The preening activity of swallows, Hirundo rustica, in relation to experimentally manipulated loads of haematophagous mites

Anita. Behav., 1991,42, 251~60

The preening activity of swallows, Hirundo rustica, in relation to experimentally manipulated loads of haematophagous mites ANDERS PAPE MI3LLER Department of Zoology, Uppsala University, Box 561, S-751 22 Uppsala, Sweden (Received 5 July 1990; initial acceptance 18 August 1990; final acceptance 8 January 1991; MS. number: 3608}

Abstract. Whether differences in preening activity among breeding swallows might be a reliable predictor of infection rates by the haematophagous mite Ornithonyssus bursa was tested by recording preening during an experimental manipulation of mite population density. Mite populations of newly built nests were either decreased by spraying with a pesticide, or increased by inoculation with ca 50 mites, while other nests were kept as controls. Adult swallows did not alter their preening rates in relation to experimental treatment despite the fact that the experimental treatments strongly affected mite densities. Nestlings raised in nests inoculated with mites preened much more than did control nestlings, which preened more than did nestlings from sprayed nests. Individual swallows had consistent preening rates throughout the breeding season. Male swallows preened more than females, and male preening activity was strongly positively correlated with that of their mates. Swallows preening much during their first clutches maintained a high preening frequency during their second clutch, although there was a general seasonal decrease in preening rates. Swallows rearing two broods preened more than did pairs rearing only a single brood.

Parasites are a major cause of loss of fitness in many animal species (e.g. Elton 1927; Mattingly 1969; Boycott 1971; Page 1976; Moiler et al. 1990). It is therefore essential for individuals to reduce their effects by preventing infections, and once infected by attempting to reduce or eliminate parasite loads or effects. Ectoparasites typically disperse whenever two or more host individuals are close to each other (e.g. Kennedy 1975), as for example during reproduction in sexually reproducing animals. Individual hosts able to assess levels of parasite infection of potential mates at a distance should less often become infected themselves and therefore should enjoy enhanced fitness. Hosts may perceive parasite infections either by observing the parasites directly or by recording altered host appearance or behaviour. Direct fitness effects due to parasites should strongly affect mate choice and lead to avoidance of conspecifics with heavy parasite loads. If parasites can be transmitted directly, and if they have a direct fitness cost to the host, individual hosts should pay particular attention to preening or similar behaviour, which could mirror parasite burdens of potential mates. Previously Clay (1957) and later Goodwin (1983) suggested that preening 0003-3472/91/080251 + 10 $03.00/0

intensity might be an important factor influencing the size of mallophaga populations in birds, and later studies of domestic fowl, Gallus gallus domesticus, supported this view (Kartman 1949; Brown 1972, 1974). Among mammals also, individuals prevented from grooming become more severely infected with ectoparasites than individuals fully able to groom (Snowball 1956; Murray 1961, 1987; Bell et al. 1962; Lewis et al. 1967; Bennett 1969). Mice, Mus dornesticus, which often altogroom, did not suffer from increased infestation levels when housed together with other individuals prevented from self scratching (Bell et al. 1962). Field studies of whether heavily infested hosts spend more time grooming than do less parasitized individuals, however, are totally wanting. I evaluated the hypothesis, that preening activity of hosts reflects parasite loads, by manipulating parasite (mite) loads of swallow nests early during reproduction and subsequently recording preening activity. Swallows are ca 20 ginsectivorous passerines that usually nest in small colonies. Nests, built of mud, straw, hair and feathers at a height of 2-3 m (facilitating observations), often last many years, and

9 1991The Association for the Study of Animal Behaviour 251

Animal Behaviour, 42, 2

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parasite loads of nests may therefore build up as nests become older. The tropical fowl mite, Ornithonyssus bursa, is a generalist haematophagous mite living both on the swallows and in their nests. Mites are ca 0-76 mm long, and they can thus not easily move between swallow nests which are usually 4-8 m apart. Their entire life cycle lasts only 5-7 days, and each female produces several clutches, each with up to seven eggs (Sikes & Chamberlain 1954). Juveniles need at least two blood meals in order to moult into the adult stage, and adults need at least two blood meals to produce a clutch of eggs (Sikes & Chamberlain 1954). Mites are found on adult swallows upon spring arrival at their breeding sites (Moller, in press). In my study area at this time, prevalences are 39% in males and 33% in females (Moller 1990a). Intensities of infection of adult swallows are 16-4 mites per infected male and 3.9 mites per infected female (Moller 1990a). Numbers of mites in swallow nests build up quickly during reproduction of their hosts, the prevalence being 45% of first clutch nests and 34% of second clutch nests, and the intensity of infection among infected nests being 63 mites for first clutch nests and 50 mites for second clutch nests (Moller 1990a), the record being 14000 mites in one swallow's nest (Moller, in press). Infestations of nests originate primarily from infestations of adults (Moller 1990a). Mites severely reduce the number and quality of young produced by their hosts (Moller 1990a). Swallow reproduction is delayed by mite infestations, and as a result fledgling survival is reduced (Moller 1990a). Mites also directly affect the well-being of adult swallows, since infested individuals reproduce later and lay fewer eggs (Moller 1990a). The size of tail ornaments in male swallows partially mirrors mite loads, with long-tailed males being more resistant to the effects of mites than shorter-tailed males (Moller 1990b).

