PARASITES OF COLUMBA LIVIA (AVES: COLUMBIFORMES)

PARASITES OF COLUMBA LIVIA (AVES: COLUMBIFORMES)

I N TENERIFE (CANARY ISLANDS) A N D THEIR ROLE I N THE CONSERVATION BIOLOGY OF THE LAUREL PIGEONS

F O R O N D A P.*. V A L L A D A R E S B . * , R I V E R A - M E D I N A J . A . * , F I G U E R U E L O E.*, A B R E U N.* & C A S A N O V A J . C * *

Summary:

The prevalence and intensity of the parasites from 5 0 wild doves (Columba livia) from the city of Santa Cruz de Tenerife, in the island of Tenerife (Canary Archipelago], were studied. The following ectoparasites were found in apparently healthy pigeons (prevalences are shown in percentage (%) and mean intensities with their standard deviations): the acari Dermanyssus gallinae (De Geer, 1778) (6 241 .0 ± 138.9) and Tinaminyssus melloi Fain, 1 9 6 2 (10 %, 2 1 8 . 3 ± 1 17.3); the louses, Columbicola columbae Linnaeus, 1 7 5 8 ( 1 0 0 %, 1 1 1 .4 ± 7 6 . 8 ) and Campanulotes bidentatus Scopoli, 1 7 6 3 (94 %, 4 8 . 4 ± 2 6 . 6 ) ; and the pigeon fly, Pseudolynchia canariensis Macquart, 1 8 3 9 (36 %, 6 . 2 ± 1 .6). The endoparasites w e found, were: a haemoprotozoan species, Haemoproteus columbae Kruze, 1 8 9 0 (82 %, 14.8 ± 10.3 per 1000); coccidian oocysts, Eimeria sp.

(50 %, 0 . 2 x 1 03 ± 1.7 x 1 03 per gr); a cestode species Raillietina micracantha (Fuhrmann, 1 9 0 9 ) Lopez Neyra, 1 9 4 7 (44 %, 12.3 ± 9.4); and four nematode species, Tetrameres (Telrameres) fissispina (Diesing, 1861) Travassos, 1 9 1 5 (4 %, 9 9 . 5 ± 34,1), Synhimantus (Dispharynx) spiralis (Molin, 1858) (8 %, 4 6 . 8 ± 1 1.6), Ascaridia columbae (Gmelin, 1790) Travassos, 1 9 1 3 (40 %, 8 . 4 ± 8.8) and Aonchotbeca sp. (1 8 %, 6 . 0 ± 3.1). Several species detected in our study can be pathogens for C. bollii and C. junoniae, which are endemic pigeons of the Canary Islands, considered endangered species.

Parasites (ectoparasites, protozoa and helminths) of C. livia found in Tenerife and others from wild and farm birds in the island were considered as healthy controls.

KEY WORDS : Columba livia, ectoparasites, helminths, protozoa, Tenerife.

Résumé : PARASITES DE COLUMBA LIVIA (AVES : COLUMBIFORMES) DE TÉNÉRIFE (ÎLES CANARIES) ET LEUR RÔLE DANS LA BIOLOGIE DE LA CONSERVATION DES PIGEONS

Nous avons étudié la prévalence et l'intensité des parasites trouvés chez 50 pigeons sauvages (Columba livia ). Il s'agissait de pigeons de Santa Cruz de Tenerife, capitale de l'île de Ténérife (Iles Canaries). Nous avons représenté les prévalences en pourcentage (%) et les intensités moyennes avec leurs déviations standard. Nous avons trouvé chez des pigeons apparemment en bonne santé les ectoparasites suivants : des acariens, Dermanyssus gallinae (De Geer, 1 7 7 8 ) 16 %, 241,0 ± 138,9) et Tinaminyssus melloi Fain, 1962 (10 %, 218,3 ± 117,3); des poux,

Columbicola columbae linnaeus, 1758 ( 1 0 0 % , 1 11 ,4 ± 76,8) et Campanulotes bidentatus Scopoli, 1763 (94 %, 48,4 ± 26,6); et la mouche du pigeon, Pseudolynchia canariensis Macquart, 1839 (36 %, 6,2 ± 1,6). D'autre part, nous avons vu des endoparasites, à savoir, une espèce de hémaprotozoaire, Haemoproteus columbae Kruze, 1890 (82 %, 14,8 ± 10,3 pour

1 000); des oocystes de coccidies, Eimeria sp. (50 %, 0,2 x 103 ± 1,7 x 103 dans 1 gr); une espèce de cestode Raillietina micracantha (Fuhrmann, 1909) López Neyra, 1947 (44 %,

12,3 ± 9,4); et quatre espèces de nématodes, Tetrameres (Tetrameres) fissispina (Diesing, 1861) Travassos, 1915 (4 %, 99,5 ± 34, 1), Synhimantus (Dispharynx) spiralis (Molin, 1858) (8 %, 46,8 ± 1 1,6), Ascaridia columbae (Gmelin, 1790) Travassos, 1913 ( 4 0 % , 8,4 ± 8,8) et Aonchotheca sp. (18 %, 6,0 ± 3,1). Quelques-unes des espèces étudiées peuvent être pathogènes pour C. bollii et C. junoniae, lesquelles sont des pigeons endémiques des îles Canaries, et sont considérées en voie de disparition. Les parasites de C. livia de l'Ile de Ténérife (ectoparasites, protozoaires et helminthes) et d'autres trouvés dans des oiseaux sauvages et domestiques de la même île peuvent être considérés comme des indicateurs de l'état de santé.

