157

PREVALENCE OF LOUSE- Diptera, Hippoboscidae PARASITING A CARDUELINE FINCH AND ITS EFFECT ON BODY CONDITION

JUAN CARLOS SENARl, JOSE LUIS COPETEl, JORDI DOMENECHI & GOTTFRIED VON WALTER2

lMuseu de Zoologia, Ap. 593, 08080 Barcelona, Spain. 2Lilienthalstr. 22, D-26129 Oldenburg, Germany.

Increasing evidence indicates that ectoparasites (see Senar 1988), and were marked with number­ have major effects on many aspects of host be­ ed aluminium rings. For each we recorded haviour and ecology (e.g. Loye & Zuk 1991). sex, age, body mass and wing-length. We trap­ This may be especially true for group-living spe­ ped a total of 6547 Serins (3468 recaptures), al­ cies. Several contact-transmitted ectoparasites though for the analysis we have only used the (e.g. fleas, mites, ticks, bugs or lices) have been trapped within the period in which louse­ shown to reduce the fitness of their host (e.g. flies appeared (May to October, 3728 Serins). Brown & Brown 1986, MOller et aZ. 1990, Loye Since average recovery period for Serins was & Zuk 1991, Moller 1993). This contrasts with longer than a month, so that the bird could get the very few data available on the ecology and additional parasites, we used first captures and prevalence of more mobile ectoparasites, such as recoveries in the analyses. Louse-flies were col­ louse flies (Diptera, Hippoboscidae). These are lected directly from the birds and were placed blood-sucking parasites, and hence can have a individually in small tubes of 70% ethyl alcohol, debilitating effect either by themselves or becau­ later being identified in the laboratory by Gw. se of the transmission of endoparasites (McClure Most of the flies were not captured, but identi­ 1984a, 1984b, Baker 1967, MOller pers. comm.). fied by size and action. Multiple regression The aim of the present paper is to describe models were built interactively using the method the phenological appearance of louse flies in the of Henderson & Velleman (1981). Serin Serinus serinus, to relate it to metereologi­ From 1985 to 1992, 48 birds with flies were cal variables and host sex and age, and to study observed (1.3% of prevalence). Four of the trap­ to what extent the presence of the parasite may ped flies were identified as turdi, and affect the body condition of the host. an additional one was identified as Ornithomyia The data presented here are based on cap­ avicuZaria. All the remaining (observed) louse­ tures of Serins from 1985 to 1992 at a permanent flies were of very small size and quick flyers, ringing station in the suburban area of Barcelona and they would most probably be Ornithoica (NE Spain). The area is formed by orchards, turdi specimens. In all cases, except one in small pine woods Pinus haZepensis and gardens, which the Serin carried two flies, only one and has a typical mediterranean climate, with per bird was recorded. mean minimum temperatures in January (10°), Louse-flies appeared from May to October, and mean maximum ones in July-August (24°). with peak prevalence in August-September (X2s Precipitation is very variable, from 30 mm in = 12.0, df = 5, p = 0.035) (Fig. 1). Prevalence January or July, to 82 mm in September (mean (arcsine transformed) for the months May to values from 1976 to 1985, Metereological Center October (months with flies positively recorded) of Barcelona). Birds were trapped at baited feed­ was positively correlated with the average mini­ ers using platform traps, clap nets and mist nets mum temperature of the previous month (r =

Received 17 December 1993, accepted 26 february 1994. ARDEA 82: 157-160 158 ARDEA 82 (1), 1994

2.5 Table 1. Multiple regression model and associated statistics for the relationship between monthly louse­

(fl flies prevalence (arcsine transformed) (dependent ~ 2.0 variable), and average minimum temperature of the cD (fl previous month and average precipitation of the .2 1.5 previous month. '0 Q) g 1.0 step 1 step 2 Constant Q) Cii ------> ~ 0.5 Variable in Temperature Precipitation

R .36 .43 R2 .13 .18 AdjustedR2 .11 .15 Fig. 1. Prevalence of Ornithoica turdi parasiting SE 2.05 2.01 Serins by month. Total number of Serins sampled: F 6.21 4.74 May, 318, June, 623, July, 502, August, 702, .02 .01 September, 842, October, 741 (only months in which P R2 change .06 louse-flies appeared have been taken into account). F change 2.98 p change .09