METHODS Study Site The study took place in three colonies of 12, 15 and 15 pairs of swallows at Kraghede (57~ 10~ Denmark, from May to August 1988 in an area of ca 15 km 2 open farmland with scattered hedgerows, mixed coniferous plantations, and old elm Ulmus glabra trees. Swallows are abundant in this area, although numbers have decreased since the beginning of the 1970s.

Capture and Marking of Swallows All swallows were caught in mist nets or sweep nets shortly after arrival at the breeding site and marked with an aluminium ring and two coloured plastic rings. I took standard body measurements such as wing length, tail length, tarsus length and body weight.

Manipulation of Mite Loads To avoid transmitting mites from old nests, I removed all nests during autumn 1987 by cutting and scratching them off their place. Nests were removed in plastic bags from the breeding area, and the remaining mud scars of the nests were then brushed with a steel brush to eliminate any mites still present. See Moller (1990a) for further details. Natural levels of mite loads vary in relation to colony size (Moller 1987), but any effects of colony size on mite numbers were controlled by restricting the range of colony sizes from 12 to 15 pairs. I randomly assigned new nests built during the breeding season of 1988 to one of three treatments during the laying of the first clutch. (1) The eggs were temporarily removed and the nest was sprayed for ca l 5 s with a 0.47% pyrethrin solution (Sprayed nests). The eggs were then put back into the nest. (2) The nest was visited and the eggs were temporarily removed and replaced (Control nests). (3) The eggs were temporarily removed, while ca 50 mites were added to the nest (Mite-infected nests). Mites were extracted from old swallow's nests from the previous breeding season. The nests were kept in plastic bags in a house at outdoor temperatures throughout winter. The mites started to move when I touched the plastic bags, and could easily be aggregated in a corner by gently shaking the bag. When approximately 50 mites were in a corner, l placed it above a glass vial and cut it off. I immediately sealed the corner with tape, and collected a new load of mites. Glass vials with mites were kept in a house at outdoor temperatures until they were used in the experiment. I added the content of a glass vial to a nest by gently knocking on its bottom until it was empty. The swallow's eggs were then put back into the nest. I chose 50 mites because that is near the maximum number found on a pair of swallows upon arrival to the breeding sites (see Moller 1990a, in press for further details). I was able to follow 44 males of which 42 later acquired a mate. I followed 13 Sprayed nests, 15 Control nests and 14 Mite-infected nests during the first clutch,

Moiler: Preening and parasites and 10, 7 and 10 of these, respectively, later had a second clutch.

Mite Population Density I estimated the number of mites per nest on the day following offspring fledging by placing my hand on the rim of the nest for 10 s. The number of mites was then scored as either 0, 10, 100, 1000 or 10 000. After estimating the number of mites on my hand, I immediately removed them in order to prevent transfer of mites between nests. These estimates of mite contents of nests were reliable as checked by extraction of mites in Berlese funnels, since the correlation between extracted and estimated numbers was high (r=0"98, N = 4 3 ; see Moiler 1990a, in press, for further data). I estimated the number of mites on adult swallows during the nestling period of first clutches and on first clutch nestlings aged 10-12 days by gently pushing forward the feathers on the head with the tip of a pencil and simultaneously counting the number of mites (Moller, in press). Few mites were obtained during 1984-1987 when I placed each of 20 swallows in a jar of chloroform vapour (Fowler & Cohen 1983), the head of the bird being outside the jar during sampling. Mite abundance estimated from chloroform extractions and from counts of mites on the heads of swallows were strongly positively correlated (r = 0.84, N = 20; MNler, in press). Mites were mostly present on the head (86% of the total number of 148 mites extracted and counted), apparently because swallows cannot easily remove parasites from there (Moller, in press). I repeatedly counted the number of mites on the same individual swallow during successive captures within the same season and in different seasons, and repeatabilities of these mite counts were highly significant (0.90 within years, 0.83 between years, respectively; see Moiler in press for further data).

