jounal of WiIdl(fi’ Diseases. 34(4). 1998. PP#{149}820-824 © \Vildlife Disease Asskiation 1998

Oestrosis in Red from Spain

M. Lourdes Bueno-de Ia Fuente,1 Virginia Moreno,1 Jesus M. Perez,14 Isidoro Ruiz-Martinez,13 and Ramon C. Soriguer,21 Departamento de Biologia , Vegetal y Ecologia, Universidad de Ja#{233}n,Paraje Las Lagun. illas, SN. E-23071 Ja#{233}n,Spain; 2 EstaciOn BiolOgica de Do#{241}ana(C.S.l.C.). Av. Maria Luisa, S.N. E-41013 Sevilla, Spain; 3Our colleague and friend, died last July while working, and because he was the soul of this work we want to dedicate it to his memory; and Corresponding author (e-mail: [email protected]).

ABSTRACT: A survey of naso-pharyngeal my- As reported for certain Cephenemyia iasis affecting red deer (Cervus elaphus) in spp., adults seem to be attracted by the southern Spain was conducted. The parasites expelled by hosts (Anderson and involved were the larvae of Phanjngomyia picta CO2 01- and Cephenemyia auribarbis (Diptera:Oestn- kowski, 1968; Anderson, 1989). Anderson dae), which coexist sympatrically within this (1975) evidenced different strategies for host. Males and older had higher prey- larviposition by Ce’phenemyia sp. adult fe- alences amid intensities of larvae. Differences males and recognition of these by ex- in behaviour and habitat use by male and fe- male deer, and the increase of head size in old- perienced deer with subsequent behavior- er males are possibly responsible for this. There a! response to evade larviposition by oes- were low densities of C. auribarbis while P pic- trid females. Cogley and Anderson (1981) ta was the species most frequently observed, suggested a dependence by these parasites although both oestrids were located in the on the anatomy of the host’s muzzle for same host cavities. The earlier larviposition by C. auribarbis, and its faster larval development larval invasion. They also noted a positive may reflect asynchronous life-cycles of both thermotropism and a negative phototro- oestrids; this may decrease inter-specific corn- pism by Cephenemyua sp. first-instar lar- petition between these sympatric species. vae. Key words: , Cephenemyia auribar- Mixed infections of red deer due to P his, Cervus elaphus, inter-specific competition, Oestndae, Phanjngoinyia picta, sympatnc spe- pucta and C. auribarbis have been com- cies. monly reported in Europe (Drozdz, 1961b; Zumpt, 1965; Sugar, 1974, 1976; Pharyngomyia picta infects the naso-ol- Gil Collado et a!., 1985; Ruiz and Palo- factory and pharyngeal cavities of deer in mares, 1993; Ruiz et al., 1993). The main Europe. Its main host is the red deer (Cer- goal of this study was to improve our vus elaphus), although it is assumed that knowledge on the epidemiology of these this species does not show a host-specifity parasites, and to analyze their co-occur- as pronounced as seen in the European rence within the same host individuals. species of the genus Cephenemyua. The From November 1994 to February genus Cephenemyma is restricted to the 1996, 521 red deer (244 males and 277 Holarctic region and the larvae parasitize females) were examined for oestrid larvae. deer belonging to the subfamilies Cervinae Samples came from different game re- and Odocoileinae. The imagos of all Ce- serves located in the Sierras de Cazorla, phenemyia spp. have a general appearance Segura y Las Villas Natural Park, Jaen like that of bumble-bees (Zumpt, 1965). Province (38#{176}30’N, 2#{176}45’E); Sierra More- The main host for C. auribarbis is the red na, Ciudad Real, Jaen and C#{243}rdoba prov- deer, although both oestrid species also in- inces (38#{176}17’N, 3#{176}45’W and 38#{176}26’N, fect the fallow deer (Dama dama) (Ruiz et 4#{176}19’W); Guadalcanal (38#{176}06’N, 5#{176}49’W)y a!., 1993). In central and western Europe Cazalla (37#{176}56’N, 5#{176}45’W), Sevilla Prov- adult P picta fly from June to August (Se- ince; Ubrique (36#{176}40’N, 5#{176}25’W) and Al- guy, 1928; Drozdz, 1961a), while C. auri- cal#{225}de los Gazules (36#{176}29’N, 5#{176}43’W), Ca- barbus imagos are active from May to July diz Province (southern Spain). Availability (Brauer, 1863; Seguy, 1928; Cameron, of samples was limited by the official hunt- 1932). ing period from October to February.

