 1826 (Aves, Laridae) 
en  las islas Chafarinas (Mediterráneo 
sudoccidental) 
Se ha llevado a cabo por vez primera en España 
un estudio de los ectoparásitos de la gaviota 
de Audouin, Larus audouinii en su colonia de 
cría de las Islas Chafarinas (fig. 1). Se detecta- 
ron tres especies de piojos masticadores, 
Austromenopon transversum (fig. 2, tabla l), 
Koeniginirmus punctatus (fig. 3, tabla 2) y 
Saemundssonia lar; (fig. 4, tabla 3) y una garra- 
pata, Ornithodoros maritimus, de todas las 
cuales se ofrecen los valores de prevalencia e 
intensidad media y sus dimensiones. A. 
transversum, S. lar; y O. maritimus se citan por 
primera vez para L. audouinii. 
Acknowledgements I 
The authors thank Enrique Rico (University 
of Valencia), M" Carmen del Arco (University 
o f  Salamanca), Georgina Álvarez (ICONA), 
Jacob González-Solis, Joan Carles Abella, 
Nuria Bertomeu, Vittorio Pedrocchi (Uni- 
versity o f  Barcelona) and the personnel 
f r o m  GENA (Anton io  Barón, Gonzalo 
Martínez) fo r  their  help in  collecting 
specimens o f  gulls in the field. 
Misce1,lania Zooloaica 23.2 (2000) 
This study is part o f  a project financed by 
the DGCONA (Spain) which also provided 
the capture licences for birds. The Ministry 
o f  Defence provided al1 licences for non- 
military personnel movements and helped 
wi th the transport o f  material t o  the islands. 
Ref erences 
ÁLVAREZ, C., 1992. Conservation programme 
for  Audouin's Gull in the Chafarinas 
Islands. Avocetta, 16: 63-66. 
BUSH, A. O., LAFFERTY, K. D., LOR, J. M. & 
SHOSTAK, A. W., 1997. Parasitology meets 
ecology o n  i t s  own  terms: Margolis e t  al. 
revisited. J. Parasitol., 83: 575-583. 
CASADO ESCRIBANO, N. JIMÉNEZ GONZALEZ, A., 
CRIADO FORNELIO, A. & RODR~GUEZ CAABEIRO, F., 
1985. Estudio comparativo de los maló- 
fagos parásitos de Larus argentatus 
Pontoppidan y Larus ridibundus L. I V  
Congr. Nac. Parasitol., Tenerife: 74. 
CLAY, T., 1959. Key t o  t h e  species o f  
Austromenopon Bedford (Mallophaga) 
parasitic on  the Charadriiformes. Proc. R. 
Ent. Soc. London (Ser. B), 28: 1 1-1 2. 
CLAYTON, D. H. & WALTER, B.A., 1997. Collection 
and quantification o f  arthropod parasites 
o f  birds. In: Host-parasite evolutíon. 
General principies and avian models: 41 9- 
440. (D. H. Clayton & J. Moore, Eds.). 
Oxford University Press, Oxford. 
CHASTEL, C., MONNAT, J. Y., LE LAY, C., & BALOUET, 
C., 1987. lnfestation et hyperinfestation 
de la mouette tridactyle, Rissa tridactyla 
L., par des tiques lxodes (Ceratixodes) 
uriae, Orn i thodoros  (Alectorobius)  
maritimus; consequences pathologiques. 
Ann. Parasitol. Hum. Comp., 62: 492-504. 
DEL HOYO, J., ELLIOT, A. & SARGATAL, J. (Eds.), 
1996. Handbook o f  the Birds o f  the World. 
Vol. 3. Hoatzin t o  Auks. Lynx, Barcelona. 
EICHLER, W. D., 1940. Notulae mallopha- 
gologicae IV. Neue Gattungen und hohere 
Einheiten von Kletterfederlingen. Zoolo- 
gischer. Anzeiger, 130: 97-1 03. 
EMERSON, K. C., 1972. Ckeck l ist o f  the 
Mallophaga o f  north America (north o f  
Mexico) Part l. Ischnocera. Deseret Test 
Center, Dugway. 
GUIGUEN, C. & MONNAT, J. Y., 1985. Facteurs 
inf luencant I 'évolution des effectifs 
d'oiseaux marins: les ectoparasites. In: 
Oiseaux marins nicheurs du mid i  e t  de la 
Corse. Ann. du C.R.O.P., 2: 23-26, Aix en 
Provence. 
GUIGUEN, C., MONNAT, J. Y. & THIBAULT, J. C., 
1986. Apports a la connaissance des tiques 
(Ixodoidea) d'oiseaux marins en France 
continentale et en Corse. Bull. Soc. Fr. 
Parasitol., 4: 267-272. 