Preening Activity Swallows preen by using their beak and, in places that otherwise cannot be reached, by scratching with their feet. I thus lump different kinds of comfort behaviour such as scratching and preening with the beak, because they are all supposed to have the same function to reduce ectoparasite loads. Swallows preen all parts of their plumage, but particularly often their wing and tail feathers. Feathers on the head and neck are scratched with the feet. Preening

253

nearly exclusively takes place when swallows are perched, and preening activity thus peaks in the morning and the evening. A preening bout started when an individual started to preen the feathers by using its beak or feet. A number of preening movements through the feathers usually follow in quick succession, often ending with the bird shivering its entire body. A new preening bout usually did not follow for several minutes, and bouts could thus be easily distinguished from each other. Only a very small fraction of preening bouts involved contact with the uropygial gland (3.1%), and this fraction did not vary in relation to mite treatment (for Sprayed, Control and Mite-infected treatments 3.0%, 2-9% and 3"1%, respectively). Uropygial gland secretions are known to have bactericidal and fungicidal properties important in the maintenance of feather condition (Jacob & Ziswiler 1982). Preening bouts always lasted less than 2 rain. I watched all swallows (42 pairs) daily for 1 h throughout the breeding season between sunrise and noon by recording every second minute whether or not they were preening the body and the feathers. Each preening bout therefore resulted in only one record, and scan samples thus result in underestimates of time spent preening (Altmann 1974), although there is no reason to believe that this should result in any bias. Watches at nests of the various treatment groups were randomized with respect to time of day. I could watch up to eight pairs simultaneously since pairs nested close to each other. Daily measures of individual preening rates consisted of the fraction of all observations at intervals of 2 min (a maximum of 30 observations per h, X_+so=22.1+l-9, N=7327 bird hours) during which an individual preened. I measured the preening activity of nestlings from 10 days of age until fledging during 1-h daily observation periods by recording every second minute whether or not any nestling of a brood preened. Since feWer nestlings survived in the group receiving the mite-infected treatment, their preening scores were relatively lower. Mean preening activity was calculated as the average of the daily means for each of seven periods of the breeding season: (1) the premating period during which the male was alone in the territory; (2) the first fertile period which lasted from pairing until the day when the penultimate egg of the first clutch was laid; (3) the first incubation period which lasted from the day when the last egg of the first clutch was laid until all eggs had hatched; (4) the first nestling period which lasted from the first

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Table I. Effect of treatment of swallow nests on mite population levels of nests after fledging of offspring, of adults during rearing of firs( clutch nestlings, and of first clutch nestlings aged 1(~12 days Mite population size (mean _+sE) Clutch

Sprayed

Control

Mites

F

0.14__+0.10" 0.71_+0.36"

0.46__ 0.12b 0.80_+ 0.36a

1.80+ 0.34c 2.00__ 0.37b

8.98** 3.98*

5'9 •

6.4 _ 6.2" 1.3 -I- 1.P

Mites in nests

First Second Mites on adults

Males Females

a

1.1 _+0.8"

12.9 _ 8.7~ 6.9 __+ 5.8b

7-43** 8.61"*

33.7 _+26.2c

18.31"*

Mites on nestlings

2.3 _+2.8a

16,2 •

b

Mite population levels of individual nests were scored as either 0, 1, 2, 3, or 4 which equals 0, 10, 100, 1000, or 10 000 mites in a nest. Mite population levels for adults and nestlings are numbers of mites. Mean values in the same row with different superscripts are significantly different from each other (P < 0.05) in a Scheffe's test. *P<0.05, **P<0.001. day all nestlings of the first brood were present until all nestlings had fledged; (5) the second fertile period which lasted from fledging of the first brood until laying of the penultimate egg of the second clutch; (6) the second incubation period which lasted from laying of the last egg of the second clutch until all eggs had hatched; and (7) the second nestling period which lasted from the first day all nestlings of the second brood had hatched until all had fledged. Similarly, mean preening activity during one reproductive cycle was calculated as the average of the daily means for the cycle.

ing against time. Regression coefficients were used in later analyses of differences in trends between sexes and clutches. Mite scores of nests were transformed from 0, 10, 100, 1000 and 10 000 to 0, 1, 2, 3 and 4 to obtain approximately normal distributions (Kolmogorov-Smirnov test). Mite loads of adults and nestlings were log(X+ 1) transformed before statistical analyses. I compared mean values after one-way A N O V A s using Scheffe's test which controls the experimentwise type I error rate (Day & Quinn 1989). Values given are m e a n + s E unless stated otherwise.