820 SHORT COMMUNICATIONS 821

T.SR!.1.; 1. Prevalence and intensity of b ized by both oestrid species. Prevalence of two species of nasal bots in red (leer from Spain ac- cording to host sex and age. oestrosis was significantly higher (x2 = 30.538; d.f. = 1; P < 0.0001) in males

/ I ntensitv ( )f I)(trasitismil (94%) than in females (77%). Prevalence Prese- also increased with host age (Table 1). An- (;thgors n’ knee Mm1’ Mast S SDd nual prevalence did not show significant Age class (‘r) differences (x2 0.79; d.f. 2; P <1 35 57 1 84 20.! ± 16.8 0.4525) within the study period (1994- 1-3 118 76 1 104 23.8 ± 20.9 4-6 115 89 1 102 21.2 ± 19.4 1996) but reached highest values (up to 7-9 116 MM 1 106 28.9 ± 26.9 96%) in winter months. >10 137 94 1 145 29.4 ± 28.6 The mean intensity ( ± SD) of parasit-

Males 244 94 1 145 :32.9 ± 27.2 ism obtained was 25.8 ± 23.9 larvae/host Females 277 77 1 106 12.1 ± 17.2 individual; 24.1 ± 21.4 for P pucta larvae

TOTAL 521 85 1 145 25.8 ± 23.9 and 7.2 ± 6.1 for C. auribarbis hots. In- tensity in male deer was significantly high- Ii = m,mmmilxr ttniineeI. NIin = mnimuimnmmmn. er than in females (F 57.63; d.f. 1; P Skis = mnaximimmimmi. < 0.0001). Number of bots/host infected S SI) = neon standard elevmatinn. also increased with host age (Table 1). The intensity of parasitism reached values of Deer heads were collected, stored, and ex- over 40 hots/host in February-April. Nev- amined according to Ruiz and Palomares ertheless, the modal value for intensity of (1993) and Ruiz et a!. (1993). Age of deer both oestrid species was 1 larva/host par- was determined following criteria given by asitized. Larson and Taber (1980) and Dimmick Data obtained on frequencies of num- and Pelton ( 1994); five host age classes her of larvae indicated that P pucta showed were considered (Table 1). a negative binomial distribution (K 3.03;

Location of each parasite was recorded, I = 2.62; variance 6.46), while that for and oestnd larvae were identified accord- C. auribarbus fitted to a Poisson distribu- ing to Cameron (1932), Grunin (1957), tion (K = 6.62; 1 0.60; variance 0.72) Zumpt (1965), and Draber-Monko (1975). (Diggle, 1983). Prevalence and intensity of parasitism Location of larvae belonging to different were derived according to Margolis et a!. instars was similar for both species. First- ( 1982) and Bush et a!. (1997). In order to instar larvae (L1) were mainly located in compare prevalence and intensity of par- the naso-olfactory area (86% of L1 P picta, asitism between different host sex and age and 98% of L1 C. auribarbis). With regard classes, we used the x2 as well as Levene’s to the second-instar larvae (L9), most of F tests (Soka! and Rohlf, 1995) which were these were found in the gnathocranium performed with the BMDP program (Dix- (64% of Lc, P picta and 61% of L2 C. an- on, 1990). Type material (five third-instar rubarbis), although important numbers larvae of each species) was deposited at (36% of L2 P pucta and 39% of L2 C. an- the Museo Naciona! de Ciencias Naturales ribarbis) were located in the splanchno- (CSIC) (Madrid, Spain). cranium. Most of the third-instar larvae Prevalence of oestrosis reached 85% (n (L3) were collected from the deer gnath-

