Carbonell, E.

Lafuente, M.

Roca, V.

Revistes Catalanes amb Accés Obert

Miscel.lania Zoologica 21.2 (1998) 105 
Trematodes of Audouin's gull, 
Larus audouiníí (Aves, Laridae), 
from Chafarinas lslands 
(W Mediterranean) 
M. Lafuente, V. Roca & E. Carbonell 
Lafuente, M . ,  Roca, V. & Carbonell, E . ,  1998. Trematodes of Audouin's gull, Larus audouinii (Aves, 
Laridae), from Chafarinas lslands (W Mediterranean). Misc. Zool., 21.2: 105-1 12. 
Trematodes of Audouin 3 gull, La rus audouinii (Aves, Laridae), from Chafarinas lslands (W Mediterra- 
nean).-A survey was carried out on the trematode fauna of Larus audouinii Payraudeau, 1826 (Aves, 
Laridae) in the Alboran Sea, south-western Mediterranean. A total of 10 trematode species was found: 
Sch/josomaatinae gen. sp., Ornithobilharzia sp., Pachytrerna calculus, Renico/a lar( Brachylecithurn 
microtesticulaturn, Condylocotyla pilodora, Knipowitschiatrema nicolai, Cardiocephalus longicollis, 
Acanthotrema armata and Aporchis rnassiliensis. The main morphoanatomic characteristics of helrninths 
and the ecological host-parasite relationships are presented. L. audouinii becomes a new host for the 10 
trematode species. 
Key words: Trernatoda, Laridae, Larus audouinii, Spain. 
(Rebut: 23 XII 97; Acceptació condicional: 18 V 98; Acc. definitiva: 15 IX 98) 
M .  Lafuente, V: Roca & E. Carbonell, Dept. de Biologia Animal (Parasitologia Animal), Fac. Ciencies 
Biologiques, Univ. de Valencia, Dr. Moliner 50, 46 100 Burjassot (Valencia), Espafia (Spain). 
This work was financed by Dirección General de Conservación del Medio Ambiente which also gave the 
licences for capture of animals. 
ISSN: 021 1-6529 O 1998 Museu de Zoologia 
Lafuente et al. 
lntroduction 
Although a large number of parasitological 
studies have been carried out on many gull 
species, no reference has yet been made t o  
helminth fauna of Audouin's gull, Larus 
audouinii Payraudeau, 1826 (Aves, Laridae). 
During its breeding period Audouin's gull i s  
an endemic species in the western Mediter- 
ranean, with the most numerous breeding 
colonies being in Spain. PEDROCCHI & RUIZ 
(1995) indicate that more than 90% of the 
world's breeding population of this gull, 
breeds in Spain. 
This species i s  catalogued by the Inter- 
national Union for Conservation of Nature, 
as "conservation-dependent" (MACE & COL- 
LAR, 1994). and among the 5% of European 
animal species that require strong efforts to  
be made for their conservation. For this rea- 
son, the Dirección General de Conservación 
del Medio Ambiente (Spain) promoted and 
financed research into the biology and 
ecology of this gull species in several breed- 
ing areas, mainly in Chafarinas Islands. As 
part of this project, the first complete re- 
search on the parasite fauna of this gull, 
has been carried out. The results on the 
Digenea are presented in this study. An- 
other work (LAFUENTE et al., in press a) is 
referred on the Cestoda and Nematoda 
parasitizing Audouin's gull. 
Material and methods 
A total of 58 adult specimens of Audouin's 
gull from their breeding colony in Cha- 
farinas lslands (35O11' N, 2O 26' W) (fig. 1) 
was examined. The breeding colony only 
fills the islands of Congreso and Rey. Sam- 
pling was made during days 6-16 V 1994 
and 13-26 V 1995. 
Sixteen specimens from Congreso lsland 
(10 males and 6 females) and 42 from Rey 
lsland (18 males and 24 females), were 
caught. Capture of animals, with the perti- 
nent permits, was made by means of nest 
traps. Animals were killed with an over- 
dose of chloroform. Twenty-four specimens 
were dissected in  situ; and the remainder 
were frozen within five minutes of collec- 
tion. In the laboratory, digestive tract, aerial 
sacks, heart, lungs, pancreas, kidneys and 
liver were removed, opened and placed in 
Ringer solution for examination. Helminths 
were removed, washed in distilled water, 
and fixed and mounted according t o  rou- 
tine techniques. 
Results and discussion 
Table 1 lists the 10 digenea found, with their 
main infection parameters. All the digenea 
are new records for the host, Audouin's gull. 
Familv Schistosomatidae Poche. 1907 
Ornithobilharzia sp. 
