I B I S 1 3 Y : 1 I 5 5 1 2 0 ~~ ~ ~ ~~ ~~

The effect of ectoparasite nest load on the breeding biology of the Penduline Tit Rerniz pendwlinws

A . DAROLOVA', H. HO12 & B. SCHLEICHER2 I lns t i tu te 01 Zoology, Slovak Acaderny of Sciences, Dubravska cesta 9, S K - 8 4 2 06 Bratislava, Slovakia

LKonrad Lorenz Ins t i t u t e for Comparative Ethology, Savoyenstr, l a , A-1 160 Vienna, Austria

In this study we investigated the importance of ectoparasite load in the nest on the breed- ing system of the Penduline Tit Remiz pendulinus, examining the effect of mite abundance in the nest on mate choice, reproductive success and parental effort. The two most common ectoparasites were the Northern Fowl Mite Dermanyssus hirundinis and the Northern Feath- er Mite Ornithonyssus sylviarum. The results show that mite load is important in mate choice but has no adverse effect on reproductive success. The results also indicate that infestation level is related to the quality of the male (mask-width). Parental feeding rate was negatively related to mite load. This relationship indicated that Penduline Tits did not compensate for higher parasite loads by increasing feeding but rather reflected the con- dition of the parent and its investment in self-maintenance behaviour.

Varioub factors influence breeding behaviour and reproduc- tive success. including intra- and interspecific competition, predation and parasitation (Wiens 1989, Meller 1990a,b). In birds, food availability and nest predation have been shown to be the two most important factors influencing re- productive success (Ricklefs 1989, Martin 1993). Relatively few studies deal with the importance of parasitation (Loye & Zuk 1991). There are several levels of bird-parasite in- teraction. Parasites can be important during the mate choice process (Meller 1990a,b, Clayton 1991, Johnson & Boyce 1991) or later on for the determination of the cost of reproduction (e.g. it has been shown that ectoparasite load can influence feeding behaviour of parents) (Hoelzer 1989, Hamilton 1990, Clayton 1991, Mder 1993). They also can influence reproductive success (either chick devel- opment or mortality) (Perrins 1965, Moss & Camin 1970, Moller 1990a,b, 1994, but see Loye & Carroll 1991).

Parasites may play an important role in mate choice be- cause of the direct benefits of choosing a partner with few or no parasites (Clayton 1990, 1991, Hamilton 1990) and the indirect benefits of choosing a mate that signals resis- tance to parasites through the quality of its plumage or display behaviour (Hamilton & Zuk 1982, Read 1988, M011- er 1990a,b, Clayton 1991). Many studies point out that risk of parasitism is related to social life (Hoogland & Sherman 19 76, Freeland 1979, Brown &Brown 1986, Mder 1987, Shields & Crook 1987). Because individuals can also reduce the risk and hazards of heavy parasitism by choosing to reproduce at sites with few or no parasites at all (Brown & Brown 1986, Shields & Crook 1987). this could have strong implications for female mate choice, for instance in a bird species in which the nest site or the nest itself is a part of the male mating display

1 1 5

In the Penduline Tit Rerniz peridulinus, the male builds an elaborate nest that is used to attract females (Schonfeld 1994). Hoi et al. (1994) and Grubbauer and Hoi (1996) showed that the nest plays a major role in the female mate choice process. Females benefit by choosing larger nests be- cause of their better insulation, which results in higher hatching and fledging success. However, the good insulation also creates an ideal environment for the invertebrate fauna found in this type of nest. KriStofZ et al. (1993, 1995) showed that there is a high abundance of arthropod fauna (see MaSan & KriStofik 1995) in Penduline Tit nests. Fur- thermore, there is high variation in ectoparasite load be- tween nests (MaSan & KriStofk 1995). The modified tem- perature conditions also seem to facilitate overwintering by ectoparasites in the nests (KriStofik et al. 1993). The fact that some males reuse material from old nests (Schonfeld 1994) might explain some of the variance in parasite load between nests, but it is likely that this variance is also de- pendent on individual variation of the ectoparasite load (Meller 1993).

Hoi P t al. (1994, 1996) showed that after an initialchoice. there was a high rate of nest desertion by female Penduline Tits prior to or during egg-laying. They suggested that this is partly explained by the female having better options (for instance by remating with males with bigger nests) and by difficulties in assessing the quality of a nest at the moment of the initial choice. However, it is possible that some vari- ation in mate choice and nest desertion might be due to the size of the initial parasite load.

