Incidence of a Haemoproteus Lari Parasitemia in a Threatened Goll
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Ornis Fennica 72:159-164 1995 Incidence of a Haemoproteuslari parasitemia in a threatened Goll: Larus audouinii Xavier Ruiz, Daniel Oro & JacobGonzález-Solís Ruiz, X., Oro, D., González-Solís, J., Dept. de BiologiaAnimal (Vertebrats), Universitat : de Barcelona, Av. Diagonal 645. 08028-Barcelona, Spain ~ Received 15 August 1995, accepted 11 October 1995 Data on haematozoan parasiternias in Laridae are scarce and, since blood parasites may influence birds fitness, it is important to report their incidence in threatenedspecies such as Audouin' s Gull. Blood smearsof 90 Audouin' s Gulls caught during incubation at their two main breeding sites, fue Ebro Delta and fue Chafarinas Islands, were exarnined for Haemoproteus lari parasiternia. Overall prevalence of fue parasite was 92.1 % for fue Chafarinas Is. and 28.9% for fue Ebro Delta. To OUTknowledge, prevalences reported in ¡~' this study are fue highest ever recorded for Laridae. Differences in prevalence between localities were significant, but not differences between fue sexes within each locality. Males were more intenselyparasitized than femalesin Chafarinas,and gulls from Chafarinas were more intensely parasitized than those from fue Ebro Delta. Differences in intensity were also checked using data from sympatric Yellow-legged Gulls, L. cachinnans, and only fue factor locality was significant. There was no significant relationship betweenbody condition and intensity of parasiternia in males or females in either locality. These data indicate higher susceptibility to H. lari for gulls breeding at fue Chafarinas Islands. ~_. Introduction infections in wild birds are neededto evaluate their potential effects (Bennett et al. 1992, May 1995), The interaction ofhaematozoa and their avian hosts particularly in fue case of rafe or endangered spe- has received increasedattention since parasiteshave cies, as such Audouin' s Gull, one of fue few SPEC : been recognized as agents influencing many host species (Species ofEuropean Conservation Con- fitness components (reviews by M011eret al. 1990 cero) belonging to category 1 (species of global and Clayton 1991). This influence may occur conservation concero) (Tucker & Heath 1995).The l through sexual selection (Harnilton & Zuk 1982, main potential threat for this species comes from Clayton 1991), through differential survival rates fue concentration of 84% of fue world population in of parasitized vs. non-parasitized birds (Atkinson only two breeding colonies, those ofthe Ebro Delta & van Riper 1991, Davidar & Morton 1993) or andChafarinasIslands (Pedrocchi & Ruiz 1995). through lowered reproductive success(Johnson & This situation is particularly sensitive to fue action Boyce 1991, Korpimaki et al. 1993, Riitti et al. of epizooties, thus deserving particular interest to 1993). fue study of prevalence (the proportion of individu- Therearefewdataonhaemotazoanparasitemias als infected in a population) and intensity (the in Laridae, andstudies reporting fue incidence of number of infected red blood cells in a standard 1. "' t Pc 160 ORNIS FENNICA Vol. 72, 1995 sample from an infected individual) of any kind of (Witt et al. 1982). Smears were air dried and flXed parasitemias,especially those affecting fue popula- in methanol within a few minutes of sampling. A tion during fue breeding season. numeric code identified each slide. In fue labora~ In this contribution we report and analyze data tory fue slides were stained with GIEMSA and on prevalence and intensity of fue haematozoan blind scores were obtained by exarnining smears Haemoproteus lari in Audouin's Gulls Larus underoilat 1000X. audouinii while breeding at its two main world Haemoproteus lari was identified following colonies and compare data of this species with Bennett et al. (1992). No other blood parasiteswere those obtained for a sympatric gull species, fue found (G.F. Bennett, pers. comm.). Smears were Yellow-legged Gull L cachinnans. scoredby one observer.Prevalence was established through inspection of 100 fields containing about 100 erythrocytes each, thus on fue basis of 10.000 2. Material and Metbods erythrocytes observed per sample. Intensity was established by counting fue number of infected 2.1. Study areas erythrocytes in 40 fields, thus on fue basis of 4.00~ red blood cells observed per sample. Additionally, ~ The Chafarinas Islands (Melilla, Spain: 35 ° 11'N, some blood smearsof Yellow-legged Gulls breed- 3° 46'35"E) are three small volcanic islands situated ing sympatricallywith fue Audouin' s Gulls were 4.5 Km offshore from fue Moroccan Mediterra- alsocollected both in fue Ebro delta (N = 26) and nean coast. The only inhabited island is fue central fue Chafarinas (N =6), and processed in fue same one (Isabel 11)and gulls nest on fue other two: Rey way. Francisco, placed very near Isabel 11,which con- tains most of fue Audouin' s Gull nests (ca. 3.700 in 1994) and about 600 nests ofYellow-legged Gull 2.3. Statistics (La rus cachinnans); and