partial correlation .42 .26 Table 2. Multiple regression model and associated B .25 .02 -3.58 statistics for the relationship between annual louse­ SE .08 .01 1.57 flies prevalence (arcsine transformed) (dependent t 3.04 1.73 2.27 variable), and the sum of monthly average minimum P <.01 .09 .03 temperatures from May to August and the sum of monthly average precipitation from May to August. 0.36, p < 0.01). Adding into the model the aver­ age precipitation the previous month, significan­ step 1 step 2 Constant ce of the model still hold, although the change in correlation was not significant (Table 1). Neither Variable in Temperature Precipitation maximum average temperatures, number of days R .47 .88 with rain, nor number of hours of sun, either R2 .22 .77 from the previous or the analysed month, im­ Adjusted R2 .09 .68 proved the predictability of the model. SE .96 .57 Prevalence of louse-flies varied significantly F 1.68 8.34 between years (x27= 27.1, df = 4, p = 0.0003). P .24 .03 Prevalence (arcsine transformed) per year (May R2 change .55 to October) was not correlated to either of the F change 11.94 yearly metereological variables used (sum of p change .02 monthly (May to August) maximum and mini­ mum average temperatures, average precipi­ partial correlation .83 .84 B .28 .01 -18.84 tations, and number of days with rain; we ex­ SE .08 .00 5.79 cluded September and October because these t 3.29 3.46 3.26 months showed a very high precipitation rate P .02 .02 .02 masking any relationship and because of its a priori small effect on the number of flies in the Senar et at.: PARASITES IN FINCHES 159

3.0 gression model improved considerably (Table 2). In Serins, as in other cardueline finches, fe­ 92• 2.5 males stay longer periods in the nest than males. 2.0 However, analysis of prevalence by sex (taking 1.5 only reproductive individuals, i.e. Euring ages 4­ 2 6), showed no significant difference (X ]= 0.08, Co 1.0 Q) df= 1, p 0.77). Juveniles in streaked plumage >, = Q; 0.5 (3J Euring age) have in comparison to yearlings a. .~ • 85• @ (3 Euring age), more recently abandoned the 0.0 91 ~ L6;!;3;--;6:f-;4,....--;:6~5----;;6';;-6 ~67:;--;!;68;--;6<';;9:--=7~0----::;7!;-1 --=!72;;---c7~3'------07,;-;-4 nest. However, comparison of prevalence be­ .§ sum of monthly mean minimum temperatures tween these two age classes did not show any 2 o significant difference (X ] = 1.90, df = 1, p = Q) 3.0 C,) 0.17). Effect of general age (yearlings -Euring c 92• ages 3J, 3 and 5, vs. adults -ages 4 and 6) was not "* 2.5 > significant either (X2] = 3.17, df= 1, p = 0.21). ~ 2.0 An index of body condition was calculated as 1.5 the bird's mass divided by the cube of wing­ 1.0 length (see Clark 1979, Johnson et al. 1985). The

0.5 86.• body condition of Serins holding louse-flies was 88 lower (about a 3%) than the mean body condition 0.0 85• • ® 91 of Serins of the same sex and age caught on the 100 150 200 250 300 350 400 same day during the same period of the day (± sum of monthly average precipitation 1 h) (Sign test, Fig. 3; Serins without individuals for comparison were excluded from the analysis). Fig. 2. Plot of the different years of the study for Serins show a low louse-fly prevalence prevalence of louse-flies per year and A: the sum of (1.3%), within the ranges for other cardueline mean minimum temperatures from May to August, finches (McClure 1984b: 0.8 - 1.8%; see how- and B: the sum of monthly average precipitation from May to August.