Our study quantified the effect of ectoparasite load in the nest, assuming that this reflected overall mite infestation of adult and nestling Pendnline Tits (Meller 1990b, 1991), on mate choice and subsequently the consequences for repro-

I l i l S 1 1 Y 1 I i l A . I > A H O L O V A . 1 1 . 1 1 0 1 & R . S f ‘ I j I , E I C ’ H E K

ductive success (quality and quantity of young). Further- more, we investigated the relationship between levels of par- asite infestation and food provisioning in this species.

METHODS

Study site

Penduline Tits were studied from 1993 to 1995 in three arcas: a riverine forest area along the Morava (48”16’N, 16”57’E), an area of Lake Neusiedl(47”46’N, 16”48’E) and a pond area in southwest Slovakia (47”56’N, 17”43’E). The riparian forest area is characterized by several species of willows Salix spp., and poplars Populus spp., Reeds Phrug- mites australis and Stinging Nettles Urtica dioica occur only along the river bank. The Lake Neusiedl region is charac- terized mainly by an extended reed belt (1 78 km2) with only a few interspersed poplars, willows and Black Locust trees Robinia pseudoacacia. The pond area has a well-developed reed belt along the pond edge and an extensive wet forest region.

Study species

Wc studied the role of ectoparasites in nests on the breeding biology of Penduline Tits, a 10-g migratory passerine. There is no sexual size dimorphism. but the sexes differ in the extension of the black forehead colouration (Schonfeld 1994). The polygynandrous Penduline Tits have a unipar- ental care system in which mainly the female but sometimes the male cares for the brood (Schonfeld 1994, Valera et al. 1996). The decision as to which parent will take care of the brood is made during the egg-laying period.

A large proportion of the Penduline Tits were mist-netted and individually colour-ringed during the nest-building stage, and others were done later during the incubation or chick-feeding period. To determine whether a male was mat- ed or a nest had been deserted by one or both parents, al- most all nests were visited daily throughout the whole breeding cycle, and the nest contents were checked every 3 to 4 days. Data on reproductive success were recorded dur- ing the course of these regular observations. Feeding rate of the attending parent was recorded for 30-min observa- tion periods, and observations were made between 07.00 and 13.00 h when the chicks were 7 to 1 7 days old.

Morphological measurements were taken whenever the birds were caught. Maslr-length and-width and tarsus- leiigth werc measured with caIipers to the nearest 0.1 mm. Wing-length was measured with a ruler to the nearest 1 mm. All birds were weighed to within 0.1 g. The same mea- surements were taken on nestlings at least once during the nestling period.

Nest collection

Parasites were obtained from Penduline Tit nests. Nests were collected either a few days after the chicks had fledged

(mode, 3 days: range, 0-7 days) or just after nest predation or desertion by both parents. Nest desertion occurred during different phases of the breeding cycle, e.g. during the differ- ent nest-building stages (Schonfeld 1994, Franz 1991), and during the incubation and nestling phases. According to when desertion or predation occurred, we collected nests in the early building phase (termed “basket”). nests in the ad- vanced building phase (termed “pouch”) and “finished” nests. We had deserted nests of all three types, both with and without eggs. Furthermore, we collected nests during incubation (nests that were deserted or whose contents were preyed upon during incubation) and during nestling (if breeding failed or predation occurred during chick feeding).

To examine the effect of parasite load on mate choice, we compared “selected” with “not selected” nests for the three building phases. A nest, and thus a male, was classified as “selected” only if the female started egg-laying.

Nest exchange

When the nestlings were 1 0 to 12 days old, 12 nests were collected and replaced by clean (parasites extracted) nests. Furthermore, 23 nests were exchanged with clean nests on the day of fledging or up to 3 days later to examine whether nestlings were still using them for roosting. Nests were stored in plastic bags until extraction of parasites.

Parasite collection

Parasites were extracted by placing each nest in a Tulgren funnel for 24 to 48 h, depending on the building stage and size of the nest. Parasites were collected and preserved in 70% alcohol. Mites were identified to species, and the nuni- ber of each species was recorded (KriStoMc et al. 1993).