MOTS CLÉS : Columba livia, ectoperasite, helminthe, protozoaire, Ténérife.

INTRODUCTION

P

i g e o n s are a c o s m o p o l i t a n group o f birds with abundant and large populations associated, in most cases, with human activities. In the Canary

* Department of Parasitology, Ecology and Genetics. Faculty of Phar- macy, University of La Laguna, Avda. Astrofisico Fco. Sanchez s/n, 38203, Tenerife, Canary Islands, Spain.

** Laboratory of Parasitology, Faculty of Pharmacy, University of Bar- celona, Avda. Diagonal s/n, 08028 Barcelona, Spain.

Correspondence: Pilar Foronda Rodriguez.

Tel.: +0034 922 31 84 84 - Fax: +0034 922 31 85 1+.

E-mail: pforonda@ull.es

Islands, three s p e c i e s o f the g e n u s Columba are des- cribed, the rock dove, C livia, the dark-tailed laurel pigeon, C. bollii, and the white-tailed laurel pigeon, C. junioniae. T h e presence o f other species such as the stock dove (C. oenas) and the w o o d p i g e o n ( C . p a l u m - bus) is accidental or irregular and they have b e e n o b s e r v e d in the migration station. Columba bollii a n d C. junioniae are e n d e m i c species o f the Canary Islands.

Roth are representatives o f a characteristic habitat o f the Canaries called laurel forest, the forest type with the highest plant diversity o f these islands. Columba bollii and C. junoniae w e r e c o n s i d e r e d in e n d a n g e r e d s p e c i e s at the B o n n Convention 1 9 7 9 o n the protec-

P a r a s i t e , 2 0 0 4 , 11. 3 1 1 - 3 1 6

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Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/2004113311

tion and c o n s e r v a t i o n o f bird s p e c i e s . T h e m o s t c o m m o n s p e c i e s o f pigeon in the Canary Islands is C. livia w h i c h inhabits in forests, cities and villages.

W h e r e a s C. liria is c o n s i d e r e d abundant in Tenerife, only 3 5 0 - 4 0 0 individuals o f C. bollii and 8 0 - 1 2 0 indivi­

duals o f C. junionae are present in this island (Emmer- son, 1 9 8 5 ) .

The parasitic fauna (arthropoda. protozoa and hel­

minths) o f C. liria in Europe, Asia, Africa and Ame­

rica is well known. Several helminth parasites decrease host survival and breeding s u c c e s s , and consequently, they can affect the population dynamics o f their hosts (Hudson et ah, 1 9 9 2 ) . Helminths o f C. livia may affect host fitness b y increasing morbidity and predation risk as well as reducing clutch size, w e a k e n i n g b o d y condi­

tion or altering m e t a b o l i c rates (Hudson & D o b s o n , 1 9 9 5 ) .

In 2 0 0 1 , the canary g o v e r n m e n t allowed the capture o f several individuals o f C. livia in the city o f Santa Cruz de Tenerife, located near the laurel forest, in order to study the parasitic infections o f these hosts. T h e aim o f this study w a s to identify the potential risk o f para­

sitic transmission b e t w e e n C. livia and the other two e n d e m i c and protected p i g e o n s p e c i e s (C. bollii and C. junionae) in Tenerife.

MATERIAL A N D METHODS

T

h e Canary Archipelago is located b e t w e e n 13°

23' to 18° 8' W and 27° 37' to 29° 2 4 ' N in Maca- ronesia along with the islands o f Madeira, Azo­

res, Savages and Cape Verde. Tenerife is the largest island o f the archipelago. For this study, p i g e o n s w e r e captured throughout the year 2001 in Tenerife.

In the captured birds, plumages w e r e e x a m i n e d for ectoparasites and the nasal p a s s a g e s w e r e e x a m i n e d for nasal mites using a magnifying glass. T h e e c t o p a ­ rasites w e r e collected with tweezers and preserved in 70° ethanol for t a x o n o m i c identification.

B l o o d samples w e r e o b t a i n e d from e a c h animal and b l o o d s m e a r s w e r e p e r f o r m e d , air-dried, fixed in m e t h a n o l and stained with G i e m s a ' s solution. T h e slides w e r e e x a m i n e d under light m i c r o s o c o p e at a magnification o f 100x. Parasitized and unparasitized cells w e r e c o u n t e d to estimate the parasite intensity.

Hosts w e r e dissected and their digestive tracts, lungs and livers w e r e e x a m i n e d for helminths. Cestode and n e m a t o d e s p e c i e s w e r e r e c o v e r e d and preserved in 7 0 % ethanol. Platyhelminths w e r e stained with Sem- m i c h o n a c e t o c a r m i n e , d e h y d r a t e d s e q u e n t i a l l y in alcohol, cleared in xylol, and m o u n t e d in Canada bal­

sam. N e m a t o d e s w e r e cleared in Amann lactophenol.