Fragmented specimens were found in the 
body cavity (but probably proceeding from 
blood system). Males had many testicles and 
females had the ovary at the anterior part of 
body, and the vitellaria at the posterior part 
and specimens were adscribed to  the genus 
Ornithobilharzia (YAMAGUTI, 197 1). Specific 
adscription was impossible however due to  
the poor condition of the worms. 
Schistosomatinae gen. sp. 
A male specimen of another blood digenea 
was also found in the body cavity, but its 
poor condition made generic adscription 
impossible. 
Family Pachytrematidae Baer, 1943 
Pachytrema calculus Looss, 1907 (fig. 2A) 
Synonymous of F! paniceum Brinkmann, 1942, 
our specimens f i t  the descriptions of PURVIS 
(1 937). BRINKMANN (1 942), TIMON-DAVID (1955) 
and SITKO (1968, 1993). This i s  a parasite of 
the gall bladder. I t s  prevalence in Audouin's 
gull is higher than in other gulls. 
Family Renicolidae Dollfus, 1939 
Renicola IariTimon-David, 1933 (fig. 2B) 
This digenea is very common in the kidneys of 
gulls. Our specimens fit the original descrip- 
Tabla 1. Global lnfection parameters of the trematode species parasitizing Audouin's 
gull in Chafarinas Islands: Bs. Blood system; Gb. Gall Bladder; K. Kidney. P. Pancreas; 
R. Rectum; CI. Cloaca; l. Intestine; n. Number of parasitized hosts; Ex. Number of 
examined hosts; N. Total number of parasites. 
Parámetros globales de infección de las distintas especies de trematodos parásitos 
de la gaviota de Audouin en las islas Chafarinas: Bs. Sistema sanguíneo; Gb. Vesícula 
biliar; K. Riñón; F! Páncreas; R. Recto; CI. Cloaca; l. Intestino; n. Número de hospedadores 
parasitados; Ex. Número de hospedadores examinados; N. Número total de parásitos. 
Prevalence lntensity Abundance 
Trematodes Site n1Ex. % % (Rwige) N % 
Schistosomatinae gen. sp. Bs 1/58 1.72 1 - 
Ornithobilharzia sp. 9s 15/58 25.86 3.07 (1-9) 46 0.79 
Pachvtrema calculus Gb 10158 17.24 1.40 (1-2) 14 0.24 
Renicola lari K 23/30 76.67 30.17 (1-90) 694 23.13 
Brachvlecithum microtesticulatum P 1/58 1.72 80 - 80 1.37 
Condylocotyla pilodora R, CI 2/58 3.45 15.50 (1-30) 31 0.53 
Knipowitschiatrema nicolai i 35/58 60.34 12.66 (1-1 10) 443 7.63 
Cardiocephalus longicollis i 14/58 22.41 4.77 (1-19) 62 1.06 
Acanthotrema armata 1 18/58 31.03 34.56 (1-137) 622 10.72 
A~orchis massiliensis I 
scription (TIMON-DAVID, 1933). lnfection 
prevalences of R. lari in different species of 
gulls, are generally very low, even void. Nev- 
ertheless, TIMON-DAVID (1955) found in herring 
gull, L. argentatus Pontoppidan, 1763 (prob- 
ably L. cachinnans Pallas, 1811) of the SE of 
France, values of prevalences similar to those 
of the present study. Obse~ed differences 
among prevalences of R. lari in other gulls 
with respect to Audouin's gull, may be due to  
factors such as distribution and/or availability 
of first (mainly crustaceans or molluscs) and 
second (fish) intermediate hosts. The special- 
ized diet in Clupeiform fish shown by 
Audouin's gull in Chafarinas lslands (PEDROCCHI 
et al., 1996) does not seem to  be the cause of 
the high prevalence of R. lari, as the yellow- 
legged gull L. cachinnans Pallas, 1811, with a 
more varied diet in the same area (WITT et al., 
1981), shows a similar prevalence. It therefore 
seems that infection of both gull species oc- 
curs throughout prey that they usually eat. 
Family Dicrocoeliidae Odhner, 1910 
Brachylecithum microtesticulatum Timon- 
David, 1955 (fig. 2C) 
From among more than 60 known species 
of Brachylecithum, only B. microtesticulatum 
parasitizes gulls and only this species is lo- 
cated in pancreas. The remaining species are 
located in liver, gall bladder and bile ducts. 