Measuring of mite abundance

The two most important ectoparasite species in Penduline Tits nests are two haematophagous mites, the Northern Feather Mite Dermanyssus hirundinis and the Northern Fowl Mite Ornithonyssus sylviarum (see KriStofik P t al. 1995). In- festation by D. hirundinis was found in 81% of all nests, and 0. sylviarum infestation was found in 58%. Overall, 84% of all individual mites were D. hirundinis, 15% were 0. sylvi- urum and only 0.2% were other species.

Both mite species live on birds and in their nests. The entire life cycle of the mites lasts about 6 days during the bird’s breeding season, and each female produces about 20 eggs per batch. Mites in the nests probably originate pri- marily from propagules introduced by the adult birds and from the use of nest material from the previous year. Be- cause there was a significant and positive relationship be- tween the occurrence of D. hirundinis and 0. syIviurum in each nest (ANCOVA [covariate is area]: F l i l o 6 = 1.65, P < 0.05), individual numbers of the two species were pooled for statistical analysis.

1 9 9 7 EFI’ECTS O F E C T O P A K A S I T E S O N P E N D U L I N E T I T B R E E D I N G 1 1 7

Figure 1. Mvarr number (2s.e.) of mites per nest (D. hirundinis, 0. sylvimwn) lor different nest building phases (“basket”, ”pouch”) and brecdirig stages (rgg-laying + incubation. nestling) and in “old“ nests (nests from the previous breeding season) of Periduiine Tits.

Statistical analyses

Parametric tests were used, and data were log x + 1 trans- formed to meet requirements of normality.

There was a high correlation between the feeding rate by adults and chick age ( r = 0.63, P < 0.02. n = 13) and between feeding rate and brood size (r = 0.70, P < 0.005, n = 13). To examine the relationship between parasite load of the nest and feeding rate, a regression analysis was per- formed with the residual feeding rate corrected for brood size and chick age. For comparisons of parasite load between “selected” and “not selected” nests, an ANCOVA was used to control for the effect of different nest-building and breeding stages. Thc consistency of mite infestation in subsequent

nests of the same male was estimated by means of a re- peatability analysis that quantified the amount of within- male variance relative to the total within- and between-male variance in mite infestation, adjusted for different building stages (Falconer 1981, Lessels & Boag 1987). The repeat- ability measure was seen as an indicator of consistency in infestation of the male and his effect on infestation of the nest. We had too few successive nests to perform a repeat- ability analysis for females.

RESULTS

Seasonal and breeding cycle variation of nest infestation

The load of the haematophagous ectoparasites D. hirundinis and 0. sylvinrum in Penduline Tit nests varied throughout the breeding cycle (ANOVA, F, ,54 = 25.3, P < 0.001, Fig. l), mainly because of the significant increase during the nestling period. However, there was no apparent increase in the number of mites with chick age (r:5= 0.001, n.s., mean number of mitednest 2 s.d. = 320.9 ? 161.9). There was no change in the proportion of adult mites to juveniles, pro- tonyinphs and deutonymphs throughout the different phases (ANOVA, F, , , = 0.87, n.s.) (Table 1). and there was no seasonal trend in mite abundance ( r ig= 0.02, ns.) in nests. However, examination of “old” Penduline Tit nests collected at the onset of the subsequent breeding season (March-April) revealed that the two ectoparasite species were frequent inhabitants (Fig. 1) but that only 255 (23.9%) of 1068 mites overwintering in old Penduline Tit nests were adults.

Table I . Maim rriimbrr fi s.e.) of males, femulcs arid ngmphs (protonymphae arid deutonymphae) of’ D. hirundinis iwd 0. sylvinrum in Rndulini~ Tit nests at dij&wnt nest-building and breeding stages. Perrentages of’ the total for each nrst (in purer1thest.s) and tlw nurnbw o / r7mts (n) Jor each nest-building or breeding stuge are givrn

Basket Pouch Finished Nestlings

D~rrn~~riyssirs Males

Females

Nymphs

01 ~ ~ i t h o n ~ ~ , s . ~ r ~ s Males

Feinales

Nymphs

I 1

0.8 ? 0.6 (17 .3)

2.0 i 1.1 (34.6)

2.8 i 1.2 (48.1)

0 (0)

4.6 2 3.5 (98.5)

0.7 i 0.1 (1.5) 30

2.5 2 1.2 (31.9)

2.5 i 1.2 (31.9)

2.8 ? 1.3 (36.2)

0.2 t 0.1

3.6 i 1.6 (91.5)

0.2 2 0.1

(4.3)

(4.2)