Congreso Is., where most of the nests correspond to Yellow-legged Gull Two collections of 15 random1y choosen smears (1.000), but algo holding about 800 nests of fromeachlocalitywerescoredtotestintraobserver Audouin's Gull in 1994. On fue Rey Is. fue domi- variations in prevalence values using fue kappa nant vegetation is formed by Suaeda vera, Lycium index of concordance (Fleiss 1981), while varia- intricatum and Atriplex halimus, whereas on tions in fue degreeof intensity recorded were tested Congreso Is. Salsola oppositifolia and Pancratium using fue intraclass correlation index, approached foetidum are almost exclusive. In both cases fue by means of fue Model 11of single factor ANOV A vegetation covers almost completely fue islands (Zar 1984). Intra-observer repeatibilities were high surface (Blanco 1988). both for prevalence (Kappa Index of Concordanc~ The Ebro Delta (40037'N, 0°21'E), is an alluvial k = 0.88) and for intensity of parasitemias(intraclasc ---"" plain of about 250 Km2 presenting a sandy flat correlation ri =0.93). peninsula of 2500 Ha, where Audouin' s Gull breeds Independence among prevalence, sex, and 10- (more than 10.000 pairs in 1994) together with cality was tested using chi-square statistics on a other seabird species.The landscapeis formed by a three-dimensional contingency table (Zar 1984). mosaic of saltmarshesand scatteredhalophytic veg- Independenceof intensity and sex was testedusing etation (Oro & Martinez 1994). fue Mann- Whitney U test, and associationbetween body condition (body mass/tarsus length) and in- fection intensity, in each locality and sex, was tested 2.2. Sampling parasites using fue Pearson corre1ation. Since, in fue caseof Yellow-legged Gull, some expected frequencies Blood smears of 90 incubating Audouin' s Gulls, were lower than 1%, we usedfue Fisher' s exact test caught under license using nest-trapson Apri11994, to check for differences in prevalence between 10- were obtained by venipuncture both in fue Ebro calities in this species.A two-factor ANOV A was Delta (N = 44) and fue Chafarinas Islands (N = 46). used on log-transformed data (K-S Lilliefors =0.07, Animals were sexed using a bill biometry index d.f. = 74, n.s.) to check for significant differences in L ~A Ruiz et al.: Blood parasites in Audouin's Gu/l 161 intensity betweenlocalities using datafrom both 4. Discussion species. All tests were two-tailed. The scant data available about haematozoans in Laridae show that fue prevalences are usually very 3. Results low (ca.5% or less,see e.g. Peirce 1981, Bennet et Table 1 shows fue number of Audouin's Gulls Table 1. Frequencies of parasitism by Haemoproteus infected vs. non-infected for each locality and sexo lari on Audouin's Gul/ by sex and locality. Globalprevalencewas92.1%fortheChafannasIs. EBRO DELTA CHAFARINAS (94.1% formales and90.5% forfemales) and28.9% d' Q d' Q for fue Ebro Delta (17.6% for males and 35.7% for females).Overallindependenceamongprevalence, PARASITIZED 3 10 20 23 sex andlocalitywasrejected(M2=62 01 P<O.OOI) NON PARASITIZED 14 17 1 2 , . .,. TOTAL 17 27 21 25 r-- and tests of partial rndependence for each varIable failed to reject fue null hypothesis only for sex (X42 =2.48, n.s.). Thus, a 2 x 2 contingencytable wasused to testfue independencebetween preva- Table 2. Intensityof Haemoproteus lari parasitism lence and locality. Results show that gulls from among infected individuals by sex and locality. Mean Chafarinas Is. presented significantly higher levels number of infected erythrocytes (standard deviation) of prevalence (X21= 39.11, P < 0.0001) thanthose andsample size are given. ofthe Ebro Delta. EBRO DELTA CHAFARINAS The results obtained checking for differences by locality using fue Yellow-legged Gull sam- MALES 30.0 (40.9) N = 3 27.35 (16.6) N = 20 pIes (Table3) alsoindicated significantly higher FEMALES 2.8 (3.36) N = 10 12.91 (8.1)N = 23 prevalencesfor fue Chafarinascolony (Fisher's exact test P = 0.002). Parasitism intensity values are given in Table Table 3. Prevalence of parasitism by Haemoproteus . lari on Yel/ow-legged Gul/s by locality. Differences 2. Srnceprevalence fo.r males at th~ Ebro Delta are statistical/y significant (Fisher's exact test P=0.002) was much lower than rn fue ChafarInasIs., thus indicating higher prevalences in the Chafarinas colony. providing a largely unbalanced sample to test intensities(Table 2), fue associationof intensity EBRO DELTA CHAFARINAS with sex was teste.d~nly at fue.Chaf.annas. ~s., PARASITIZED 7 6 /"""" wheremales had slgmficantly hlgher rntenslties NON PARASITIZED 19 O than females(U = 96.0,P < 0.001).The correla- TOTAL 26 6 tion analysesof body conditionwith intensity showedthat fue correlation was not significant l' mal l' al t .th 1 alit (Eb D lta Table 4. Intensity of Haemoproteus lari parasitism J.or esor J.em es a el er oc y ro e . f d . d. 'd I b . d I I. among In ecte In IVI ua s y specles an oca Ity . males, rl = 0.56, P = 0.62; Ebro Delta females, Mean number of infected erythrocytes (standard de- rs = -0.08, p:;; 0.83; Chafarinas males, rlO= 0.57, viation) and sample size are given.