Faecal samples w e r e c o l l e c t e d from the rectum o f all dissected p i g e o n s , stored in 2.5 % ( w / v ) potassium

dichromate solution ( K r2C r207) , maintained at r o o m temperature ( 2 3 - 2 8 ° C) for the c o c c i d i a sporulation and e x a m i n e d m i c r o s c o p i c a l l y after flotation using saturated saline solution. O o c y s t s o f c o c c i d i a w e r e c o u n t e d in a 1 g sample o f feaces using the McMaster t e c h n i q u e .

Several s p e c i m e n s o f four n e m a t o d e s p e c i e s w e r e pre­

pared for Scanning Electronic Microscopy (SEM) study following the general m e t h o d o l o g y d e s c r i b e d in the literature (Miquel et al., 1995). T h e specimens w e r e exa­

mined with an electron m i c r o s c o p e (Hitachi S - 2 3 0 0 ) . Statistical %² and ANOVA tests w e r e used to determine differences in the prevalences and mean intensities o f parasites b e t w e e n males and females o f C. livia a n d b e t w e e n s e a s o n s ( B u s h et al.. 1 9 9 7 ) . S p e c i e s counts w e r e log transformed to normalize the distribution.

RESULTS

A

total o f fifty pigeons w e r e e x a m i n e d . Five e c t o ­ parasite s p e c i e s w e r e r e c o v e r e d and represen­

tative s p e c i m e n s w e r e d e p o s i t e d at the Natural History Museum o f Tenerife: Tinaminyssus inelloi Fain, 1962, ( a c c e s s i o n no. T F M C / A C - 1 8 ) Dermanyssus gal­

linae (De Geer, 1778) (TFMC/AC-17) ( D e r m a n y s s i d a e ) [Acari]; Campanulotes bidentatus Scopoli, 1763, (TFMC/

ML-16) Columbicola columbae Linnaeus, 1 7 5 8 ( T F M C / ML-15) (Phylopteridae) [Mallophaga]; and Pseudolyn- chia canariensis Macquart, 1839 ( T F M C / D I - 3 8 7 ) (Hip- p o b o s c i d a e ) [Dipteral. T h e ectoparasite s p e c i e s w e r e collected from the plumage o f the hosts e x c e p t for T.

inelloi w h i c h was r e c o v e r e d from the nasal passages.

The mallophaga w e r e found with high p r e v a l e n c e s , C. columbae was present in all the e x a m i n e d p i g e o n s and C. bidentatus in 9 4 % o f the d o v e s , with a m e a n intensity and a standard deviation o f 1 1 1 . 4 ± 7 6 . 8 and 48.4 ± 2 6 . 6 . respectively. Pseudolyncbia canariensis was found in 18 hosts ( 3 6 % ) with a m e a n intensity of 6.2 ± 1.6. Tinaminyssus melloi and D. gallinae was found with l o w e r p r e v a l e n c e s ( 1 0 % and 6 %, r e s p e c ­ tively) but with high m e a n intensities, 2 1 8 . 3 ± 1 1 7 . 3 for T. melloi and 2 4 1 . 0 ± 138.9 for D. gallinae.

T w o s p e c i e s o f protozoa w e r e found: Haemoproteus columbae Kruze. 1890 ( H a e m o p r o t e i d a e ) in 8 2 % o f the e x a m i n e d animals, with a m e a n intensity o f 14.8 ± 10.3 infected cells per 1,000 red b l o o d cells, and Eimeria spp. (Eimeriidae) in the faeces o f 5 0 % o f the d o v e s with a m e a n o f 0.2 x 1 0 ' ± 1.7 x 1 0³ per gr.

Helminth species recovered from the parasitized doves were deposited in the Natural History Museum o f T e n e ­ rife: Raillietina micracantha (Fuhrmann, 1 9 0 9 ) Lopez Neyra, 1942 ( a c c e s i o n n o . T F M C C S / 0 0 0 6 ) (Davainei- dae) [Cestoda], Tetrameres (Tetrameres) fissispina (Die- sing, 1861) Travassos, 1915 ( T F M C N A / 0 0 0 6 ) ( T e t r a m e -

M é m o i r e P a r a s i t e . 2 0 0 4 , 11. 3 1 1 - 3 1 6

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PARASITES OF COLUMBA LIVIA IN TENERIFE

ridae), Synhimantus (Dispharynx) spiralis (Molin. 1858) ( T F M C N A / 0 0 0 7 ) ( A c u a r i i d a e ) , Ascaridia columbae (Gmelin, 1790) Travassos, 1913 ( T F M C N A / 0 0 0 8 ) (Asca-

ridiidae) and Aonchotheca sp. ( T F M C N A / 0 0 0 9 ) (Tri- c h u r i d a e ) [Nematoda]. Raillietina micracantba was first described by Lopez Neyra ( 1 9 4 7 ) and J o y e u x &

B a e r ( 1 9 3 6 ) . Only males o f T. (T.) fissispina w e r e found w h e r e a s individuals o f both s e x e s w e r e r e c o ­ vered from S. ID.) spiralis and A. columbae. S p e c i e s identification o f these n e m a t o d e s was carried out by metrical m e a s u r e m e n t s and SEM studies.