Statistical Procedures

Preening activity was arcsine-transformed to obtain a data set with a normal distribution (Kolmogorov-Smirnov test). The percentage of time spent preening (per period or per clutch) by each individual was used as the independent observation in the analyses, and pseudo-replication was thus avoided. I analysed for effects of mite treatment on preening activity using a repeated measures A N O V A where mite treatment was the classification variable and the mean preening activity during each of the periods of the breeding season was the repeated measures variable. I compared preening activity during first and second clutches and for males and their mates by means of p r o d u c t - m o m e n t correlations and paired t-tests. The change in preening activity during a particular breeding cycle was measured as the regression coefficient of daily preen-

RESULTS Effects of M i t e s

Experimental manipulation of mite loads during the egg laying of the swallow host significantly affected mite loads of nests after fledging of offspring. The difference in mite loads between treatments was significant during both first and second clutches ( F = 8 . 9 8 , df=2,39, P<0-001; F = 3 . 9 8 , df= 2,24, P < 0-05, respectively), despite the fact that mite loads were manipulated only during laying of the first clutch, and that the majority of swallows whose first clutch nests were infected with mites built a new nest for the second clutch at a distance of 1-5 m within the territory (Moller, in press). Mite loads of Sprayed nests were lower than those of Mite-infected nests with Controls in between (Table I). Adult swallows in the Mite-

Moiler: Preening andparasites

255

Table II. Effect of mite treatment of swallow first clutch nests on preening activity of their adult hosts during first clutches and during the entire breeding season for pairs having two clutches Sex

Period

Male

First clutch

Male

Female

Female

First and second clutch

First clutch

First and second clutch

Source Treatment Subjects within groups Repeated measure Treatment x repeated measure Repeated measure x subjects within groups Treatment Subjects within groups Repeated measure Treatment x repeated measure Repeated measure x subjects within groups Treatment Subjects within groups Repeated measure Treatment x repeated measure Repeated measure • subjects within groups Treatment Subjects within groups Repeated measure Treatment x repeated measure Repeated measure x subjects within groups

infected treatment had more mites than adults receiving the Sprayed or the Control treatment (Table I). There were more mites on swallow nestlings from Mite-infected nests than on those from Control nests, which had more mites than had swallows with Sprayed nests (Table I). Preening activity of adult swallows was highly variable (males first clutch: 3-5+0-6%, range 0-14-6, N = 4 2 , second clutch: 1 . 1 _ 0 . 3 % , range 0 5.1, N=27, females first clutch: 1.0+0"3~ range 0-10.6, N = 4 2 , second clutch: 0 . 7 + 0 . 2 % , range 0-3"4, N = 27). The preening activity of adult swallows was not significantly affected by the three treatments (Table II; see Fig. 1 for data). However, the preening activity of individual adult swallows was highly consistent throughout the breeding season as indicated by the highly significant repeated measures term in a repeated measures analysis of variance (Table II; see Fig. 1 for data), some individuals preening a lot and others only very little throughout the breeding season. Preening by nestlings was highly variable (first clutch: 9-7__ 1-2%, range 2.0-32.0, N = 4 2 , second clutch: 10"3 ___1.3%, range 3.0-22'0, N = 27). Preening activity was strongly affected by the treatment

df

SS

F

2 39 3 6

0-03 1.17 0-46 0-05

0.55

117 2 24 6 12

1-35 0'08 0-79 0.70 0-04

144 2 38 2 4

1-53 0-04 0-44 0-13 0.03

76 2 23 5 10

0.32 0-09 0.33 0-20 0.06

115

0-52

13.31 0.69 1.20 10.96 0-29 1.81 15.84 1.46

P 0.58 0-0001 0.66 0.32 0.0001 0-99 0' 18 0.0001 0.22

2.99

0.07

8.70 1.33

0.0001 0.22

of the nests during both first and second clutches ( F = 15-41, df= 2,39, P < 0.0001, F = 5.44, df= 2,24, P < 0 ' 0 2 , respectively). Nestlings in Sprayed nests preened significantly less (3-7 _+0'3%, N = 14) than nestlings in Control nests (9.8 • 1-7%, N = 13) and than nestlings in Mite-infected nests (15-1 • 2.2 %, N = I 5 ) during first clutches (P<0.05, Scheffe's test). Nestlings in Sprayed (7'5 ___1-7%, N = 10) and in Control nests (7.1 +__1-9%, N= 7) preened significantly less than nestlings in Mite-infected nests (15.2+2.1%, N = 1 0 ) during second clutches (P<0"05, Scheffe's test). Preening activity was strongly positively related to the n u m b e r of mites per nest within treatments (Fig. 2), suggesting a causal relationship. Seasonal Differences

