Ardeola 47(2), 2000, 191-195

INTESTINAL PARASITES IN THE TETRAO UROGALLUS CANTABRICUS: A COPROLOGICAL STUDY

José Ramón OBESO*, Luis Darío RODRêGUEZ**, Ibo ÁLVAREZ**, Eloy NIÑO*** & Juan Carlos DEL CAMPO***

SUMMARY.ÐIntestinal parasites in the Cantabrian Capercaillie, Tetrao urogallus cantabricus: a copro- logical study. The intestinal parasites of the Cantabrian Capercaillie were Estudied by counting the of pa- rasitic found in 154 faecal samples from 34 localities in the . Prevalence was 58% for sp. and 25% for sp.; however, both intensity and mean intensity of these parasi- tes were very low if compared to other populations of Tetraonidae. Other parasites were infrequent and, spe- cifically, we found no cestodes which are characteristic parasites of the Tetrao (Raillietina sp. and Da- vainea sp.). We conclude that it is unlikely that intestinal parasites cause the decline of Capercaillie populations in the studied localities of the Cantabrian range. Key words: Ascaridia, Cantabrian range, Capercaillie, Capillaria, Eimeria, faecal analysis, intestinal pa- rasites.

RESUMEN.ÐParásitos intestinales en el Urogallo Común Cantábrico Tetrao urogallus cantabricus: un es- tudio coprológico. Los parásitos intestinales de los Urogallos Cantábricos Comunes se estudiaron analizando el número de huevos de estos parásitos que aparecieron en 154 muestras fecales correspondientes a 34 loca- lidades de la cordillera Cantábrica. La prevalencia fue del 58% para Eimeria sp. y del 25% para Capillaria sp. No obstante tanto la intensidad como la intensidad media fueron muy bajas comparadas con las que pueden encontrarse en otras poblaciones de Tetraonidae. Otros parásitos fueron muy poco frecuentes y en concreto no se encontraron los céstodos típicos del género Tetrao (Raillietina sp. y Davainea sp.). Se concluye que es im- probable que los parasitos intestinales sean la causa del declive observado en las poblaciones cantábricas de Urogallos Comunes. Palabras clave: análisis fecal, Ascaridia, Capillaria, Cordillera Cantábrica, Eimeria, parásitos intestina- les, Tetraonidae, Urogallo Común.