Raillietina micracantba. was presented with a preva­

l e n c e o f 4 4 % and a mean intensity and standard deviation o f 12.3 ± 9.4. T h e most prevalent n e m a t o d e was A. Columbae which was found in 4 0 % o f the stu­

died hosts with a mean intensity o f 8 . 4 ± 8.8. followed by Aonchotheca sp. ( 1 8 %. 6.0 ± 3 - D . T h e o e s o p h a - gial n e m a t o d e s a p p e a r e d in a lower n u m b e r o f the doves, with prevalences and m e a n intensities o f 8 % and 4 6 . 8 ± 11.6 in 5. (D.) spiralis, and 4 % and 9 9 . 5 ± 34.1 in T. (T.) fissispina.

No significant differences in the prevalences and mean intensities o f the parasites w e r e found b e t w e e n host s e x e s . T h e parasite s p e c i e s w e r e found in all s e a s o n s with NS seasonal differences in the p r e v a l e n c e s and m e a n intensities for a n y s p e c i e s .

DISCUSSION

E

ctoparasite s p e c i e s found in our study are c o m ­ monly cited in Columbiformes and specifically in C. Iicia. Campanulotes bidentatus has b e e n r e c o v e r e d from several Columba s p e c i e s (Cordero del Campillo et al.. 1994). Columbicola columbae infects different families o f birds, for e x a m p l e Turdidae and Accipitriclae (Corclero del Campillo et al, 1994). Tina- minyssus melloi is a c o s m o p o l i t a n s p e c i e s o f domestic p i g e o n s ( P e n c e . 1 9 7 3 ) and has b e e n reported at a n o ­ ther related g e n e r a o f hosts, such as Streptopelia (Cor­

dero del Campillo et al, 1 9 9 4 ) . Dermanyssus gallinae ( D e G e e r ) . the c o s m o p o l i t a n poultry red mite o r c h i c k e n mite, is an e c o n o m i c a l l y important ectopara­

site o f domesticated fowl (Kettle. 1993). It may b e c o m e a serious pest, causing irritation and anemia and in s o m e c a s e s e v e n death o f its host (Kirkwod, 1 9 6 7 ) . Dermanyssus gallinae feeds on the b l o o d o f domestic- fowl, c a g e d birds and p i g e o n s as well as wild birds (McGarry & T r e e s , 1 9 9 1 ) , and it may eventually attack m a m m a l s ( D u c a n , 1957; Hoffman, 1 9 8 7 ) .

It is interesting to realize that in the low n u m b e r o f e x a m i n e d hosts, the p r e s e n c e o f P. canariensis and H. columbae has considered usual. T h e p i g e o n fly, P. canariensis, is the intermediate host o f this h a e m o - proteid which lives in the nest o f the pigeon (Garnham,

1 9 6 6 ) , and it w a s i n c r i m i n a t e d as t h e v e c t o r o f H. columbae in natural (Klei & de Giust. 1 9 7 5 ) and experimental infection ( A h m e d & M o h a m m e d . 1977).

Haemoproteus columbae is the only haemoparasite found in blood smears o f the cloves e x a m i n e d . It is a c o m m o n and c o s m o p o l i t a n parasite o f the domestic pigeon in most parts o f the world (Garnham. 1966), and it has b e e n found in different species o f wild doves o f the g e n e r a Zenaida, Cohtmbina and Scardafell (Adriano & Cordeiro, 2 0 0 1 ) , although it is not consi­

dered p a t h o g e n i c . T h e high prevalence may involve behavioral aspects o r s o m e physiological condition within the s p e c i e s (White et al, 1978). From a beha­

vioural point o f view, C. livia inhabits in Tenerife in large flocks which e a s e s the transmission o f vectors and leads to a high prevalence and intensity o f para­

sites.

Eimeria is p r o b a b l y o n e o f the most frequent genera o f coccidia in nature (del C a c h o el al, 1999). Eimeria spp. from p i g e o n s are clearly c o n s i d e r e d pathogens with a morbidity in y o u n g individuals that could rise up to 1 5 - 7 0 % but it is not a pathogen in mature doves (Cordero del Campillo & Hidalgo Arguello, 1999).

B e s i d e s C. livia, only two other s p e c i e s o f this genus are e x a m i n e d for helminths. C. inornata and C. oenas.

In both o f them, only o n e species was found, Tanaisia bragai dos Santos, 1934 in Puerto Rico (Arnizaut et al.

1992) from C. innornata and Raillietina echinobo- Ihrida (Megnin, 1 8 8 0 ) from C. oenas in Spain (Cordero del Campillo et al., 1994). Rock doves from Tenerife harboured a helminth community relatively p o o r in s p e c i e s if it is c o m p a r e d to many other populations o f pigeons o f this s p e c i e s . For C. livia, a total o f 47 hel­

minth s p e c i e s have b e e n cited in the world.