There was considerable variation in preening during the breeding cycle with peaks during the fertile and the incubation periods (Fig. 1). Preening activity decreased during the breeding cycle among both males and females (mean regression coefficient for males' first clutch: - 1.59 + 0'38, one-sample ttest, t~=4.22, df=4l, P < 0 . 0 0 1 , males' second

Animal Behaviour, 42, 2

256

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No, of miles Time period Figure 1. Preening activity ( % time spent preening) of

adult swallows ((a) males and (b) females) whose nests

received different parasite treatments during laying of their first clutch in relation to time in their breeding cycle. Values are mean+sD (vertical bars). A Spray; IS], control;

9

Figure 2. Preening activity (% time spent preening) of nestling swallows in relation to experimental treatment of their nests during laying of the first clutch and to a scaled measure of mite loads of nests after fledging for first (a) and second clutches (b). See text for definition of levels of mite loads. A, Spray; [Z, control; (2), mites.

mites.

clutch: - 0 . 5 6 + 0 . 2 3 , ts=2-41, dr=26, P=O.02, females' first clutch: - 0.94 + 0.24, ts = 4.00, df= 41, P
Preening activity during first clutches was significantly higher than during second clutches (males: ts = 5.93, dr= 26, P < 0-001, females: ts = 3.01, df= 26, P = 0 - 0 0 6 ) . Preening decreased more sharply during the breeding cycle of first than second

Moiler." Preening and parasites

257

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Figure 3. Relationship betweenpreening activity (% time spent preening)of t~maleswallowsand their mates during first (a) and second clutches (b). clutches (males: ts = 1.09, df= 26, P = 0'04, females: ts=2.57, df=26, P=0-02). Individual swallows preening a lot during their first clutches also did so during their second clutches (males: r=0-42, t = 2.29, dr= 25, P < 0.05, females: r = 0"64, t =4-13,

df = 25, P
P<0-0001), but not during their second clutches (t~= 1.26, df=26, NS). Both males and their mates preened less with the advancement of the breeding cycle, but the decrease among males was steeper than that among females during first clutches (ts = 2.37, df=41, P=0"02), but not during second clutches (ts = 0.88, df= 26, Ns). Male preening was significantly positively correlated with preening by their mates during both first and second clutches (Fig. 3; first clutch: r=0'69, t=6-06, df=40, P<0"001; second clutch: r=0'69, t=4"71, df=25, P < 0"001, respectively). DISCUSSION

Parasite Loads and Preening Sex Differences Males preened significantly more often than did their mates during their first (t~=7.69, df=41,

Preening has been demonstrated to reduce parasite loads efficiently. Individual debeaked chickens cannot preen efficiently and their parasite loads

258

Animal Behaviour, 42, 2

increase dramatically (Brown 1972). Experimental manipulation of mallophaga loads in chickens clearly increases their grooming activity (Brown 1974), although mallophaga are generally considered to be benign parasites (Marshall 1981). However, they are often vectors of detrimental endoparasites (Marshall 1981). A study of allopreening in penguins demonstrated that unmated individuals, which for that reason could not engage in allo-preening, harbour many more ticks than mated penguins frequently engaging in allopreening (Brooke 1985). However, in my own experimental study, parasite loads of nests and adult swallows did not affect the preening activity of adults, although there was a tendency among females during some periods of the breeding cycle to preen more when nests were infected with mites than when sprayed with a pesticide (Fig. 1). Adult swallows were thus unable to perceive the mite infection rate of conspecifics from their preening behaviour as recorded in this study, although mite loads of experimental nests were kept within the range recorded for unmanipulated nests (Moller 1990a). Since mites have highly detrimental effects on the reproductive success of their swallow hosts (Moller 1990a), it would clearly be beneficial for adult swallows to be able to avoid infections. Since mite populations of nests originate primarily from inoculates derived from adult hosts (Moller 1990a), individual swallows able to discriminate against heavily infected conspecifics on average should leave more or better quality offspring. Higher parasite loads of unmated than mated male swallows and assortative mating for both mite and mallophaga loads (Moller, in press) suggest that swallows, if not through observation of preening activities, are able to estimate the parasite loads of conspecifics. As mites affected the expression of tail ornaments in swallows (Moller 1990b), assessment of parasite loads by females may therefore be indirect through plumage traits, as suggested by Zuk et al. (1990). Nestling swallows differed from adults by preening more with increasing parasite loads of their nests (Fig. 2). At least four explanations may account for this age difference. First, nestlings are confined to the nest and are therefore forced to live with the mites, whereas adults may be able partially to avoid severe parasite infections by visiting their nests infrequently. Second, juvenile animals are often affected more severely by parasites than are adults due to age-related differences in immune defence, hypersensitivity reactions or morphology (Wakelin 1978;