34

5.1 2 1.8 (20.1)

9.2 i 3.7 (36.4)

11.1 i 4.5 (43.5)

0.2 t 0.1

5.6 2 3.2

0.4 2 0.3

(3.4)

(90.3)

(6 .3 )

44

71.9 t 3 1 5 (18.7)

132.1 i- 57.3 (34.4)

179.4 t 75.4 (46.8)

1.0 i 0.6 (6.1)

10.2 2 4.2 (59.6)

5.9 2 5.3 (34.3)

4 7

1 1 x A . 1 ) A K O L O V A . H H O I li 13. S C H L l i L C H E K I B I S 1 1 9

35

30

25 4 v)

' 20 0 ' 5

2 10

-0 W - ._ E

5

0

T I Basket Pouch Finished

Nest stage

Figure 2. l'datioriship hctween mate choice 0 1 female Peiiduline Tits arid the mean number (+s.c.) of U. hir-urrdiriis and 0. q/Ivimwn for "se- lected" ( q x i l bars) and "not selected" llilled bars) nests in the "basket". "pouch" or "linished" stage.

Effect on mating behaviour

Comparison of the number of mites per nest selected by a female and the number per those not selected showed a sig- niticant difference in mite density after controlling for dif- ferent building phases (ANCTJVA. P , = 5.6, P < 0.02; Fig. 2 ) . For all building phases, "not selected" nests (nests with- out eggs) had mite densities some three times higher than densities in nests that successfully attracted a female (nests with eggs).

Effect on reproductive success

We found no relation between the number of nestlings and the number of mites (r:?= 0.005, n.s.). Mite ectoparasites did not affect chick mortality in the Penduline Tit. Tn nests with the highest number of mites (>1000) all chicks sur- vivtd, whereas the mortality rate was actually highest in nests with the lowest infestation rates (x:= 10.7, P < 0.03: Fig. 3 ) , and there was no relation between the number of nests in which chicks died and the number of mites (G, = 7.07, n.s.).

There was no obvious effect of parasite load on chick de- velopment (r ' = 0.03, d.f. = 9, ns.). Chick development was calculated as deviation froin mean mass in grams of a givrn chick age.

Effect on parental behaviour and individual quality

To examine the feeding rate of the attending adult in rela- tion to mite infestation, we used the residual variation of feeding rates, which was not explained by brood size and chick age. and found a significant negative relation ( r , { =

Examining different morphological features, we found a -0.72. P < 0.03).

60

50 m K

0 x U D Q)

3 40

30

D 20 w

10

0 n (100 <200 <500 <800 >I000

Mite load in the nest Figure 3 . load in Penduline Tit nests (ti = 24 cliiclts).

Relative distributicin ( ' X , ) 0 1 dead chicks in relation to mite

negative relation between infestation level of the nest and mask-width of the male (r,7 = -0.33, P < 0.03; Table 2). However, there was no relation between the number of mites in the nest and male mask-length, body-weight or wing-length (Table 2). There was also no relation between the number of mites in the nest and female mask-width, mask-length, body-weight or wing-length (Table 2). Addi- tionally, we found significant repeatability ( K = 0.76. d.f. = 7, 10, P < 0.002) of ectoparasite load in two successive nests with nestlings (of individual males) throughout the breeding season.

DISCUSSION

We examined the different levels of bird-parasite interac- tions in Penduline Tits, and our results indicate a relation between mite load and both mate choice and parental effort. Selected nests had significantly lower parasite loads for a longer time than nests that were never observed to be visited by an interested female. This is a surprising result because

Male Female

r r P II 1' I f

Mask-width -0 .33 c0.03 47 -0.04 n.s. 29 Mask-length -0.26 n.s. 47 -0.07 n.s. 29 Wing-lcngth -0.17 11,s. 22 0.03 n.s. 34 Body-weight -0.08 n.s. 22 -0.08 11s. 34

1 9 9 7 E F F E C T S O F E C T O P A R A S I T E S O N P E N D U L I N E 'TIT B R E B 1 ) I N G 1 1 9

selected nests are nests where the female had already started laying or incubating and later disappeared for whatever rea- son (e.g. predation, better option). Thus, the female could have contributed to an increase in parasite load by trans- ferring mites to the nest. One could also imagine that female activity in the nest, such as egg-laying or incubation, in- creased the temperature in the nests and in turn stimulated mite development. Thus, it would be predicted that a higher mite load would occur in selected nests when nest choice is not related to mite load. The fact that selected nests have significantly lower infestation levels supports the idea that mite infestation is a direct or indirect feature of female mate choice.