T h r e e s p e c i e s o f digenean trematodes [Brachy/aima columbae Mazzanti, 1899, Brachylaima fuscata Rudol- phi. 1 8 1 9 and Echinoparyphium recurvatum (Linstow, 1873) Luhe. 19091 w e r e found in C. livia from Europe (Catelli et al. 1999; Cordero del Campillo et al. 1994;

Kulisic, 1 9 8 8 ; Martinez-Moreno et al, 1989). No dige- neans w e r e found in our study. In the prospected urban area, terrestrial and aquatic snails s e e m e d to b e unimportant in the diet o f C. livia, but in the laurel forest, with a high diversity and a b u n d a n c e o f terres­

trial snails, it could b e possible that C. bollii and C. junoniae include these potential intermediate hosts o f brachylaimid trematodes (Pojmanska, 2 0 0 1 ) , in their diets. Davained c e s t o d e s , mostly from the genus Rail­

lietina Schmidt ( 1 9 8 6 ) or Raillietina. Skrjabinia and Furhmannetta ( J o n e s & Bray, 1994) are dominant spe­

cies in the fauna o f plathyhelminthes against anoplo- cephalids and hymenolepidids (Foronda, 2 0 0 2 ) . Only o n e s p e c i e s , R. micracantba, has b e e n previosly cited in the Canary Islands parasitizing C. livia (Gijon Botella et al. 1 9 8 9 ) .

M é m o i r e ³¹³

P a r a s i t e . 2 0 0 c 11. 3 1 1 - 3 1 0

T h e African mainland is near the Canary Islands (only 100 k m a w a y ) . Individuals o f C. livia c o u l d originally be from Africa but n o genetic data o n the Canarian and African p o p u l a t i o n s are available. In v i e w o f our results, it is difficult to confirm the hypothesis o f an interelation b e t w e e n Africa and the Canaries from the helminthological point o f view. As in Tenerife, n o d i g en ea ns w e r e cited in C. livia from Africa. T h e spe­

cies o f the g e n u s Raillietina are not g o o d indicators o f the g e o g r a p h i c a l origin o f C. livia in the Canary Islands, b e c a u s e African s p e c i e s o f this g e n u s parasi­

tizing r o c k doves have not b e e n n a m e d (Mushi et al., 2 0 0 0 ) . Cotugnia digonopora (Davaineidae) is presented in African and Asian pigeons (Ibrahim et al., 1995; Patel et al., 2 0 0 0 ) but it is absent in Tenerife. W e c o m p a r e d the helminth fauna o f C. livia in Tenerife with that o f Iberian Peninsula, from the s a m e host, b e c a u s e the h u m a n introduction o f C. livia from Iberia into the Canaries is well k n o w n . All the s p e c i e s found in the rock d o v e in Tenerife w e r e previously d e n o u n c e d in the Iberian Peninsula but they s e e m to b e p o o r g e o ­ graphic indicators. T h e e n d e m i c c e s t o d e species found in Spanish doves, Hymenolepis cordobensis J o r d a n o , 1952 was not found in Tenerife. From the rest o f c e s - todes cited in the Iberian Peninsula in C. livia (Cboa- notaenia infundibulum, Killigrewia delafondi, Para- dicranotaenia anormalis, R. echinobothrida, R.joyeuxi, R. micracantha, Furhmannetta pluriuncinata, Skrja- binia bonini, Sobolevicanthus columbae) (Cordero del Campillo et al, 1 9 9 4 ) , only R. micracantha s e e m s to have possibly b e e n introduced from Spain into the Canary Islands, but this s p e c i e s is widely distributed in this host in E u r o p e ( F o r o n d a , 2 0 0 2 ) and it is not an specific parasite, for it has b e e n o b t a i n e d from several genera o f birds (Turdus, Columba and Stigmatopoelia) (Schmidt, 1 9 8 6 ) . T h e species, C. infundibulum B l o c h , 1779 cited in C. livia in Spain (Cordero del Campillo et al., 1 9 9 4 ) w a s found in Tenerife parasitizing Alec- toris barbara ( P h a s i a n i d a e ) [Foronda, 2002, Foronda

"unpublished data" ( G e n e B a n k a c c e s s i o n n° A J 5 5 5 1 7 1 - AJ555172)]. As well as in C. livia, the p r e s e n c e in T e n e ­ rife o f introducted farm specimens o f Alectoris sp., from the Iberian Peninsula, could explain the introduction o f C. infundibulum in the Canary Islands.

Paleartic cestodes o f C. livia which have b e e n not cited in the Iberian Peninsula for this host, includes the davaineid, Davainea proglottina from Serbia (Kulisic et al., 1 9 9 6 ) and R. tetragona from G r e e c e ( G i t h k o - p o u l o s & Liakos, 1 9 8 7 ) , Italy ( T a c c o n i et al., 1 9 9 3 ) and Serbia (Kulisic et al., 1 9 9 6 ) . H o w e v e r they w e r e repor­

ted in Iberia in other hosts, D. proglottina w a s found in chickens, and R. tetragona in chickens, Alectoris rufa and Meleagridis gallopavo (Cordero del Campillo et al., 1 9 9 4 ) .

