Causes of Hatching Failure in the Pied Flycatcher ’

The Condor98:328-336 0 The CooperOrnithological Society 1996

CAUSES OF HATCHING FAILURE IN THE PIED FLYCATCHER ’

JAIME POTTI AND SANTIAGO MERINO Departamento de Biologia Animal, Universidad de Alcalri de Henares, E-28871, Madrid, Spain, e-mail: [email protected]

Abstract. Correlates of egg hatchability in Pied Flycatchers were investigated during a four year study. Hatchability decreased in small eggs, the effect of egg size being more marked among fertile eggs,than in infertile eggs.There was a significant decreasein egg hatchability with increasingclutch size. Hatching successwas higher for clutcheswith larger eggsand was associatedwith largernumbers of breedingrecruits. However, hatching success was unrelated to female condition during incubation or to clutch initiation date. Hatching failure as a whole, and egg infertility in particular, followed a concave-up trajectory across the laying sequence,indicating an optimum for egg hatchability in intermediate positions of the clutch. No singlecause can explain the relationship of egghatchability to laying order. Although hatching successdid not differ across female or male ages, it was significantly lower in pairs formed by yearling males and older females than in other pair/age combinations. Results are discussedin the light of possibletrade-offs between clutch size and egg size and parental investment theory determining differential effort by males and females depending on their residual reproductive value. Key words: Clutch size; egg size; egg infertility: egg inviability; Ficedula hypoleuca;laying order; parental age.

INTRODUCTION ficiently by incubating parents than small clutch- Hatching failure due to infertility or embryo between clutch size and eggsize (Blackburn 199 1, mortality is a potentially important cause of re- Clutton-Brock 199 1). A larger clutch may entail duced breeding successin birds (Koenig 1982, a reduction in the size of the eggsin the clutch, Ojanen 1983). Aside from failures due to pre- thus decreasing the survival prospects of some dation on incubating parents, common causesof egg(s)in the clutch. hatching failure are inbreeding depression (van Almost all of these effectsmay be confounded Noordwijk and Scharloo 198 1) and environ- by parental, mostly maternal, ageor quality (Nis- mentally-induced stresssuch as bad weather dur- bet 1978, Amundsen and Stokland 1990, Bolton ing the incubation stage(Jarvinen and V&linen 1991, Meathrel et al. 1993, Williams 1994). For 1984) or poor condition of incubating parents, example, in many bird species,egg size, clutch usually females, leading to abandonment of nests size and breeding successincrease with parental (Wiggins et al. 1994). age (Ssether 1990), making the relative contri- Egg size has been shown to be related to nest- butions of different factors difficult to unravel ling growth, fledgling size and survival in many without experimental manipulations. These can avian species,(e.g., Potti and Merino 1994) and provide strong evidence on the nature of the is an important causeof hatching failure (Murton cause-effectrelationship of egg size to offspring et al. 1974). However, in many avian species, fitness by experimentally separating egg size ef- egg size varies in predictable ways in the course fects of parental quality (Amundsen and Stok- of the laying sequence(Clark and Wilson 198 1, land 1990, Reid and Boersma 1990, Bolton 199 1) Slagsvold et al. 1984) and thus the chances of To date, most of the available evidence on survival for individual eggsmay differ depending those interactions derives from studies of pre- on laying order (Rofstad and Sandvik 1985, Spear cocial and semi-precocial species (Williams and Nur 1994). Clutch size may also affect egg 1994). However, there have been few studies hatchability due to physical constraints of in- controlling for confounding factors. While ex- cubation. Large clutches may be covered less ef- perimental manipulations are the most promis- ing means to this end, we have tried to address this goal by expanding the range of factors ex- I Received 18 September 1995. Accepted 26 Feb- amined while statistically controlling for some ruary 1996. of them.