The results showed that the variation in mite load was inversely correlated to the mask-width of males but with no other morphological measure of males or females. This is interesting because mask-width is the only sexual dimorphic trait in Penduline Tits (Schonfeld 1994). Grubbauer and Hoi (1996) showed that females chose males with bigger masks and that mask-width expresses age and dominance of a male. It is likely that the male sexual dimorphic trait is an indicator of male quality, which includes the ability to avoid parasites, which in turn could be determined by genetic variation inducing parasite resistance (Hamilton & Zuk 1982, Wakelin & Blackwell 1988). This negative relation between male quality and parasite load in the nest is also supported by the significant repeatability of mite loads in successive nests built by the same male (see also Mdler 1991a). The data of Grubbauer and Hoi (1996) and Hoi et al. (1994) suggest that females choose males according to their nest-building skill and morphological traits and hence, indirectly, parasite loads.

There was no obvious effect of parasite load on repro- ductive success. Neither chick development nor chick mor- tality was related to the parasite load in the nest. The results indicate that in nests with the highest ectoparasite loads, the chicks had higher average weights, whereas in nests where the chicks died, the parasites were less frequent. There was no relation between clutch size and parasite load (but see Merller 1990a, 1991b) nor a confounding effect of the season. Instead of searching for a negative effect of par- asite load, as may be the case in other bird species (Merller 1993, Powlesland 1977), it is suggested that the condition of the nestlings is reflected in the condition (development) of their parasites. In other words, there may be parasite selection for good-quality chicks.

Some authors have not found a negative effect of parasite load on chick development, arguing that parents can com- pensate for this extra cost of blood-sucking parasites by in- creasing feeding (Johnson & Albrecht 1993). There seems to be an extra cost for increased parental care in the Swal- low Hirundo rustica through the prolonged duration of the incubation period with higher parasite loads (Mdler 1993). In contrast, Mdler (1994) showed that feeding rates were higher when there were few ectoparasites, and this result agrees with our findings, namely a negative relation be- tween parasite load and feeding rate. Chicks in nests with

few parasites are fed more food than those in more heavily parasited nests. There are several possible explanations for this result: (1) parents try to avoid the contact with strongly infested nests (Merller 1990b); (2) the parasite load reflects the condition of the chicks, i.e. increased mite load might weaken the chicks and hence influence their begging be- haviour, which could then be reflected in lower feeding rates by the parent; ( 3 ) feeding rates reflect the condition of the parents (quality), which is also reflected in the parasite load of their young: and (4) heavier parasite loads may increase the need for self-maintainance behaviour (e.g. preening, for- aging) and hence decrease the time available for chick feed- ing (Schmid 1985).

The first explanation is unlikely because parasite loads of chicks and adults are similar, and we do not believe that the parents would increase their own load by feeding the chicks more often. The second explanation is also unlikely because we did not find a negative effect on reproductive success. In fact, heavily parasited chicks did relatively better. The third explanation (regarding parental quality) and the fourth (in- creased self-maintainance behaviour) seem to be the most likely explanations.

However, the results are contradictory because on one hand we found that parental feeding rates increase with decreasing mite loads but on the other that chick mortality was higher in nests with lower mite loads. This apparent discrepency might be explained by the fact that chick mor- tality has many causes (e.g. cold stress, infection) and is confounded by a decrease in mite load since weak (dying) chicks are not good hosts for parasites. There are two con- tradictory processes working in this system that might pro- duce such a result. One process is driven by the host, namely to avoid ectoparasites (although the cost of parasites does not seem to be very high in our case), and the second is driven by the interest of the parasite to choose hosts in good condition, or at least the condition of the host may influence the development of the parasites. This process may lead to increased parasite loads in nests with better-quality chicks, thereby devaluing the influence of genetic quality in chicks as a measure of fitness.

We would like to thank J. KriStofik and I! MaSin for analyzing thc mites, J. KriStofik and E Valera Hernandez for field assistance and J. Coulson and S. Kleindorfcr for valuable comments on earlier drafts of this article. This study was funded by grants fram the Austrian Ministry of Sciences (45.265/2-IV/6a/93) and the Buro fur wissenschaftlich-technische Abltorninen des OAD (9).

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