T h e n e m a t o d e fauna o f C. livia in Tenerife includes only a h a b r o n e m a t o i d , an acuarioid, an ascarid and a

thrichurid s p e c i e s . Tetrameres fissispina was identified by SEM. This s p e c i e s has a w i d e range o f distribution parasitizing farm birds. Moreover, other wild bird s p e ­ cies such as Larus larus and Tardona tardona h a v e b e e n cited as hosts o f this n e m a t o d e . F r o m the north to the south o f Spain, this s p e c i e s is widely distributed in diverse bird s p e c i e s (Cordero del Campillo et al., 1 9 9 4 ) . Synhimantus spiralis is present in all b i o g e o - graphical regions parasitizing G a l l i o r m e s , C o l u m b i - formes and Passeriformes ( H w a n g et al., 1 6 9 D - T h e low specificity o f this nematodes for the definitive hosts and the high apparent adaptation o f their life cycle in Tenerife c o u l d b e an important risk for C. bollii and C. junionae b e c a u s e both, T. fissispina and D. spiralis, are often c a p a b l e o f causing the death o f infected ani­

mals (Tarazona Vilas, 1 9 9 9 ) .

Ascaridia columbae is a typical parasite o f Columba spp. with a c o s m o p o l i t a n distribution ( F o r o n d a , 2 0 0 2 ) that can also affect other genera, such as Zenaida ( B a m s & Herrera Rodriguez, 1969). This parasite causes weight loss and diarrhoea in h e a v y infections similar to capillariosis in the parasitized birds ( T a r a z o n a Vilas, 1 9 9 9 ) .

T h e dark-tailed laurel p i g e o n and the white-tailed lau­

rel pigeon are e n d e m i c to the Canary Islands. Columba bollii is classified as Rare b y IUCN ( G r o o m b r i d g e , 1 9 9 3 ) and considered Vulnerable at world level (Collar et al., 1 9 9 4 ) . Columba junoniae is classified as Vulnera­

ble at global and E u r o p e a n levels (Collar et al., 1 9 9 4 ) and it is classified as Rare b y IUCN ( G r o o m b r i d g e , 1 9 9 3 ) . B o t h s p e c i e s w e r e also listed in A n n e x I o f the EU Wild Birds Directive and the A p p e n d i x II o f the Bern Convention. T h e diet o f b o t h p i g e o n s consists mainly o f fruit ( E m m e r s o n , 1 9 8 5 ) . In C. bold b e s i d e s fruit, the birds feed o n leaves, shoots, and leaf and flower buds, and they may, if the opportunity arises, supplement their diet with small invertebrates (Emmer­

son, 1 9 8 5 ) .

O n l y o n e important viral disease, the Newcastle, is considered dangerous for C. bollii and C. junoniae (Action Plan for the dark-tailed laurel pigeon, and Action Plan for the white-tailed laurel pigeon, SEO/BirdLife Inter­

national, T e n e r i f e ) due to the a b s e n c e o f data from other parasitic diseases. Our faunistical study o f C. livia in Tenerife s h o w s that parasite diseases (arthropods, p ro t oz oa and helminths) c o u l d p r o d u c e d a n g e r o u s diseases in the e n d e m i c dove populations in Tenerife.

Parasites detected in C. livia in Tenerife are considered generally as s p e c i e s with a l o w d e g r e e o f specificity due to the fact that they are able to establish in diffe­

rent s p e c i e s o f Columbiformes and other hosts with a wide range o f distribution in the wrorld, therefore it is r e a s o n a b l e to c o n s i d e r t h e m as threats to the endan­

g e r e d s p e c i e s . In the v i e w o f the C. livia parasites that w e r e found in native and introduced bird s p e c i e s in Tenerife ( F o r o n d a , 2 0 0 2 ) w e c o n s i d e r that an i n c r e a s e

3 1 4 M é m o i r e P a r a s i t e , 2 0 0 4 , 11. 3 1 1 - 3 1 6

PARASITES OF COLUMBA LIVIA IN TENERIFE

in the frequency o f health controls o n wild a n d farm birds in the Canary Islands w o u l d b e highly re co m- m e n d a b l e .

ACKNOWLEDGEMENTS

W

e wish to thank the "Excelentísimo Ayunta- m i e n t o d e Santa Cruz d e T e n e r i f e " a n d 2 0 0 1 S G R 0 0 0 8 8 project b y the "Comissionat por la R e c e r c a y Universitats d e la Generalitat d e Cata- lunya (Catalonia Government)" for supporting this study.

REFERENCES

ADRIANO E.A. & CORDEIRO N . S . Prevalence and intensity of Haemoproteiis columbae in three species of wild doves from Brazil. Memorias do Instituto Oswaldo Cruz, 2001, 96, 175-178.

AHMED F . E . & MOHAMMED A.H. Schizogony in Haemoproteiis columbae Kruse. Journal of Protozoology, 1977, 24, 389- 393.