= 521), Pharyngoinyia picta being the ocranium (93% of L3 P picta and 93% of species most frequently observed, 85% of L3 C. auribarbis). the total larvae collected (11,433). Phar- When analyzing monthly percentage of yngomyia picta affected 77% of hosts ex- each larval instar for both species (Fig. 1), amined, and C. auribarbis larvae were we observed that increases of L1 C. ann- found in 46% of red deer in our study. The barbis larvae did not happen at the same 39% of deer were simultaneously parasit- time as those for P picta, with a difference 822 JOURNAL OF WILDLIFE DISEASES, VOL. 34, NO. 4, OCTOBER 1998

correspond well with those given by other authors (Drozdz, 1961b; Sugar, 1974, 1976; Gil Collado et a!., 1985). As expect- ed, prevalence of P picta was higher than that obtained for C. auribarbis, and adult deer were more frequently parasitized than younger animals. However, this is the first report of males being more severely parasitized, in terms of both prevalence MQIJTI-4S and number of hots. Perez et al. (1996) reported a significantly higher prevalence of oestrosis due to caucasicus in Spanish ibex (Capra pyrenauca) females. These above differences in prevalence and intensity of nasal hots may be ex- planed by (1) differential activity patterns and habitat use by male and female deer (Soriguer et a!., 1994); (2) spatial distri- bution and location of adult flies; and/or

Sop ct Do J” Fob P,4ar A (3) differential behaviour patterns of both AFJTI-IS host sexes when attacked by flies larvipos- iting, with subsequent differences in infec- I OC tion success. With regard to the third point, we also consider the fact that groups of fawns may improve their defense against flies. The increased number of larvae with host age and in males (Table 1) seems to be related to increasing head size, provid- ing greater availability of suitable habitat II for parasites. Alternatively, the lower prev- Te4S alence shown by C. auribarbis, together

FIGURE 1. Monthly fluctuations of percentages of with the small number of larvae/host and different larval instars (A = L1, B = L2, C L3) of the type of distribution within the host Plmanjngoinyia pick! (-) afl(l Cephenemyia an ri ha r- sample, may reflect low densities of this his ( ) in red (leer from Spain. oestrid species with respect to those of P picta. of about 2 mo (Fig. 1). Some pupae were As a standardized value, the mean in- removed during sampling in both deer na- tensity, or the average intensity of a par- sa! and pharyngeal cavities, 41 belonging ticular parasite species among the infected to C. auribarbis and 29 belonging to P individuals of a particular host species picta. Over 95% of C. auribarbis pupae (Margolis et a!., 1982; Bush et al., 1997) were found during December and January, was used. Nevertheless, frequently we ob- while almost 90% of P pucta pupae were served asymmetric or biased distributions. collected in February. In such cases we think that the mean in- The mean prevalence of nasal hots in tensity (± SD), together with the modal red deer obtained in our study was similar value could describe their pattern of abun- to those values reported in previous stud- dance in a better way. ies for the same geographic area (Ruiz and The larval maturation period is shorter Palomares, 1993; Ruiz et a!., 1993), and for C. auribarbis (Cameron, 1932; Zumpt, SHORT COMMUNICATIONS 823