B. microtesticulatum shows high morpho- 
logic variability. Our specimens f i t  the 
descriptions of TIMON-DAVID (1 955). BARTOLI & 
MAS-COMA (1989) and KOSTADINOVA (1996). The 
low prevalence o f  this trematode in  
Audouin's gull might be a consequence of 
i t s  terrestrial life cycle, similar to  that of B. 
americanum (DENTON, 1944). and also to  the 
feeding habits (basically piscivorous) of  
Audouin's gull in the sampled area (PEDROCCHI 
et al., 1996). It should be kept in mind that 
108 Lafuente et al. 
pain -,. m Mediterranean Sea Chafarinas lslands 
Isabel II 
Fig. 1. Location of the study area in the Mediterranean Sea. 
Localización geográfica del área de estudio en el mar Mediterráneo. 
the different species of Brachylecithum are 
terrestrial birds such as falconids, corvids and 
paseriforms (SINGH, 1962; YAMAGUTI, 1971). 
Family Heterophyidae Odhner, 1914 
Condylocotyla pilodora Pearson et Prévot, 
1985 (fig. 2D) 
This trematode has only been recorded, with 
a low prevalence, in gulls by PEARSON & PREVOT 
(1985) (in herring gull) and in the present 
work. Many parasitological studies have 
been made on gulls and C. pilodora was 
not found: SULGOSTOWSKA (1 960, 1963) on 58 
and 102 black-headed gulls, L. ridibundus 
L., 1766, respectively; PEMBERTON (1963) on 
146 black-headed,gulls; SITKO (1968, 1993) 
on 302 and 542 black-headed gulls respec- 
tivelyi BAKKE, (1972) on 269 common gulls, L. 
canus L.; POJMANSKA et al. (1984) on 151 black- 
headed gulls; VOJTEK (1981) on 364 black- 
headed gulls; BUSTA & GROSCHAFT (1986) on 
778 black-headed gulls; BRGLEZ et al. (1987) 
en 215 black-headed gulls. This suggests 
that the more habitual defini&e host for 
this trematode is still unknown. 
Knipowitschiatrema nicolai (Issaitschikow, 1927) 
(fig. 3A) 
This trematode, located in the posterior part 
of  the intestine, shows a characteristic 
acetabulogenital complex and a seminal vesi- 
cle S-shape. 
Its prevalence in Audouin's gull (60%) i s  
higher than in the herring gull(24%) (TIMON- 
DAVID, 1955) and lesser black-backed gull, L. 
fuscus L. (25%) (PEMBERTON, 1963). As first 
and second intermediate hosts of this trema- 
tode, a Prosobranch mollusc, Cerithium 
vulgatum and the garfish, Belone belone 
have been recorded. The former is a com- 
mon species in the Mediterranean Sea 
(PEARSON & PREVOT, 1985; D'ANGELO & GARGIULLO, 
Miscel.lania Zoologica 21.2 (1998) 109 
Fig. 2. A. Pachytrerna calculus; B. Renicola lari; C. Brachylecithurn rnicrotesticulaturn; D. 
Condylocotyla pilodora. 
R Pachytrema calculus; B. Renicola lari; C. Brachylecithum microtesticulatum; D. 
Condylocotyla pilodora. 
110 Lafuente et al. 
Fig. 3.A. Knipowítschiatrerna nicolai;. B. Ca 
arrnata; D. Aporchis rnassíliensis. 
A. Knipowitschiatrema nicolai; B. Cardio 
D. Aporchis massiliensis. 
Miscel.lania Zoologica 21.2 (1998) 11 1 
1978). The latter i s  not a usual prey in the Resumen 
diet of Audouin's gull (PEDROCCHI et al., 1996). 
The high prevalence suggests that other fish Trematodos de la gaviota de Audouin, Larus 
species may also be second intermediate audouinii (Aves, Laridae) de las islas 
hosts in the life cycle of  K. nicolai. Chafarinas (Mediterráneo occidenal) 
Acanthotrema armata Lafuente, Roca et 
Carbonell, 1999 (fig. 3C) 
This i s  a new species found on Audouin's 
gull, the description of which is presently in 
press (LAFUENTE et al., in press b). 
Most individuals (98%) were located in 
the posterior part of  the intestine. I t s  preva- 
lence, mean intensity and abundance are 
relatively high and suggest that i t  i s  a com- 
mon species in the helminth community of L. 
audouinii. 
Family Strigeidae Railliet, 1919 
Cardiocephalus longicollis (Rudolphi, 181 9) 
(fig. 38) 
This trematode shows a higher prevalence 
than those in other gulls from north Eu- 
rope (W~LLIAMS, 1962; PEMBERTON, 1963; HARRIS, 
1964; BAKKE, 1972) in which this species is 
absent or very scarce. Studies on gulls Iiving 
near the Mediterranean Sea show pre- 
valences between 1.3 and 10.8% (TIMON- 
DAVID, 1955; SITKO, 1968; 1993; BUSTA & 
GROSCHAFT, 1986; BRGLEZ et al., 1987). 