ARNIZAUT A . B . , HAVES L.. OLSFX G . H . , TORRES J.S., Ruiz C. &

PÉREZ-RIVERA R. An epizootic of Tanaisia bragai in a cap- tive population of Puerto Rican plain pigeon (Columba inornata wetmorei). Annals of the New York Academy of Sciences, 1992, 655, 202-205.

BARUS V. & HERRFRA-RODRIGCEZ R. Sobre la presencia del nematodo Eucolueus annulatus (Molin, 1858) en Cuba.

Serie Monográfica del Instituto Nacional de Medicina Vete- rinaria. Habana. 1969. 9. 3-7.

BUSH A . O . , LAFFERTY K . D . , LOTZ J.M. & SHOSTAK A . W . Parasi- tology meets ecology on its own terms: Margolis et al. revi- sited. Journal of Parasitology. 1997, 83. 575-583-

CATELLI E., POGLAVFN G . , TERREGIXO C , ORLANDO C , TONFILI A..

ISSA GADALE O , RODA R. & AGXOLETTI A . Indagine sui para- ssiti dell'apparato diferente di Columba livia (Gmelin 1789) nella città di Firenze. Selezione Veterinaria, 1999, 2, 75-85.

COLLAR N.J., CROSBY M.J. & STATTERSFIELD A.J. Birds to watch 2:

the world list of threatened birds. Cambridge UK: Bird- Life International (BirdLife Conservation Series n° 4), 1994.

CORDERO DEL CAMPILLO M., CASTAXOX-ORDOXEZ L. & REGUERA FEO A. índice-catálogo ele zooparásitos ibéricos, 2n d ed., Secretariado de Publicaciones, Universidad de León, León, 1994, 650 pp.

CORDERO DEL CAMPILLO M. & HIDALGO ARGUELLO R. Otras coc- cidiosis aviares, in: Parasitología Veterinaria. Cordero del Campillo et al. (eds). McGraw-Hill-Interamericana de España, Madrid, 1999, 768-770.

DEL CACHO E.. SIERRA M.A. &. SÁNCHEZ-ACEDO C . Coccidiosis aviar (Eimeriosis), in: Parasitología Veterinaria. Cordero del Campillo et al. (eds), McGraw-Hill-Interamericana de España, Madrid, 1999. 757-768.

DUNCAN S. Dertnanyssus gallinae (De Geer, 1778) attacking man. Journal of Parasitology, 1957, 43, 6.37.

EMMERSON K.W. Estudio de la biología y ecología de la Paloma Turqué y la Paloma Rabiche con vistas a su conservación, 1 and 2. Tenerife: Ornistudio S.L.. 1985.

FORONDA P. Estudio faunístico y sistemático de helmintos de aves de Canarias. Ph. Thesis, La Laguna. Universidad de La Laguna. 2002.

GARNHAM P.C.C. Malaria parasites and other Haemosporidia.

Blackewll Scientific Publications, Oxford, UK, 1966.

GIJÓN-BOTELLA H.. DEL CASTILLO-REMIRO J.A. & LÓPEZ-ROMÁN R.

Estudio al M.E.B, de Raillietina (Raillietina) micracantha Fuhrmann 1908 parásito de Columba livia domestica cap- turadas en las Islas Canarias. Revista Ibérica de Parasito- logía, 1989, 49, 37-40.

GITHKOPOLLOS P.R. & LIAROS V.D. Parasites of the alimentary tract of pigeons in Greece. Deltion tes Ellenikes Kteniatrik.es Eta i reías, 1987, 38, 79-83.

GROOMBRIDGE B. (ed.) 1994 IUCN Red List of threatened ani- mals. IUCN Gland, Switzerland and Cambridge, UK: Inter- national Union for Conservation of Nature and Natural Resources, 1993.

HOFFMAX G.V. Vogelmilben als Lüstlinge, Kranken-heitsser- zeuger und Vektoren bei Mensch und Nutztier (Veterinary and hygienic importance of the red chichen mite and the northern fowl mite). Deutschen Tierarztliche Wochen- schrift, 1987, 95, 7-10.

HUDSON P.J. & DOBSOX A.P. Macroparasites: observed patterns in naturally fluctuating animal populations, in: Ecology of infections diseases in natural populations. Grenfell B T . &

Dobson A.P. (eds). Cambridge University Press. Cam- bridge. 1995. 144-176.

HUDSON P.J., NEWBORN D. & DOBSON A.P. Regulation and sta- bility of free-living host-parasite system. Trichostrongylus tenuis in red grouse. Monitoring and parasite reduction experiments. The Journal of Animal Ecology, 1992, 61, 477- 486.

HWANG J.G., TOLGAY N., SHALKOP W.T. & JAQUETTE D.S. Case report Disphaiynx nasula causing severe proventriculitis in pigeon. Avian Diseases, 1961. 5, 60-65.

IBRAHIM A.I., HASSANN H.H., ALY S.E.M. & ABDEL AAL A.A. A study on some parasitic affections in domestic pigeons in Lsmalia province. Assiut Veterinary Medical Journal, 1995.