INTRODUCTION 1986a); however, this particular has not been confirmed by Moss et al. (1990). Within the Diseases and parasites have been proposed Tetrao genus, the Black , T. tetrix, is as factors associated to the decline in numbers parasitized by the protozoan Leucocytozoon lo- of several Tetraonidae species. For example, vati and microfilaria, probably produced by the lagopus scoticus often nematode worm Splendidofilaria tuvensis. Hö- have outbreaks of Çgrouse diseaseÈ, when glund et al. (1992) found that parasites have adults die in poor condition, parasitized by the no effect on adult mortality of caecal threadworm Trichostrongylus tenuis, males. infected with microfilaria had whose prevalence is almost 100% in adults shorter tail ornaments, which is compatible (Watson & Shaw, 1991). Population studies on with the hypothesis of Hamilton & Zuk (1982). this species also show a negative correlation However, there is no evidence that parasitic in- between breeding success and the intensity of fection can diminish mating success in Tetrao infection by Trichostrongylus (Hudson, 1986b; (Höglund et al., 1992). This effect has been Shaw & Moss, 1989, 1990). It seems that in- demonstrated in Sage Grouse ( fected Red Grouse could undergo an increase urophasianus) and in semi-captive in their vulnerability to predators (Hudson, (Gallus gallus; Zuk et al., 1990). In fact, very * Departamento de Biología de Organismos y Sistemas, Unidad de Ecología, Universidad de Oviedo, E- 33071 Oviedo. ** Sección de Microbiología y Parasitología, Laboratorio de Sanidad , Consejería de Agricultu- ra, Jove, E-33299 Gijón. *** Consejería de Medio Ambiente, Principado de Asturias, Coronel Aranda, 2, E-33071, Oviedo. 192 OBESO, J. R.; RODRÍGUEZ, L. D.; ÁLVAREZ, I.; NIÑO, E. & DEL CAMPO, J. C. little is known about the intestinal parasites of were introduced in plastic vials, kept in the re- Capercaillie, Tetrao urogallus, which have frigerator and sent to the laboratory and analy- been described by Bezubik (1969). Its nemato- sed within two days after collection. de species throughout the Palaearctic Region Three grams of each sample were weighed were reviewed by Barus et al. (1984). De Fran- and shaken in a saturated solution of potassium ceschi (1994) asserted that parasites can incre- iodomercuriate, and the eggs of the parasites ase Capercaillie mortality rate in the Italian counted under the microscope. We assumed a Alps, where it suffers from the Nematoda positive relationship between the number of Ascaridia cylindrica and the Mallophaga Go- parasites and the number of worm eggs appea- nioides tetraornis. However, there is no infor- ring in the droppings, as reported for captive mation at all about these parasites in the subs- Red Grouse (Shaw & Moss, 1989). pecies T. u. cantabricus. Because our method of evaluation of parasi- The Cantabrian Capercaillie, T. u. cantabri- tic infection was indirect (droppings analysis), cus, population has declined during the last two two or more samples might belong to the same decades and, although the available information . To avoid this source of error, one sample on its population trends is still very scant, some was taken from each group of droppings, and studies have estimated about 25-50% popula- the samples were collected well apart (e.g. in tion reduction in the last twenty years (Purroy, different leks) to warrant that they belonged to 1997, 1999). The most commonly reported li- different individuals. A second methodologi- miting factors for Capercaillie are reduc- cal problem may be related to the phenology of tion and fragmentation (Storch, 1991, 1997; Me- sample collection because the number of eggs noni et al., 1997), predation, which might laid vary with the phase of the life history of increase in fragmented (Kurki et al., the parasites, which in turn may change from 1997), competition with ungulates (Klaus & late March to early June. In this sense, we con- Bergmann, 1994; Moss & Picozzi, 1994; Picoz- sidered separately two phenological periods: zi et al., 1996) and climatic change (Moss, 1985; 25 March to 30 April and 1 May to 9 June. Pulliainen & Tunkkari, 1991; Moss & Picozzi, The prevalence (percentage of a host popu- 1994). The relevance of these factors varies ac- lation infected with a specific parasite), inten- cording to geographical areas. In this study we sity (number of parasites in a particular host) examine the intestinal parasites found in the and mean intensity (mean number of parasites droppings to determine whether the infection by per host in a population of hosts, including non intestinal parasites might be a relevant factor infected hosts) were calculated for each genus. for Cantabrian populations of Capercaillie. The effect of geographical location (western vs. central-eastern Cantabrian range localities) and phenology on prevalence of infection was STUDY AREA AND METHODS tested using chi-square tests. Two-way ANO- VAs considering geographical location and Fresh droppings were collected in leks from phenological period as random factors (Model the Cantabrian range between 25 March and 9 II), were used to test differences in mean inten- June 1998. This period was suitable to examine sity of infection between zones and periods. parasites in faeces because eggs laid by adult When only infected host were considered, the- worms are voided in the droppings during the re were no data for all cells and genera in two- spring. Despite the droppings being very rare in way ANOVAs, so the intensity of infection was the field, only fresh faeces were collected in tested using one-way ANOVAs. order to avoid contamination by soil organisms. We collected 154 fresh droppings from 34 lo- calities, 7 from northeastern León province and RESULTS 27 from Asturias province (north of the Canta- brian range): Allande (1), Ibias (1), Degaña (1) Nearly 69% of droppings were found to be and Cangas de Narcea (16) in the western Can- infected by at least one species of parasite. We tabrian range; Somiedo (2), Terverga (2), Lena found one parasite genus in 44% of the drop- (1) and Aller (1) in the center and Ponga (2) in pings, two genera in 24% and the occurrence of the eastern Cantabrian range. The droppings more than two genera simultaneously in only INTESTINAL PARASITES IN THE CANTABRIAN CAPERCAILLIE TETRAO UROGALLUS CANTABRICUS 193 lation). = 91) de la cordillera Cantábrica. Pre- n = 91) of the Cantabrian range. Prevalence (percentage n ) y del centro-oriente ( 63 = n 1 ABLE T = 63) and central-eastern zones ( n [Occidente] [Centro-oriente] Western Cantabrian range Centre-Eastern Cantabrian range Prevalence Intensity Mean intensity Prevalence Intensity Mean intensity [Prevalencia] [Intensidad] [Intensidad media] [Prevalencia] [Intensidad] [Intensidad media] sp. 3.2 1.0 0.03 ± 0.17 1.0 2 0.02 ± 0.22 sp. 22.2 1.93 ± 1.27 0.43 ± 0.99 29.7 8.7 ± 8.9 2.60 ± 6.20 sp. 4.8 6.7 ± 2.1 0.32 ± 1.47 8.8 2.4 ± 0.9 0.21 ± 0.72 sp. 1.6 2.0 0.03 ± 0.25 5.5 12.6 ± 13.6 0.69 ± 4.07 sp. 58.7 181.2 ± 198.9 106.4 ± 176.2 62.6 79.5 ± 113.9 49.8 ± 97.8 Eimeria Ascaridia Capillaria Trichostrongylus Heterakis valencia (en porcentaje), intensidad en los individuos afectados, (media ± d.t.), e intensidad (media, ± d.t.), en la población.] Unidentified parasites: 7.9 3.6 ± 1.5 0.28 ± 1.05 4.4 1.5 ± 1.0 0.07 ± 0.35 Eggs of intestinal parasites appearing in droppings from western ( of infected hosts), intensity (mean, SD, eggs per host) and mean number host popu [Huevos de parásitos intestinales encontrados en las muestras fecales del occidente ( Coccidia: Nematodes: 194 OBESO, J. R.; RODRÍGUEZ, L. D.; ÁLVAREZ, I.; NIÑO, E. & DEL CAMPO, J. C.