Family Echinostomatidae Poche. 1926 
Se ha llevado a cabo un estudio sistemático, 
faunístico y ecológico de los trematodos pa- 
rásitos de Larus audouinii Payraudeau, 1826 
(Aves, Laridae) en el mar de Alborán (Medite- 
rráneo sudoccidental), concretamente en las 
islas Chafarinas (fig. 1). Se detectó un total de 
10 especies de digénidos: Schistosomatinae 
gen. sp., Ornithobilharzia sp., Pachytrema 
calculus, Renicola lari, Brachylecithum 
microtesticula tum, Condylocotyla pilodora, 
Knipowitschiatrema nicolai, Cardiocephalus 
longicollis, Acanthotrema armata y Aporchis 
massiliensk. De estas especies, se presentan y 
discuten sus principales rasgos morfoanató- 
micos (figs. 2 y 3) y las relaciones parásito- 
hospedador. La tabla 1 recoge los parámetros 
globales de infección de las distintas especies 
de digénidos encontradas y su localización 
en el hospedador. Todas y cada una de estas 
especies resultaron ser nuevas citas para el 
hospedador Larus audouinii. 
Acknowledgements 
The authors would like to  thank the Ministry 
of Defence, Ministry of Environment, lberia 
Air Lines, Dr. Xavier Ruiz (Univ. de Barcelona) 
and al1 those people who took part in the 
field work: Georgina Álvarez, Enrique Rico, 
M" Carmen del Arco, Jacob González-Solís, 
Juan Carlos Abella and Vittorio Pedrocchi. 
Aporchis massiliensis Timon-David, 1955 
(fig. 3D) 
References 
Only one Echinostomatid trematode was 
found, this being in the intestine of a gull. 
This specimen shows eggs with a long polar 
filament, and lobed testicles fitting the origi- 
nal description of A. massiliensis (TIMON-DAVID, 
1955), who found this species parasitizing 
the herring gull in southeast France. The 
species was also recorded on the lesser black- 
backed gull in Great Britain with a preva- 
lence of 12.5% (PEMBERTON, 1963). Our find- 
ing is the third for European gulls. A. 
massiliensis appears t o  be a rare parasite on 
palaearctic gulls. 
BAKKE, T. A., 1972. Studies on the Helminth Fauna 
of Norway XXII: The common gull, Laruscanus 
L., as final host for Digenea (Platyhelminthes) 
l. NON J. Zool., 20: 165-1 88. 
BARTOLI, P. & MAS-COMA, S., 1989. Dicrocoeliose 
pancreatique des goélands leucophées en 
Corse. Données nouvelles sur Brachylecithum 
microtesticulatum (Digenea: Dicrocoeliidae) 
parasite de Larus cachinnans michaellis. 
Ann. Parasitol. Hum. Comp., 64: 100-1 09. 
BRGLEZ, J., LEPOJEV, O. MUZINIC, J. & BAMBIR, S., 
1987. Endohelminths of some species of 
Lafuente et al. 
gulls (Laridae) in Yugoslavia. Int. Symp. uber 
die Erkrankungen der Zootiere, 29: 75-80. 
BRINKMANN, A., 1942. A new trematode, 
Pachytrema paniceum n. sp. from the gall 
bladder of the lesser blackbacked gull 
(Larus fuscus L.). Goteborgs K. Vet. O. 
Vitterh. Samh. Handl. F. 6. Ser. B, 2: 1-19. 
BUSTA, J. & GROSCHAFT, J., 1986. Trematodes of 
birds of the family Laridae in the southern 
Bohemia. Vest. cs. Spolec. zool., 50: 1-1 2. 
D'ANGELO, G. & GARGIULLO, S., 1978. Cuida alle 
conchiglie mediterranee. Gruppo Edito- 
riale Fabbri, Bompiani, Sonzogno. Milano. 
DENTON, F, 1944. Studies on the life history of 
Brachylecithum americanum n. sp., a liver fluke 
of passerine birds.J. Parasitol., 12: 131-141. 
HARRIS, M. P., 1964. The incidence of some 
species of Trematoda in three species of 
Larus gulls in Wales. Ibis, 106: 532-536. 
KOSTADINOVA, A., 1996. Morphological variabil- 
ity of Brachylecithum microtesticulatum 
(Digenea: Dicrocoeliidae) in the Black Sea 
region. Folia Parasitol., 43: 47-51. 