[3W HATCHING FAILURE IN PIED FLYCATCHERS 329

This paper analyzes hatching failures of Pied ure. That is, nestswith hatching failure were those Flycatchers (Ficedula hypoleuca) during a four where at least one egg failed to hatch. year study in central Spain and attempts to dis- Nest box quality was ranked by an index based criminate between failures due to infertility and on the proportion of years occupied assuming those due to embryo death. We address both that in the long term, the most frequently used causes of failure by focusing on differences in nest boxes are of higher quality (Askenmo 1984, basic breeding and individual parameters such Potti and Montalvo 199 la, 199 1b). Original nest as breeding phenology, clutch size, parental age, box quality scoreswere transformed to catego- size, and condition, and relating failures to egg rize boxes as high or low quality (Potti and Me- size and position in the laying sequence. rino 1994). The distribution ofhatching successwas highly METHODS skewedand transformations did not improve the The study was conducted from 1988 to 1991 in fit of data to a normal distribution. We therefore a population breeding in nest boxes in central analyzed hatching successwith nonparametric Spain (see Potti 1993). The area was visited al- statistics when appropriate or as a categorical most daily after the birds’ spring migration ar- variable (henceforth “transformed hatching suc- rival in late April. Nest boxes were checked for cess”)by dividing nestsinto “successful” (all eggs signsof nest building and egglaying and any new hatched) and “unsuccessful” (at least one egg egg was distinctively marked with pencil. Max- failed to hatch). imum length and breadth of all eggsin a clutch To investigate the variation of hatching suc- were measured to the nearest 0.1 mm during cess across parental ages and the possibility of incubation time when females were caught, aged interactions among different combinations of ages as yearling or older (Karlsson et al. 1986) mea- between pair mates, we conducted log-linear suredand released.Egg volume, which is strongly analysis (Sokal and Rohlf 198 1). This procedure correlatedwith fresh eggweight (Potti 1993), was is analogous to an analysis of variance in that calculated from egglength and breadth using the total variance of frequency data is partitioned formula of Hoyt (1979) and a mean egg volume into different factors,making possiblethe testing was calculated for each clutch. Males were caught of interactions between them. We ran the test while feeding nestlings by means of a nest-trap hierarchically beginning with the highest order and were aged following Karlsson et al. (1986) interaction so that dropping a significant (P < and Potti and Montalvo (199 1a). After the cap- 0.05) term would result in a significant lack of ture of adult birds we recordedtarsus length (Pot- fit of the model. Statistical tests are two-tailed. ti and Merino 1994) with dial calipers to the Means are given f 1 SD except otherwise stated. nearest 0.05 mm and body mass to the nearest For simplicity, unstandardized values are pre- 0.1 g. To control for size effects, a “body con- sented in the figures even though statistical tests dition” index was calculated as the residual of were conducted with standardized or trans- within-sex yearly regressionsof mass on cubed formed values. tarsus length (Potti and Merino 1994). We recorded the number of eggs hatched, RESULTS hatching success(eggs hatched/eggs laid x 100) and number of breeding recruits found until 1993 HATCHING SUCCESS (see Potti and Montalvo 199 lb). On day 13 of Excluding one entire infertile clutch of seven eggs nestling age (hatching day = day l), we broke in 1990, overall hatching successwas 92.4 f any unhatched egg in the nest and scored it as 13.7% (n = 289, range 33.3-100%). Hatching either infertile or inviable (containing a clearly successvaried significantly across years (Krus- visible embryo which died before hatching), not- kal-Wallis ANOVA, H = 27.28 P < 0.0001). A ing its position in the laying sequencewhen pos- posteriori comparisons showed that the differ- sible. Eggsscored as infertile contained no more enceswere entirely due to the bad seasonof 1988, than a yellow yolk, while we scored as inviable when rainy and cold spellsduring incubation pre- addled eggswhere the embryo could have died sumably reducedhatching success.We standard- at an early developmental stage. For an overall ized hatching successfor yearly variation by us- analysis of egghatchability, we have lumped to- ing the deviations from the yearly medians in gether infertility and inviability as hatching fail- subsequentanalyses. 330 JAIME POTTI AND SANTIAGO MERINO

83 I 151

3 f

/ I I 3-4 5 6 7-6 Clutch size FIGURE 1. Hatching success(&SE) in relation to clutch size in the Pied Flycatcher. Numbers are sample sizes.