5%. The prevalence for each generus showed found (Watson & Shaw, 1991). Nevertheless, high variability (Table 1), being 57.7% for the differences between species may be remarkable Coccidia Eimeria sp. and 25% for the Nemato- despite sharing the same habitat, as occurs in de Capillaria. The prevalence for other hel- sympatric populations of Lagopus mutus and minthic parasites was very low. Neither geo- L. lagopus scoticus: the prevalence of Trichos- χ2 graphical location ( 4= 2.96, P > 0.05; Table 1) trongylus in the latter is 100% and only 50% in χ2 nor phenological periods ( 2 = 5.2, P > 0.05) the former species (Watson & Shaw, 1991). had significant effects on the prevalence of the Prevalence found in this study was similar to genera found in the samples. that reported for Tetrao tetrix in Norway (Hö- Intensity of the infection was relatively high glund et al., 1992), except for Eimeria, where only in the case of Eimeria sp. (115 eggs per 3 we found higher levels of infection. Surpri- grams of fresh faeces and nine samples with singly we did not detect eggs of cestodes, Rai- more than 500 eggs). Mean intensity was low llietina globocauda, R. urogalli and Davainea for all specific parasites, and Eimeria sp. sho- tetraonensis, which are typical parasites of the wed the highest values (Table 1). genus Tetrao. In the same way, Trichostrongy- Droppings from the western Cantabrian lus sp. only appeared in three droppings from range showed significantly higher intensity two western and one eastern locality. Howe- of infection with Eimeria sp. than droppings ver, it should be pointed out that estimated pre- from the central-eastern range (Table 1; valence is a minimum value since eggs are laid

F1, 92 = 9.936, P = 0.002). However, the in- by adult worms, and in some life history stages tensity of infection with Capillaria sp., alt- of the parasite only larvae are present. hough low in all sites, was significantly higher The review by Barus et al. (1984) describes in the central-eastern zone than in the wes- some nematode species parasitizing T. uroga- tern zone (F1,40 = 7.933, P = 0.008). llus that were not found here: Cyrnea aptero- The intensity of infection showed no signifi- cerca, relatively widespread in the stomach of cant differences between phenological periods Tetraonidae, Aonchotheca caudinflata, cosmo- for Capillaria sp. (F1,39 = 0.959, P = 0.334), politally widespread and common intestinal pa- and was only barely significant for Eimeria sp. rasite of T. urogallus, and Subulura brumpti,

(F1,92 = 3.828, P = 0.053), which exhibited caecal parasite rare in T. urogallus. However, slightly higher numbers of eggs in the drop- this review describes Capillaria sp. and Asca- pings from the period May-June. ridia sp. as common parasites of T. urogallus When mean intensity of infection was consi- that were found throughout its range. dered, two-way ANOVA results showed that Differences between zones in both prevalen- neither geographical location (F1,1 = 37.575, ce and intensity of infection might be attributed P = 0.369 for Capillaria sp. and F1,1 = 36.542, in the case of Eimeria sp. to the higher density P = 0.104 for Eimeria sp.) nor phenology of Capercaillie in the western zone, which