34, 153-161.

JOXES A. & BRAY R.A. Family Davaineidae Braun 1900. in:

Keys to the cestode parasites of vertebrates. Khalil L.F..

Jones A. & Bray R.A. (eds), CAB International, Walling Ford. Oxon. UK. 1994, 407-441.

JOYEUX C. & BAER J G . Cestodes. in: Faune de la France Paul Lechevalier et Fils, Paris, 1936, 613.

KETTLE D.S. Ascari-Prostigmata and Gamasidae. In: Medical and veterinary entomology, 1st ed.. CAB, Wallingford. UK.

199.3, 380-405.

KIRKWOOD A.C. Anemia in poultry infested with red mite Der- manyssits galinae. Veterinary Record, 1967, 80, 514-516.

KLEI T.S. & DE GIUSTI D.L. Seasonal occurrence of Haemo- proteiis columbae Kruse and its vector Pseodolynchia

canariensis Bequaert. Journal of Wildlife Diseases 1975. 11, 130-135.

Parasite. 200-t. 11. 311-316

M é m o i r e 315

KULISIC

Z. Endoparasite fauna of pigeons (Columba liria) as detected in the city of Belgrade. Acta Veterinaria, 1988,

38, 3 7 - 4 2 .

KULISIC Z.. PAVLOVIC I. & Milutovic M. Contribution to

knowledge of parasitofauna of pigeons in Belgrade from

1 9 9 0 - 1 9 9 4 .

Veterinarski Glasnik,

1 9 9 6 .

50.

7 8 5 - 7 9 0 . LÓPEZ NEYRA C.R. Helmintos de los vertebrados ibéricos.

CSIC, Instituto Nacional de Parasitología de Granada, Gra- nada. 1947.

MARTÍN MATEO M. P. Revision de malofagos Philopteridae

denunciados en España como parásitos de aves demés- ticas. Revista Ibérica de Parasitología

1 9⁷5 .

35(1-2),

4 1 - 6 8 . MARTÍNEZ-MORENO F.J., MARTÍNEZ-MORENO A.. BECERRA-MARTELL

C. & MARTÍNEZ-CRUZ M.S.

Parasitofauna of pigeon Columba livia in the province of Cordoba Spain. Revista Ibérica de Parasitología.

1989.

49.

2 7 9 - 2 8 2 .

MCGARRY J.W. & TREES A.J. Trap perches to assess the acti- vity of pyrethrins against poultry red mite Dennanyssus gallinae in cage birds. Experimental Applied Acarology

1991,

12.

1-7.

MIQUEL J.. CASANOVA J.C., TENORA F.. FELIU C. & TORRES J . A

scanning electron microscope study of some Rictulariidae (Nematoda) parasites of Iberian mammals. Helmintho- logia 1995, 32. 3-14.

MUSHI E.Z., BINTA M.G., CHAIR.) R.G., NDEBELE R. & PANZIRAH R.

Parasites of domestic pigeons (Columba livia domestica) in Sebele, Gaborone. Botswana. Journal of the South African Veterinary Association.

2 0 0 0 .

71.

2 4 9 - 2 5 0 . PATEL P.V.. PATEL A.I., SAIII R..K. & RAJU V. Prevalence of gas-

trointestinal parasites in captive birds of Gujarat zoos. Zoos' Print Journal,

2 0 0 0 .

15,

2 9 5 - 2 9 6 .

PENCE D.B. The nasal mites of birds from Louisana. IX. Synop- sis. The Journal of Parasitology.

1 9 7 3 . 59. 8 8 1 - 8 9 2 .

POJMANSKA T. Family Brachylaimidae Joyeux and Foley 1930, in: Keys to the Trematoda. Gibson D.I.. Jones A. & Bray RA. (ed). CAB International. Walling Ford. Oxon. UK.

Vol. I. 2 0 0 1 . 3 7 - 4 3 .

SCHMIDT

G.D. CRC handbook of tapeworm identification.

Boca Raton. Florida: CRC Press. 1986. 6 7 5 .

TACCONI G.. MORETTI A.. PIFRGILI FIORETTI D. & LATINI M. Endo-

parasitosi del Colombo torraiolo (Columba livia Gmelin 1789, forma urbana):rilievi epidemiológica nella citta di Terni. Zootecnia Internacional,

1 9 9 3 ,

4,

8 3 - 8 5 .

TARAZONA VILAS J.M. Nematodosis. in: Cordero del Campillo

et al. Parasitología Veterinaria. McGraw-Hill-Interameri- cana de España. Madrid. 1999. 791-808.

WHITE E.M.. GREINER E C . BENNET G.F. & HERMAN CM. Dis-

tribution of the hematozoa of Neotropical birds. Revista de Biología Tropical,

1 9 7 8 ,

26,

4 3 - 1 0 2 .

Reçu le 2 0 novembre 2 0 0 3 Accepté le 1^er avril 2 0 0 4

3 1 6 M é m o i r e Parasite. 2 0 0 4 , 11. 3 1 1 - 3 1 6