There was a significant decrease of hatching = 280) of the clutches, one or more embryos successwith increasingclutch size (Kruskal-Wal- failed to hatch. Overall, one or more eggsfailed lis ANOVA, H = 12.41, n = 270, P = 0.006; to hatch in 31.1% of the clutches (n = 289). Fig. 1). Hatching successcorrelated positively Confirming the previous analyses,clutches with with mean clutch egg volume (Spearman rank hatching failure were larger than those where all correlation, r, = 0.17, P = 0.007) and with the eggshatched (Table 1). The same is true when number of breeding recruits originating in the the analysis is restricted to clutcheswith at least clutches (Y, = 0.18, n = 270, P = 0.009) sug- one inviable egg (one-way ANOVA, Fl,278 = gesting an association with other fitness factors. 10.49, P = 0.0013) but not for clutches with Hatching successwas unrelated to female con- infertile eggs(F,,2,, = 1.98, P = 0.16). Hatching dition during incubation (r, = 0.04, P = 0.55) or failure was unrelated to laying dates (Table 1). to clutch initiation date (r8 = 0.00, P = 0.96). Average egg size was significantly smaller in Hatching successdid not differ acrossfemale clutches where one or more eggsfailed to hatch or male ages (Mann-Whitney tests, z = 0.92, P (Table 1). Clutches with infertile eggs differed = 0.36 and z = - 1.40, P = 0.31, respectively). significantly from those with all eggsfertile only However, the interaction term male x female in egg length, being shorter (F,,277= 4.23, P = age was significant in a log-linear analysis of 0.041). Egg volume and breadth were signifi- transformed hatching successwith male and fe- cantly smaller in clutches with one or more un- male age (log-likelihood, G = 5.67, df = 1, P = hatched, fertile eggs than in clutches where all 0.017), showing that variation of hatching suc- eggshatched (F,,2,, = 4.10, P = 0.04 and F,,2,, = cesswith female age changed across the age of 6.29, P = 0.01, respectively), while egg length their mates. Hatching successwas significantly did not differ significantly between both types of lower in adult females paired with yearling males clutches(F, 279= 0.46, P = 0.50). However, when than in the rest of pair age combinations (Fig. egg dimensions and volume of infertile and un- 2). hatched eggswere compared with the mean dimensions of fertile or hatched eggsin the same CORRELATES OF HATCHING FAILURE clutch, no significant differences were found In 13.3% (n = 289) of the clutches, one or more (Wilcoxon’s testsfor matched pairs, IZ= 23 pairs eggswere scored as infertile. In at least 20% (n (infertility) and n = 33 pairs (inviability), P > HATCHING FAILURE IN PIED FLYCATCHERS 331

33 47 z 155 I older male yearlingmale older male g 85

! 18 Z I

55’ 1 I I yearling older yearling older Female age FIGURE 2. Interaction between age of male and female parents on hatching successin the Pied Flycatcher (Kruskal-Wallis ANOVA, H = 7.89, P = 0.048). Shown are means +SE. Numbers are sample sizes.

0.20 in all comparisons).In other words, clutches were no associationsbetween frequency ofhatch- with infertile and unhatched eggstend to have ing failure and female age or nest site quality smaller eggsthan clutches where all eggshatch (chi-square tests, both P > 0.20). but, within clutches, neither infertile eggs nor eggsthat fail to hatch can be distinguished by LAYING ORDER AND size from fertile or viable eggs. HATCHING FAILURE Tarsus length, weight, and condition were not Due to small sample sizes of complete laying significantly related to hatching failure (Table l), sequences,the analyses below are restricted to egginfertility or egginviability, either in females clutches of five and six eggs,the most frequent or males (P > 0.10 in all ANOVAs). Also, there clutch sizes in our population (Potti et al. 1987,

TABLE 1. Differences in breeding parameters and parental measurementsbetween clutches where all eggs hatched (“Successful”) and clutcheswhere at least one egg failed to hatch (“Unsuccessful”) in Pied Flycatchers. Shown are means f SD. Differences between groupswere tested with t-tests.

Clutch size 5.8 + 0.77 90 5.5 * 0.74 199 2.95 0.0035 Laying date’ 0.86 + 5.95 0.99 + 5.47 199 0.20 0.8454 Female tarsus 19.652 + 0.572 ;: 19.571 & 0.562 190 1.11 0.2683 Female mass 14.85 f 0.90 82 14.91 ? 0.89 167 0.55 0.5800 Female condition* 0.02 f 0.79 82 -0.03 -e 0.82 167 0.42 0.6718 Egg volume’ 1.57 f 0.12 1.61 f 0.11 199 2.96 0.0034 Egg length4 17.31 + 0.68 ;: 17.51 + 0.66 199 2.36 0.0188 Egg breadth4 13.32 f 0.34 90 13.43 + 0.33 199 2.53 0.0121 Male mass 12.65 f 0.58 72 12.70 + 0.80 152 0.48 0.6334 Male condition2 0.02 + 0.58 70 -0.03 f 0.49 151 0.67 0.4989 ’ Staqdardizedfor yearly vafiation. : Ft;$;ls from the regressmnof masson cubedtarsus length. ’ In mm. JAIME POTTI AND SANTIAGO MERINO