1965; Sugar, 1974; Gil Collado et a!., tera: Oestridae: Oestrinae). International Journal 1985). In this sense, we have observed of Parasitology I 1: 28 1-286. DIGGLE, P. J. 1983. Statistical analysis of spatial how C. auribarbis larvae reach larger size point patterns. Academic Press. London. UK, and heavier weight than P picta larvae, de- 148 pp. spite L1 P picta being almost twice the DINIMIcK, R. W., AND M. R. PELTON. 1994. Criteria size of C. auribarbis. When analyzing of sex and age. hi Hesearch and management monthly frequencies (Fig. 1), we also oh- techniques for wildlife and habitats, TA. Book- bout (ed). The Wildlife Society, Bethesda, Mary- served that increases of L1 larvae did not land, pp. 169-214. happen simultaneously in both oestrid spe- DIxoN, W. J. (ED.). 1990. BMDP statistical software cies, C. auribarbis increases occurred manual. University of California Press, Berkeley, about 2 mo earlier. A similar trend was oh- California, 1385 pp. served regarding L3 larvae and pupae. DRABER-MONKO, A. 1975. Morphologic einiger Fliegenlarven der Familie Oestridae (l)iptera). Ruiz and Palomares (1993) noted little co- Annales Zo()logici 32: 239-247. incidence between percentages of differ- DR0zDZ, J. 1961a. New data from biology of P/mar- ent larval instars and pupae for both oes- yngo;nyia picta Meigen larvae ( l)iptera:Oestri- tnd species. In our opinion these differ- dae) a Cervus clap/ins parasite. Wiadomosci Par- ences in larval and pupal phenology must azytologiczne 7: 373-379. . 1961h. Cephenomyinae (I)iptera:Oestridae) be considered as a part of the asynchro- of cervids in Poland. Wiadomosci Parazvtologi- nous life-cycles of these oestrid species; czne 7: 381-382. this may help reduce the inter-specific Cu. CoI.I.AD0, J., J. L. VAI.!.S, AN!) Y. FIERRO. 1985. competition between these sympatric dip- Estudio de las larvas eje Oestridae par#{225}.sitasde tera. Cervidae en Espa#{241}a. Boletim de Ia Sociedade Portuguesa de Entomologia I : 467-475. The authors wish to thank M. A. Simon CRUNIN, K. Y. 1957. Nasopharvngeal gad-flies (Oes- and A. Blanco for their help in obtaining tridae). Fauna of the USSR. Zoological Institute, material examined in this study. We also Academy of Science, USSR 19: 1-146. (In Rus- are indebted to J. E. Granados, J. Navarro, sian) LARSON, J. S., AN!) H. D. TABER. 1980. Criteria of and E . Garcia for their collaboration in sex and age. in Wildlife management techniques transporting samples. manual, S. D. Schemnitz (ed). The Wildlife So- ciety, Washington I).C., pp. 143-202. LITERATURE CITED MARGOLIS, L., C. W EscI-i, J. C. hOLMES, A. M. ANDERSoN, J. H. 1975. The behaviorofnose bot flies KURIS, AN!) (. A. SCHAD. 1982. The use of eco- (Ceplieneinyia apicata and C. jellisoni) svhen at- logical terms in Parasitology (report of an a(1 hoc tacking black-tailed (leer (Odocoilens Imeinionus committee of the American Society of Parasitol- coluinhianus) and the resulting reactions of the ogists). The Journal of Para.sitology 68: 131-133. (leer. Canadian Journal of Zoology 53: 977-992. PEREZ, J. M., J. E. GRANADOS, H. C. SORIGUER, AND 1989. Use of deer models to study larvipo- I. HuIZ. 1996. Prevalence and seasonalitv of sition b wild nasopharvngeal bot flies (Diptera: Oestrus caucasicus Crunin, 1948 (Diptera:Oes- Oestridae). Journal of Medical Entomology 26: tridae) parasitizing the Spanish ihex. Capra pyr- 2:34-2:36. enaica (Mammalia:Artiodactila). The Journal of .NI) W OI.K0WSKI. 1968. Carbon dioxide as Parasitology 82: 233-236.

an attractant for host-seeking Ceplmeememyia fe- RU!Z, I., AND F. PALOMARES. 1993. Occurrence and males (l)iptera:Oestridae). Nature 220: 190-191. overlapping of pharvngeal hot flies Plmaryngo- BRAUER. F. 186:3. Monographie der oestriden. W ?nyia picta and Cep/wnemyia an nbarbis (Oestri- Brammmiiller. Wien, Austria, 291 pp. dae) in red (leer of southern Spain. Veterinary Bus!!. A. 0., K. 1). LAFFERTY, J. M. L017., AN!) A. Parasitology 47: 119-127. \V. SIIOSTAK. 1997. Parasitology meets ecology H. C. SORIGUER, AND J. M. PEREZ. 1993. on its own terms: Margolis et al. revlsite(l. The Pharyngeal hot flies (Oestridae) from sympatric Journal of Parasitologv 83: 575-583. wild cervids in southern Spain. The Journal of CAMERON, A. E. 1932. The nasal hot fly, Cepimene- Parasitology 79: 623-626. ini,ia an nharhis Meig. (1)iptera:Tachinidae) of SEGUY, E. 1928. Etude sur les mouches parasites. I. the red (leer, Ccrvus clap/ins’ L. Parasitology 24: Conopides, Oestrides et Calliphori nes (Ic I 85-195. l’Europe occidentale. Paul Lechevalier, Paris, COG!.EY, T. P.. AN!) J. H. ANDERSON. 1981. Invasion France, 240 pp. of l)lack-taile(I (leer b’ nose hot fly larvae (1)ip- SOKAL, H. H., AN!) F. J. ROHLF. 1995. Biometry. The 824 JOURNAL OF WILDLIFE DISEASES, VOL. 34, NO. 4, OCTOBER 1998

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