LAFUENTE, M., ROCA, V. & CARBONELL, E. (in press 
a). Cestodos y Nematodos de la gaviota 
de Audouin, Larus audouinii (Aves, 
Laridae), en las Islas Chafarinas (Medite- 
rráneo Sudoccidental). Bol. R. Soc. Esp. 
Hist. Nat. ser. Biol. 
- (in press b). Description of Acanthotrema 
armata n. sp. (Trematoda: Heterophyidae) 
from Larus audouinii (Aves: Laridae) with 
an amended diagnosis for the genus 
Acanthotrema Travassos, 1928. Syst Parasitol. 
MACE, G. M. & COLLAR, N. J., 1994. Extinction 
risk assessment for birds through quanti- 
tative criteria. Ibis, 137: 240-246. 
PEARSON, J. C. & PREVOT, G. 1985. A revision of 
the subfamily Haplorchinae Looss, 1899 
(Trematoda: Heterophyidae). 111. Genera 
Cercaríoides and Condyloco tyla n. g . Syst. 
Parasitol., 7: 169-1 97. 
PEDROCCHI, V., ORO, D. & GONZALEZ-SOLIS, J., 1996. 
Differences between diet of adult and 
chick Audouin's gulls Larus audouinii at 
the Chafarinas Islands, SW Mediterranean. 
Ornis Fennica, 73: 124-1 30. 
PEDROCCHI, V. & RUIZ, X., 1995. On the current 
status of Audouin's Gull (Larus audouini~] 
in the Mediterranean. In: Proceedings o f  
the 5th lnternational Seabird Group Con- 
ference. Threats to seabirds: 1-38 (M. L. 
Tasker, Ed.). Seabird Group, Sandy. 
PEMBERTON, R. T. 1963. Helminth parasites of 
three species of British gulls, Larus 
argentatus Pont., L. fuscus L. and L. 
ridibundus L. J. Helminthol., 37: 57-88. 
POJMANSKA, T., MACHALSKA, J. & NIEWIADOMSKA, 
K., 1984. Parasites of birds from the Lake 
Goplo and heated lakes of the Konin re- 
gion. Acta Parasitol. Polon., 29: 277-290. 
PURVIS, G. B., 1937. The synonyms of the trema- 
tode genus Pachytrema Looss, 1907. Ann. 
Trop. Med. Parasit., 3 1 : 457-460. 
SINGH, K. S., 1962. Parasitological survey of 
Kumaun region. Part VI. Two new species 
of Brachylecithum Strom, 1940 (Dicro- 
coeliidae: Trematoda) from birds. Ind. J. 
Helminth., 14: 45-52. 
SITKO, J., 1968. Trematodes of birds of the 
family Laridae in Czechoslovakia. Vest. cs. 
Spolec. zool., 32: 275-292. 
- 1993. Ecological relations of trematodes 
infesting lariform birds in the Czech Re- 
public. Acta Sc. Nat. Brno, 27: 198. 
SULGOSTOWSKA, T., 1960. Intestinal trematodes 
of birds of mesotrophic lakes. Goldapiwo 
and Mamry Polnocne. Acta Parasitol. 
Polon., 8: 85-1 14. 
- 1963. Trematodes of birds in the biocenosis 
in the lakes Druzno, Doldapiwo, Mamry 
Polnocne and Swiecajty. Acta Parasitol. 
Polon., 1 1 : 239-264. 
TIMON-DAVID, J., 1933. Sur une nouvelle espece 
de Renicola trématode parasite du rein 
des Laridés. Bull. lnst. Océanogr. Monaco, 
616: 1-16. 
- 1955. Trématodes des goélands de I'ile 
de Riou. Ann. Parasitol. Hum. Comp., 30: 
446-476. 
VOJTEK, J., 1981. Fauna motolik ptaku CSSR. 
Univerzita J. E. Purkyne, Brno. 
WILLIAMS, l. C., 1962. A list of parasitic worms, 
including twenty-five new records, from 
British birds. Ann. Mag. Nat. Hist. (Ser. 
7 3), 4: 467-480. 
Win, H. H., CRESPO, J., DE JUANA, E. & VARELA, J., 
1981. Comparative feeding ecology of 
Adouin's gull Larus audouinii and the 
herring gull L. argentatus in the Mediter- 
ranean. Ibis, 123: 519-526. 
YAMAGUTI, S., 1971. Synopsis of digenetic 
Trematodes of Vertebrates. Vol. l. Keigaku 
Publishing Co., Tokyo (Japan). 


Trematodes of Audouin's gull, Larus audouinii (Aves, Laridae), from Chafarinas Islands (W Mediterranean)

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