publ.). Although this uncertainty does not affect our conclusions on overall hatching failure, it should be consideredwhen examining correlates of egg infertility or embryo mortality. Unhatched, fertile eggswere more frequent in large clutches.A linear decreaseof hatching successwith increasing clutch size in the Pied Fly- catcher was not observed by Creutz (1955), although reduced hatchability was evident in his study above a threshold clutch size of eight eggs. In our study, reduced hatching successwas entirely due to embryo mortality rather than egg 1 2 3 4 5 6 infertility and thus may reflect a cost, in terms Laylng order of hatching success,of laying larger clutches.Re- FIGURE 3. Frequencies of hatching failure due to duced hatchability in larger clutches might be presumedsterility and embryo mortality in relation to due to the fact that these may be more difficult layingorder and clutchsize in the Pied Flycatcher[clutch sizes 5 (n = 22) and 6 (n = 42) combined]. to cover efficiently by the incubating females, although this explanation does not seem plausible for altricial birds (Klomp 1970). Reduced Potti 1993). We lumped together egg infertility hatchability in large clutches could also reflect and embryo mortality for an overall analysis of the inability of femalesto producean entire batch hatching failure in relation to laying order. of viable, high-quality eggs.That is, large clutch- Grouping together clutches of five and six eggs es may contain one or more low-quality eggsand and lumping positions 5th and 6th in clutchesof this difference might be reflected in some other, six eggs, hatching failure significantly changed more subtle and as yet unknown, aspect of egg with laying order, with more frequent failures in quality (Monaghan et al. 1995). first and, especially, last positions in the laying An alternative hypothesis might be that the sequencexz4 = 21.6, P = 0.0002; Fig. 3). viability of eggsmay decline in larger clutches There was also a similar trend for egginfertility due to the longer time the eggsare exposed to associatedwith laying order, with infertility be- environmental factors before incubation begins ing relatively more common for eggslaid early (Veiga 1992). Furthermore, larger clutches take and late in the laying sequencex24 = 17.4, P < longer to hatch (Moreno and Carlson 1989, Smith 0.002; Fig. 3). An analysis of embryo mortality 1989, Jlrvinen 1990, Veiga and Vifiuela 1993) in relation to laying order did not reach statistical and are energetically more costly to incubate significancexz4 = 8.2, P = 0.08). Contrary to the (Moreno and Carlson 1989, Moreno and Sanz casewith infertility, no clear pattern is apparent 1994). Both these factors could cause energetic in the variation of hatchability with laying order, bottlenecks affecting embryos. except that the last egg seems to have low via- In a study of the related Collared Flycatcher bility (Fig. 3). (Moreno et al. 1991) experimental clutch en- largements led to reduced hatching success. DISCUSSION However, this trend should not be confounded We have shown that hatching failure in the Pied by the effect of female condition as measured in Flycatcher is dependent on at least four different our study, as there is a positive relationship be- factors: the mother’s clutch size, the mean size tween clutch size and both weight and condition of the eggsin the clutch, the position of the eggs in female Pied Flycatchers(Askenmo 1982, Potti in the laying sequence, and the interaction be- and Merino, unpubl.). The absence of any rela- tween the age of male and female parents. A tionship between female condition and egg drawback in the interpretation of our data when hatchability in our population does not imply trying to gain insight into the causesof hatching that parental quality is unimportant, only that failure is that some eggsthat we scored as “in- our index may not reflect relevant aspectsof pa- fertile” could be in fact fertile ones where the rental quality while even it is positively and sig- embryo died at an early stage of development nificantly related to other traits related to paren- (See1 1968; Birkhead, Fletcher and Veiga, un- tal performance such as female persistence at HATCHING FAILURE IN PIED FLYCATCHERS 333 incubation during cold spells(Wiggins et al. 1994) clutch differencesin hatchability related to small and fledgling condition (Potti and Merino, un- differencesin egg size. publ.). There was a clear pattern for hatching failure Our results show that hatching successmay as a whole to follow a concave-uptrajectory across pose a limit to the evolution of clutch size in the laying sequence,with relatively high rates of altricial