Marshall 1981; Wikel 1982; Baron & Weintraub 1987). Third, efficient preening behaviour may be an ability acquired during ontogeny, and adults may be more experienced at removing parasites than are nestlings. Fourth, nestlings had more parasites than adults, and they should thus preen more frequently. The present experiment was not designed to distinguish between these alternatives. Seasonal Differences

An obvious reason why adult swallows preened more early during the breeding season could be a spring peak in the number of parasites with a subsequent decrease. This is not likely, however, since the prevalence of mites in second clutch nests was higher than that of first clutch nests, whereas their intensity of infection was approximately similar during first and second clutches (Moller 1987). A second alternative is that adult swallows may change their time use priorities during the breeding cycle, and this would affect the proportion of time spent preening (Krebs & McCleery 1984). And, indeed, both in males and females the proportion of time spent preening decreased during the breeding cycle. Adults of both sexes are particularly busy during the rearing of nestlings (Turner 1980), and benefits of preening should therefore be relatively smaller during the nestling period than in earlier parts of the breeding cycle. This is in accordance with the hypothesis that preening activity of hosts is inversely proportional to their time spent on reproduction during different parts of their reproductive cycle. Other seasonal differences in preening activity, e.g. more preening during first than second clutches, are not in agreement with a hypothesis of trade-offs between preening and other activities. A third alternative is that preening activity reflects parasite loads (not necessarily of mites), and that transmission of ectoparasites is more common among males and particularly so during the fertile period and the incubation period. Male swallows, in particular, spend considerable time engaged in extra-pair copulation attempts during these periods (Moller 1985), and may acquire ectoparasites then. Males may also come into contact with conspecifics more often than females during fighting leading to more opportunities for transmission of parasites. Both the breeding cycle and the seasonal patterns of preening are in agreement with the explanation that transmission rate of parasites to males during extra-pair copulations and fights may be higher than among females.

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Moller: Preening and parasites If preening does reflect parasite infestation levels, swallows preening a lot should have more frequent physical contacts with conspecifics than swallows preening less frequently. These individuals may also be of a higher phenotypic quality and therefore more often rear two clutches per season. Swallows that had two clutches preened significantly more often than did swallows with only a single clutch, and the pattern was similar for males and females. An obvious null hypothesis is that individuals of high phenotypic quality are able to forage more efficiently and thus to spend more time preening than other individuals. High quality individuals are also more likely to be double brooded than other conspecifics (e.g. Lack 1966). Sex Differences Some individuals preened a lot throughout the breeding season while others only preened very little. Thus, individuals preening a lot during their first clutches did likewise during their second clutches. If such individualdifferences reflect quality differences (e.g. in terms of frequency of physical contacts with conspecifics and/or resistance or other kinds ofdefence against parasites), one expects that mates should resemble each other with respect to preening activity. This was in fact also observed (Fig. 3). However, a pair also shares a common environment,i.e. the nest site, and this should lead to similarity in parasite infestations and resemblance in preening rate. This seems not to be the entire explanation because preening activity of pair members was also similar during the fertile period of the first clutch before any nest was present (r=0.57, P<0.001). Preening may improve the overall appearance of the plumage of individual swallows (e.g. Simmons 1985), and males should therefore spend relatively more time preening during periods when females choose mates and extra-pair copulation partners. Male swallows with fewer mites grew longer tails during the next moult than did others, and they were therefore preferred as mates to males with high mite loads (Moller 1990b, in press). Males should thus always preen a lot in order to reduce mite loads. Higher male than female preening rates during the fertile periods of both first and second clutches (Fig. 1) and higher preening activity during first than second clutches are in agreement with the hypothesis that preening activity of hosts is higher in the sex being chosen during mate choice.

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