33 whole season [i.e. they are the last months]). x However, plotting of prevalence against these .gs 31 .~ variables, showed a positive relationship between c prevalence and the sum of monthly average mi­ o ~ 29 c nimum temperatures (Fig. 2A), two outliers o C,) (years 1987 and 1992) being the cause of the lack >, '8 27 of significance in the correlation (r = 0.47, p = .0 0.24). Exclusion of these two points raised corre­ lation to r = 0.996 (p < 0.001). In these years, 25 precipitation was very high (they were the first infected non-infected and third year with highest precipitation, respec­ tively; 1991 was the second one but temperature Fig. 3. Body condition (mass/wing-length3) oflouse was probably too low) (Fig. 2B). Therefore, we fly infected and non-infected Serins. Values plotted as added to the model the index of annual precipita­ means ± SE. Infected birds = 30.711 ± 0.65; non­ tion (sum of monthly average precipitation from infected birds = 31.568 ± 0.56, Sign test, z = 2.028, n May to August), and the predictibility of the re- = 35, p = 0.043. 160 ARDEA 82 (1), 1994 ever Bouvier 1973). The occurrence of Orni­ cost of co1oniality in Cliff Swallows (Hirundo thoica turdi during summer and autumn with a pyrrhonota). Ecology 67:1206-1218. Burt, E.H. Jr, W. Chow & G.A Babbitt 1991. peak at the end of the summer, is also similar to Occurrence and demography of mites of Tree that of other (McClure 1984b, Walter et Swallow, House Wren, and Eastern Bluebird al. 1990). Variation in prevalence, either among nests. In: J.E. Loye & M. Zuk (eds). Bird-parasite months or years, can be explained by metereo­ interactions: ecology, evolution and behaviour: logical variation (average minimum tempera­ 69-92. Oxford Univ. Press, Oxford. Chapman, B.R & J.E. George 1991. The effects of tures and precipitation) (see also Bequaert 1952). ectoparasites on Cliff Swallow growth and Mobile ectoparasites seem therefore to be more survival. In: J.E. Loye & M. Zuk (eds). Bird­ sensitive to external variables not directly relat­ parasite interactions: ecology, evolution and ed to the host than contact-transmitted parasites behaviour: 69-92. Oxford Univ. Press, Oxford. (e.g. Burt et al. 1991, Dobson & May 1991, Clark, G.A Jr. 1979. Body weights of birds: a review. Condor 81:193-202. Harper 1992), a fact that should be taken in­ et al. Dobson, A.P. & RM. May 1991. Parasites, cuckoos, and to account when studying the interaction be­ avian population dynamics. In: C.M. Perrins, J.D. tween louse-flies and bird populations. Lebreton & G.J.M. Hirons (eds). Bird population Until recently, many ecologists assumed that studies: relevance to conservation and manage­ parasites do not harm their host. However, recent ment: 391-412. Oxford Univ. Press, Oxford. Harper, G.H., A. Marchant & D.G. Boddington 1992. studies reveal a multitude of effects of ectopara­ The ecology of the hen flea Ceratophyllus sites on hosts (e.g. Loye & Zuk 1991). Reduction gallinae and the Moorhen flea Dasypsyllys in body condition has been reported for bugs and gallinulae in nestboxes. J. Anim. Ecology ticks parasitizing nestlings (Chapman & George 61:317-327. 1991), and here we show how louse-flies may Henderson, H.V. & P.E Velleman 1981. Building multiple regression models interactively. Biome­ have a similar effect on adult hosts. trics 37:391-411. Johnson, D.H., G.L. Krapu, K.J. Reinecke & D.G. Jorde. 1985. An evaluation of condition indices ACKNOWLEDGEMENTS for birds. J. Wildl. Manage. 49:569-575. Loye, J.E. & M. Zuk 1991. Bird-parasite interactions: We thank to AP. Mpller for his comments on an ear­ ecology, evolution and behaviour. Oxford Univ. lier draft, to C.A Toft for sending us related papers, to Press, Oxford. L.M. Copete, D. Valera, A. Degollada and J. Cascales McClure, E. 1984a. Bird Banding. The Boxwood for their assistance in the field, and to Montse Aran, Press, Pacific Grove, CA from the Centre Metereologic de Barcelona for kindly McClure,E. 1984b. The occurrence of hippoboscid allowing us access to the metereo1ogical data. This flies on some species of birds in southern California. J. Field Ornithol. 55:230-240. study is a contribution to DGICYT research project Mpller, AP., K. Allander & R. Dufva 1990. Fitness PB92-0044-C02-02. effects of parasites on passerine birds: a review. In: J. Blonde1, A Gosler, J.D. Lebreton & RH. McCleery (eds). Population biology of passerine REFERENCES birds: an integrated approach: 269-280. Springer­ Verlag, Berlin. Baker, J.R. 1967. A review of the role played by the Mpller, A.P. 1993. Ectoparasites increase the cost of Hippoboscidae (Diptera) as vectors of endopara­ reproduction in their hosts. J. Anim. Ecol. sites. J. Parasitol. 53:412-418. 62:309-322. Bequaert, J.e. 1952. The Hippoboscidae or Louse­ Senar, J.C. 1988. Trapping finches with the Yunick Flies (Diptera). of and birds. Part I. Platform Trap: the residence bias. J. Field Structure, Physiology and Natural History. Ent. Ornithol. 59:381-384. Am. 32:1-209. Von Walter, G., M. Kasparek & M. von Tschirnhaus Bouvier, G. 1973. La frequence des Mallophages chez 1990. Zur Lausfliegenfauna (Diptera: Hippo­ les oiseaux de Suisse. Nos Oiseaux 32:9-15. boscidae) der Vogel in der Bundesrepublik Brown, e.R. & M.B. Brown 1986. Ectoparasitism as a Deutschland. Ecol. Birds 12:73-83.