birds, particularly if there is a trade-off failure in both first and last positionsin the clutch. between eggsize and clutch size (Blackburn 199 1, This indicates an apparent optimum for hatch- Clutton-Brock 199 1, Hillstrom 1992, Potti 1993). ability in intermediate positions of the clutch. Such a trade-off is very difficult to demonstrate This result agrees with those of Creutz (1955) (van Noordwijk and de Jong 1986, Lessellset al. and Ylimaunu and Jarvinen (1987), who found 1989), although some correlative evidence points reducedfledging successfrom first and final eggs. to its existencein the Pied Flycatcher (Hillstrom “Terminal egg neglect” (Evans and Lee 199 1) 1992, Potti 1993). could be invoked to explain the high rate of fail- Small eggs were a second cause of reduced ure in last eggs,as females could “neglect” in- hatchability, especially embryo death. This sup- cubation of last eggsdue to feeding trips for re- ports previous studies demonstrating that nest- cently hatched nestlings, or the embryo devel- ling growth and survival of chicks (e.g., Grant opment could be hampered by the already 199 1) and fledgling size (Potti and Merino 1994) hatched siblings, leading to increased mortality are positively correlated with egg size. Egg size of last eggs.Although this seems a plausible ex- in the Pied Flycatcher seems an a priori good planation for the Pied Flycatcher, where asyn- predictor of the energeticcontent of the yolk and, chronous hatching is common (Slagsvold 1985) especially, of the albumen (Ojanen 1983, Hill- the increase of mortality of embryos in later po- Strom 1992). Hence, embryos in small eggsmay sitions of the laying sequencewas not statistically have died from insufficient reservesto complete significant. Also, early onset of incubation and normal development. Alternatively, small eggs subsequenthatching asynchrony cannot account may cool faster during the periods females are for the high rate of failure of first eggs in the out of the nest, which would impair the embryo clutches. development (O’Connor 1979). The reduced hatchability of early-laid eggs In Pied Flycatchers, egg size increases along could be due to their greater temporal exposure the laying sequence(Potti 1993) and reduced egg to environmental factors (Arnold et al. 1987 for size and subsequentdecreased hatchability could precocial birds; Veiga 1992 and Veiga and Viii- therefore account for the high rates of failure of uela 1993 for the altricial House Sparrow), or to eggslaid early in the sequence.But this cannot the fact that the physiological efficiency of egg be the only causeof reduced hatchability because production may improve along the laying se- we should then also expect higher viability of the quence (Leblanc 1987). larger,last-laid eggs.This was not observed,which In contrast, egginfertility combined with em- may mean that within-clutch variation in eggsize bryo mortality may explain the overall pattern is a poor predictor of egg contents (see Bryant of variation of hatching failure with laying se- 1978). Alternatively, the presumed increase in quence. This relationship is also concave-up and energy contents of eggsis not sufficient to over- can be explained by several complementary hy- come increasesin the mortality rate of last-laid potheses.Leblanc ’s (1987) hypothesis could ac- eggs. count for the high rate of failure early in the The hatching advantage of large eggs in the sequence,but not for failures late in the sequence. population wasnot observedwithin clutches.This Reserve depletion, i.e., decreasedquantityiqual- could be taken as evidence that egg size itself ity of albumen and yolk reserves, may be in- might not be related to hatchability and a third, voked for explaining failures late in the laying unknown variable should be responsiblefor both sequence.The increaseof eggweight and volume small eggsand low hatchability. However, the acrossthe laying sequencein the Pied Flycatcher apparent inconsistency may be due to low sta- (Potti 1993) apparentlycontradicts this latter idea: tistical power of our tests.This is becausea large larger eggsare more likely to hatch, as shown by percentage of variation in egg size, around 60- our between-clutch analyses of hatchability (but 70%, is explained by differencesbetween females see above). (Potti 1993), making it difficult to detect within- Finally, we speculate that reduced fertility of 334 JAIME POTTI AND SANTIAGO MERINO eggslaid late in the laying sequencemay be ex- Flycatcher Ficedula albicollis, who found that plained by reduced sperm and ova viability, or yearling males put less effort on brood rearing by sperm depletion (Birkhead and Moller 1992: when they were paired