GUIGUEN, C., TEIXEIRA, . M., & MONNAT, J. Y., 
1 989. Xenopsylla gra tiosa (Siphonaptera, 
Pulicidae) y Ornithodoros marit imus 
(Acarina, Ixodoidae, Argasidae), ecto- 
parásitos hematófagos de aves marinas, 
nuevos para Portugal. Rev. Ibér. Parasitol., 
49: 177. 
HOOGSTRAAL, H., CLIFFORD, C. M., KEIRANS, J. E., 
KAISER, M. N., & EVANS, D. E., 1976. The 
Ornithodoros (Alectorobius) capensis 
group (Acarina: lxodoidea: Argasidae) of 
the Palearctic and Oriental Regions: O. 
(A,) maritimus. J. Parasitol., 62: 799-81 0. 
HOPKINS, G. H. E., & CLAY, T., 1953. Additions 
and corrections t o  the  check list o f  
Mallophaga. Ann. Mag. Nat. Hist. (ser. 
12), 6: 434-448. 
KRANTZ, G. W., 1978. A Manual o f  Acarology. 
Second edition. Oregon State University 
Book Stores, Inc., Corvallis (OR). 
LAFUENTE, M., 1997. Estudio parasitológico de 
la gaviota de Audouin, Larus audouinii, 
en su colonia de cría de las islas Chafarinas 
(Medi terráneo sudoccidental). Tesis 
Doctoral, Universitat de Valencia. 
LEDGER, J. A., 1980. The arthropod parasites 
o f  vertebrates in Africa. South o f  the 
Sahara. Vol. IV. Phthiraptera. Publ. South 
Afr. Inst. Med. Res., 56: 1-327. 
LEE, P. L. M. & CLAYTON, D. H., 1995. Population 
biology o f  swift (Apus apus) ectoparasites 
in relation t o  host reproductive succes. 
Ecological Entomology, 20: 43-50. 
MANILLA, C., 1990. Ornithodoros (Alectorobius) 
maritimus (Ixodoidea: Argasidae) specie 
nuova in Italia e osservazioni su1 gruppo 
coniceps-capensis. Parassitologia, 32: 265-274. 
MARTIN-MATEO, M. P., 1989. Estado actual del 
conocimiento sobre los malófagos (Insecta) 
parásitos de aves y mamíferos en España. 
Rev. Ibér. Parasitol., 49: 387-41 0. 
PEDROCCHI, V. & RUIZ, X., 1995. On the current 
status o f  Audouin's Gull (Larus audouini~) in 
the Mediterranean. In: Threats to seabirds: 
Proceedings o f  the 5th Interna tional Seabird 
Group Conference: 1-38 (M. L. Tasker, Ed.). 
102 Lafuente et al. 
Seabird Group, Sandy. 
TIMMERMANN, C., 1951. Die Movenkneifer. Eine 
Revision samtlicher bei echten Moven 
schmarotzenden Federlinge der Gattung 
Saemundssonia Timm., 1936. Parasit. News 
Reykjavik, 2: 1-12. 
- 1952. The species of the genus Quadraceps 
(Mallophaga) from the Larinae, with some 
remarks on the systematic and the 
phylogeny of the gulls. Part I and II. Ann. 
Mag. Natl. Hist. (Ser. 12), 5: 209-222. 
- 1954. Vorlaufiger Ubersicht über das 
Amblycerengenus Austromenopon Bedford, 
1939 (Mallophaga). Bonn. zool. Beitr., 5: 
195-206. 
VERMEIL, C. & MARGUET, S.  1967. Sur le 
diagnostic des larves d'ornithodores du 
complexe coniceps-capensis (Acarina: 
Argasidae) Ornithodoros coniceps (Canes- 
trini 1890) maritimus n. ssp. prevaut dans 
les lles de basse Bretagne. Acarologia, 9: 
557-565. 
WATERSON, J., 1914. On some ectoparasites in 
the South African Museum, Cape Town. 
Ann. Sth. Afr. Mus., 10: 271-324. 
ZLOTOR~YCKA, J., 1961. Mallophaga from birds 
associated with the water environment 
in Poland. Acta Zool. Crac., 6: 273-343. 
- 1967. Studien über Quadraceps s. l. 
(Mallophaga: Quadraceptinae). Ubersicht 
der Arten und systematische Revision mit 
besonderer Berücksichtigung der syn- 
hospitalen und allohospitalen Arten. Polski 
Pismo Entomologizne, 37: 705-785. 
- 1968. Systematische Studien an den 
mitteleuropaischen Arten der Gattung 
Austromenopon Bedford (Mallophaga: 
Austromenoponinae). Polski Pismo Ento- 
mologizne, 37: 301-340. 
- 1978. Klucze do oznaczaina owadow 
Polski. XV. Mallophaga 5. Philopteroidea, 
Rallicolidae. Polish. Ent. Soc., 28: 1-86. 


Lice and ticks parasitizing Audouin's Gull Larus audouinii Payraudeau, 7826 (Aves, Laridae) in the Chafarinas Islands (W Mediterranean)

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