(F1,1 = 2.201, P = 0.096 for Capillaria sp. and might increase the probability of infection. Ca- F1,1 = 10.240, P = 0.193 for Eimeria sp.) had percaillie populations are declining in eastern significant effects on mean intensity of infec- and especially central zones of the Cantabrian tion. Similarly, the interactions between the range at higher rates than in the western zones, two factors were not significant (F1,144 = 0.129, where both population and range remain relati- P = 0.065 for Capillaria sp. and F1,144 = 0.103; vely steady (unpublished census, Consejería P = 0.369 for Eimeria sp. ). Medio Ambiente, Principado de Asturias). Ho- wever, this association between prevalence and density of hosts is very speculative because dif- DISCUSSION ferences in prevalence between localities seem to be an usual pattern in the Tetraonidae and The results suggest that the extent of infec- there is no straightforward explanation for re- tion by helminth parasites in the Cantabrian ported differences (Watson & Shaw, 1991). Capercaillies was relatively low when compa- We can conclude that intestinal parasites are red to other populations of Tetraonidae, where probably not a limiting factor for the Canta- prevalences of 100% and intensities of thou- brian Capercaillie populations, at least in the sands of eggs per gram of faeces have been localities considered in this study. However, INTESTINAL PARASITES IN THE CANTABRIAN CAPERCAILLIE TETRAO UROGALLUS CANTABRICUS 195 an estimation of worm eggs is still a valuable MENONI, E., LANDRY, P. & BERDUCOU, C. 1997. Ha- information about the body condition of the bitat fragmentation and viability of Capercaillie birds, and should be included in future monito- populations in the French Pyrenees. Wildlife Bio- ring of Cantabrian Capercaillie populations. logy, 3: 277. MOSS, R. 1985. Rain, breeding success and distri- bution of Capercaille Tetrao urogallus and black ACKNOWLEDGEMENTS.ÐLuis Llaneza and Luis Ro- grouse Tetrao tetrix in Scotland. Ibis, 128: 65-72. bles collected the samples from León province. S. MOSS, R., TRENHOLM, I. B., WATSON, A. & PARR, Solano, P. Silva and P. Quirós collected several sam- R. 1990. Parasitism, predation and survival of hen ples from the western Cantabrian range. Several ran- Red Grouse Lagopus lagopus scoticus in spring. gers from the Servicio de Guardería del Principado Journal of Animal Ecology, 59: 631-642. de Asturias have enthusiastically contributed to this MOSS, R. & PICOZZI, N. 1994. Management of work by collecting samples in many places during for Capercaillie in Scotland. Forestry Commission spring the 1998 counts in the leks. The comments by Bulletin, 113: 1-29. an anonymous referee improved the original draft. PICOZZI, N., MOSS, R. & CATT, D. C. 1996. Caper- There was no financial support for this study. caillie habitat, diet and management in a Sitka spruce plantation in central Scotland. Forestry, 69: 373-388. BIBLIOGRAPHY PULLIAINEN, E. & TUNKKARI, P. 1991. Responses by the Capercaillie Tetrao urogallus, and the Willow BARUS, V., SONIN, M. D., TENORA, F. & WIGER, R. Grouse Lagopus lagopus, to the green matter avai- 1984. Survey of nematodes parasitizing the genus lable in early spring. Holarctic Ecology, 14: 156- Tetrao () in the Palaearctic region. 160. Helminthologia, 21: 3-15. PURROY, F. J. 1997. El Urogallo desaparece de la BEZUBIK, B. 1969. Helminth parasites of Black Grou- Cordillera Cantábrica. 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Oecologia, 88: 359-361. urogallus) in central Europe, particularly in Ger- ZUK, M., JOHNSON, K., THORNHILL, R. & LIGON, J. D. many, including an evaluation of reintroductions. 1990. Parasites and male ornaments in free-ran- Game & Wildlife, 11: 57-80. ging and captive Red Jungle . Behaviour, KURKI, S., HELLE, P., LINDÉN, H. & NIKULA, A. 114: 232-248. 1997. Breeding success of Black Grouse and Ca- percaillie in relation to mammalian predator den- [Recibido: 29-11-99] sities on two spatial scales. Oikos, 79: 301-310. [Aceptado: 11-5-00]