to older females because 19 1). Although there are no published data on they were capitalizing on the terminal effort of this relationship for any bird species(Birkhead “senescent” females. Thus, reduced hatchability and Moller 1992), both processesare possible in in these nests in our study may have been due the Pied Flycatcher, where females may store to reduced males’ help to their females e.g., dur- sperm in their utero-vaginal junction, opening ing incubation feeding (Lifjeld and Slagsvold the possibility of reducedviability of sperm stored 1986), thus forcing their mates to more frequent- for longer time, and males engage in extra-pair ly abandon incubation duties to forage. copulations (Lundberg and Alatalo 1992), which This study points out that future work on the could deplete sperm reserves (Birkhead and relationship of egg size to both parental and off- Moller 1992). In summary, no single cause can spring fitnessesin altricial birds should expand explain the curve of hatchability acrossthe laying the range of traits usually consideredto affect egg sequence, and we believe that several different viability. In particular, while it is clear that both phenomena in conjunction may explain it. eggsize and laying order are important for hatch- In an across-speciesanalysis of hatchability in ing success,more work is necessaryto disentan- birds revealing the role of various ecologicaland gle the complex interplay between these factors. social factors on egghatchability, Koenig (1982) This task will probably be difficult until non- was unable to find significant effects of egg size destructive methods for ascertaining egg quality or clutch size, but found evidence suggestingthat are developed. breeding date and female age could be involved in the hatchability of eggsin at least some bird ACKNOWLEDGMENTS species. In fact, both breeding date (Bird and This paperwas written while JP spenta sabbaticalleave Lague 1982) and parental age or quality have in the Department of Evolutionary Ecologyat the Mu- been found to affect hatchability of eggsin some seo National de Ciencias Naturales de Madrid. JP is intraspecific studies of birds (Reid and Boersma indebted to A. Barbosa,L. M. Carrascal,M. Gomen- dio, E. Minguez, E. Moreno, J. Moreno, A. Salvador, 1990, Williams et al. 1993). M. Teiedo. J. P. Veiaa and the rest of ecolodsts at the Among birds in general, breeding successis Muse; for’hospitalit;, ideas, and fun. L. MrCarrascal higher in adult than in yearling birds (Sather and J. Moreno deservespecial thanks for providing an 1990). In this study, there were significant effects stimulating working environment and for helping in many ways. We thank L. M. Carrascal,J. Moreno, T. of parental age on hatching successbut not as Slagsvold,J. P. Veiga and the refereesfor reading and expected,as the nests of some older females had suggestingmany improvements to earlier drafts of the significantly lower hatchability than those of paper. The study was supportedby the Spanish DGI- younger females. In fact, S&her (1990) found CYT (projects PB86-0006X02-02 and PB9 1-0084- that, among the reproductive traits he examined co3-03). in a review of age-specificvariation of breeding successin birds, hatchability showedthe smallest LITERATURE CITED differences between juveniles and adults, with AMUNDSEN, T., AND J. N. STOKLAND.1990. Egg size 37% of species(n = 19 species)showing lower and parental quality affect nestling growth in the hatching successin adult than in yearling fe- shag.Auk 107:401-413. males. ARNOLD,T. W., F. C. ROWER,AND T. ARMSTRONG. 1987. Eggviability, nest predation, and the adap- Our study is one of the first demonstrating a tive significance of clutch size in prairie ducks. significant interaction between the age of male Am. Nat. 130:643-653. and female parents on hatching success,so that ASKENMO,C.E.H. 1982. Clutch size flexibility in the older females paired to yearling males had re- Pied Flycatcher,Ficedula hypoleuca. Ardea 70:189- 196. duced hatchability. This result may be inter- ASKENMO,C.E.H. 1984. Polygyny and nest site se- preted in light of some models of parental in- lection in Pied Flycatcher. Anim. Behav. 32:972- vestment predicting decreasedreproductive ef- 980. fort by one parent when the other sex increases BIRD, D. M., AND P. C. LAG& 1982. Fertility, egg its effort (reviewed in Clutton-Brock 199 1). Con- weight loss, hatchability, and fledging successin replacement clutches of captive American Kes- sistent with this model are the findings of Part trels. Can. J. Zool. 60:80-88. et al. (1992) working with the related Collared BIRKHEAD,T. R., AND A. P. MILLER. 1992. Sperm HATCHING FAILURE IN PIED FLYCATCHERS 335

competition m birds: evolutionary causesand con- LUNDBERG,A., AND R. V. ALATALO. 1992. The Pied sequences.Academic Press, London. Flycatcher. T&A D Poyser, London. BLACKBURN,T. 199 1. An interspecific relationship MEATHREL,C. E., J. S. BRADLEY,R. D. WOOLLER,AND between ege.size and clutch size in birds. Auk 108: I. J. SKIRA. 1993. The effect ofnarental condition 973-917. -- on egg-sizeand reproductivesuccess in Short-tailed BOLTON,M. 1991. Determinants of chick survival in Shearwaters Pufinus tenuirostris.Oecologia 93: the Lesser Black-backed Gull: relative contribu- 162-164. tions of egg size and parental quality. J. Anim. MONAGHAN,P., M. BOLTON,AND D. C. HOUSTON. Ecol. 60:949-960. 1995. Egg production constraints and the evo- BRYANT,D. M. 1978. Establishment of weight hi- lution of avian clutch size. Proc. R. Sot. London erarchiesin the broods of House Martins Delichon B. 259:189-191. urbica. Ibis 120:16-26. MORENO,J., ANDA. CARLSON.1989. Clutch size and CLARK,A. B., ANDD. S. WILSON. 1981. Avian breed- the costs of incubation in the Pied Flycatcher Fi- ing adaptations: hatching asynchrony, brood re- cedula hypoleuca.Omis Stand. 20: 123-128. duction, and nest failure. Quart. Rev. Biol. 56: MORENO,J., AND J. J. SANZ. 1994. The relationship 253-277. between the energyexpenditure during incubation CLUT~ON-BRINK,T. 1991. The evolution of parental and clutch size in the Pied Flycatcher Ficedula care. Princeton Univ. Press, Princeton, NJ. hypoleuca.J. Avian Biol. 25:125-130. CREUTZ.G. 1955. Der Trauerschnaooer(Muscicava MORENO,J., L. GUSTAFSSON,A. CARLSON,AND T. P.&RT. hy&euca)-eine Populationsstudie.J. Ornithbl. 1991. The costsof incubation in relation to clutch 96~241-285. size in the Collared Flycatcher Ficedula albicollis. EVANS,R. M., AND S. C. LEE. 1991. Terminal-egg Ibis 133:186-193. neglect:brood reduction strategyor cost of asyn- MURTON,R. K., N. G. WESTWOOD,AND A. J. ISAACSON. chronoushatching. Acta XX Congr.Int. Om. 1734- 1974. Factors affecting egg-weight, body-weight 1740. and moult of of the Wood-pigeon Columba pal- GRANT,M. C. 1991. Relationships between eggsize, umbus.Ibis 116:52-73. chick size at hatching, and chick survival in the NISBET,I.C.T. 1978. Dependence of fledging success Whimbrel, Numeniusphaeopus. Ibis 133:127-l 33. on egg-size, parental performance and egg com- HILLS-~R~~M,L. 1992. Patterns of hatching and adult position among Common and Roseate Terns, body mass changein the Pied FlycatcherFicedula sterna hirundoand S. dougallii. Ibis 120:207-2 15. hypoleuca; adaptations and constraints. Comp. O’CONNOR. R. .I. 1979. Eee weights and brood re- Summ. Uppsala Diss. Fat. Sci. 384: l-37. ductioh in the EuropeanSwift &pus apus).Condor HOYT, D. F. 1979. Practical methods of estimating 81:133-145. volume and fresh weight of bird eggs.Auk 96:73- OJANEN,M. 1983. Significance of variation in egg 77. traits in birds, with specialreference to passerines. JKRVINEN,A. 1990. Incubation and nestling periods Acta Univ. 0~1. A 154. 1983. Biol. 20. in hole-nestingpasserines in Finnish Lapland. Or- P;~RT,T., L. GUSTAFSSON,AND J. MORENO. 1992. nis Fennica 67165-72. “Terminal investment” and a sexual conflict in J;~RVINEN,A., AND R. A. V,&IS.&NEN.1983. Egg size the Collared Flycatcher (Ficedula albicollis).Am. and related reproductive traits in a southern pas- Nat. 140:868-882. serine Ficedula hypoleucabreeding in an extreme Porr~, J. 1993. Environmental, ontogeneticand ge- northern environment. Omis Stand. 14:253-262. netic variation in eggsize ofPied Flycatchers.Can. J. Zool. 71:1534-1542. JKRVINEN,A., AND R. A. V.&IS&TEN. 1984. Repro- POTTI. J., AND S. MERINO. 1994. Heritability esti- duction of Pied Flycatchers (Ficedula hypoleuca) mates and maternal effectson tarsuslength in Pied in good and bad breeding seasonsin a northern Flycatchers, Ficedula hypoleuca. Oecologia 100: marginal area. Auk 101:439-450. 331-338. KARLSSON,L., K. PERSSON,AND G. WALINDER. 1986. Porr~, J., AND S. MONTALVO. 1991a. Male arrival Ageing and sexing in Pied Flycatchers Ficedula and female mate choice in Pied Flycatchers Fi- hypoleuca(In Swedish, with English summary). cedula hypoleucain central Spain. Omis Stand. Var Fagelvlrld 45:131-146. 22145-54. CLOMP, H. 1970. The determination of clutch-size Porr~, J., ANDS. MONTALVO. 1991 b. Return rate, age in birds. Ardea 58:1-124. at first breeding and natal dispersal of Pied Fly- KOENIG,W. D. 1982. Ecological and social factors catchersFicedula hypoleucain Central Spain. Ar- affecting hatchability of eggs.Auk 99~526-536. dea 79:449-458. LEBLANC,Y. 1987. Intraclutch variation in egg size POTTI,J., F. J. SANCHEZ-AGUADO,D. BLANCO,AND S. of Canada Geese. Can. J. Zool. 65:3044-3047. MONTALVO. 1987. Breeding data for a popula- LESSELIS,C. M., F. COOKE,AND R. F. ROCKWELL.1989. tion of Pied Flycatchers (Ficedula hypoleuca)in Is there a trade-off between eggweight and clutch central Spain. Ardeola 34: 105-l 10. size in wild Lesser Snow Geese (Anser c. caeru- REID, W. V., AND P. D. BOERSMA. 1990. Parental lescens).J. Evol. Biol. 2:451-412. quality and selectionon egg-sizein the Magellanic LIFJELD,J. T., ANDT. SLAGSVOLD.1986. The function Penguin. Evolution 44: 1780-1786. of courtshipfeeding during incubation in the Pied ROFSTAD,G., ANDJ. SANDVIK. 1985. Variation in egg Flycatcher Ficedula hypoleuca.Anim. Behav. 34: size of the Hooded Crow Corvus corone cornix. 1441-1453. Omis Stand. 16:38-44. 336 JAIME POTTI AND SANTIAGO MERINO

SCHIFFERLI,L. 1973. The effect of egg weight on the VAN N~ORD~LIK,A., AND G. DE JONG. 1986. Acqui- subsequentgrowth of nestling Great Tits Parus sition and allocation of resources:their influence major. Ibis 115549-558. on variation in life history tactics. Am. Nat. 128: SEEL,D. C. 1968. Clutch-size, incubation and hatch- 137-142. ing successin the House Sparrow and Tree Spar- VEIGA,J. P. 1992. Hatching asynchronyin the House row Passer spp. at Oxford. Ibis 110:270-282. Sparrow:a test of the egg-viabilityhypothesis. Am. S~~GSVOLD,T. 1985. Asynchronoushatching in pas- Nat. 139~669-675. serine birds: influences of hatching failure and VEIGA,J. P., AND J. V~~UELA. 1993. Hatching asyn- brood reduction. Omis Stand. 16:81-87. chrony and hatching successin the House Spar- SLAGSVOLD,T., J. SANDVIK, G. ROFSTAD,ii. LOR- row: evidence for the eggviability hypothesis.Or- ENTSEN, AND M. HUSBY. 1984. On the adaptive nis Stand. 241237-242. value of intra-clutch egg size variation in birds. WIGGINS,D. A., T. PXRT, ANDL. GUSTAFSSON.1994. Auk 101:685-697. -- Correlates of clutch desertion by female Collared SMITH. H. G. 1989. Lamer clutches take lonaer to Flvcatchers Ficedula albicollis.J. Avian Biol. 25: incubate. Omis Stand: 20: 156-l 58. - 93-97. SOKAL,R. R., ANDF. J. ROHLF. 1981. Biometry. 2nd WILLIAMS,T. D. 1994. Intraespecificvariation in egg ed. Freeman, San Francisco. size and eaa comnosition in birds: effects on off- SPEAR,L., AND N. NUR. 1994. Brood size, hatching spring fit&. Bidl. Rev. 68:35-59. order and hatchingdate: effectson four life-history WILLIAMS,T. D., D. B. LANK, F. COOKE,AND R. F. stages from hatching to recruitment in Western ROCKWELL.1993. Fitness consequencesof egg- Gulls. J. Anim. Ecol. 63:283-298. size variation in the LesserSnow Goose.Oecologia S;~THER,B.-E. 1990. Age-specificvariation in repro- 961331-338. ductive oerformance of birds. Current Ornithol. YLIMAUNU.J.. ANDA. JKRVINEN. 1987. Do Pied Flv- 7:251-283. catcherskicedula hypoleucahave a brood-survival VAN NOORDWLTK,A., AND W. SCHARLOO.1981. In- or a brood-reduction strategy?Omis Fennica 64: breeding in an island population of the Great Tit. 10-15. Evolution 35:674-688.