Climate change and micro-geographic variation in laying date

Climate change has been shown to affect the timing of reproduction, with earlier reproduction being associated with an increase in temperature. Changes in the timing of reproduction arise from changes in food availability as well as other factors, and differences in the timing of reproduction among sites may cause sites with early reproduction to contribute disproportionately to local recruitment. In this study, spatial variation in the laying date of barn swallows Hirundo rustica at 39 sites in a 45-km²study area during the period 1971–2004 was used to investigate micro-geographic patterns in the timing of breeding. I found that individuals breeding at sites with early reproduction had a disproportionately large reproductive success. Early sites were characterized by early plant phenology, as determined by the date of leafing of the broad-leaved elm Ulmus glabra and date of flowering of the snowdrop Galanthus nivalis during a single year. Such early sites showed greater advancement in laying date between 1971 and 2004 than the average site. Early sites were also generally occupied during more years by a larger number of breeders than were late sites. Breeders at early sites produced more fledglings, and breeders at such sites were characterized by a smaller adult body size and larger secondary sexual characters than individuals at the average site. These observations are consistent with the hypothesis that temporal changes in the timing of reproduction occur as a consequence of differential recruitment at phenologically early sites that produce disproportionately large numbers of offspring. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Mating systems,philopatry and dispersal in birds and mammals

Many species of birds and mammals are faithful to their natal and breeding site or group. In most of them one sex is more philopatric than the other. In birds it is usually females which disperse more than males; in mammals it is usually males which disperse more than females. Reproductive enhancement through increased access to mates or resources and the avoidance of inbreeding are important in promoting sex differences in dispersal. It is argued that the direction of the sex bias is a consequence of the type of mating system. Philopatry will favour the evolution of cooperative traits between members of the sedentary sex. Disruptive acts will be a feature of dispersers.     

Calcium transport in strongly calcifying laying birds: Mechanisms and regulation

Birds that lay long clutches (series of eggs laid sequentially before a “pause day”), among them the high-producing, strongly-calcifying Gallus gallus domesticus (domestic hen) and Coturnix coturnix japonica (Japanese quail), transfer about 10% of their total body calcium daily. They appear, therefore, to be the most efficient calcium-transporters among vertebrates. Such intensive transport imposes severe demands on ionic calcium (Ca²⁺) homeostasis, and activates at least two extremely effective mechanisms for Ca²⁺ transfer from food and bone to the eggshell. This review focuses on the development, action and regulation of the mechanisms associated with paracellular and transcellular Ca²⁺ transport in the intestine and the eggshell gland (ESG); it also considers some of the proteins (calbindin, Ca²⁺ATPase, Na⁺/Ca²⁺ exchange, epithelial calcium channels (TRPVs), osteopontin and carbonic anhydrase (CA) associated with this phenomenon. Calbindins are discussed in some detail, as they appear to be a major component of the transcellular transport system, and as only they have been studied extensively in birds. The review aims to gather old and new knowledge, which could form a conceptual basis, albeit not a completely accepted one, for our understanding of the mechanisms associated with this phenomenon. In the intestine, the transcellular pathway appears to compensate for low Ca²⁺ intake, but in birds fed adequate calcium the major drive for calcium absorption remains the electrochemical potential difference (ECPD) that facilitates paracellular transport. However, the mechanisms involved in Ca²⁺ transport into the ESG lumen are not yet established. In the ESG, the presence of Ca²⁺-ATPase and calbindin—two components of the transcellular transport pathway—and the apparently uphill transport of Ca²⁺ support the idea that Ca²⁺ is transported via the transcellular pathway. However, the positive (plasma with respect to mucosa) electrical potential difference (EPD) in the ESG, among other findings, indicates that there may be major alternative or complementary paracellular passive transport pathways. The available evidence hints that the flow from the gut to the ESG, which occurs during a relatively short period (11 to 14 h out the 24- to 25.5-h egg cycle), is primarily driven by carbonic anhydrase (CA) activity in the ESG, which results in high HCO₃^? content that, in turn, “sucks out” Ca²⁺ from the intestinal lumen via the blood and ESG cells, and deposits it in the shell crystals. The increased CA activity appears to be dependent on energy input, whereas it seems most likely that the Ca²⁺ movement is secondary, that it utilizes passive paracellular routes that fluctuate in accordance with the appearance of the energy-dependent CA activity, and that the level of Ca²⁺ movement mimics that of the CA activity. The on-off signals for the overall phenomenon have not yet been identified. They appear to be associated with the circadian cycle of gonadal hormones, coupled with the egg cycle: it is most likely that progesterone acts as the “off” signal, and that the “on” signal is provided by the combined effect of an as-yet undefined endocrine factor associated with ovulation and with the mechanical strain that results from “egg white” formation and “plumping”. This strain may initially trigger the formation of the mammillae and the seeding of shell calcium crystals in the isthmus, and thereafter initiate the formation of the shell in the ESG.     

Calcium homeostasis and vitamin D metabolism and expression in strongly calcifying laying birds

Egg laying and shell calcification impose severe extra demands on ionic calcium (Ca2+) homeostasis; especially in birds characterized by their long clutches (series of eggs laid sequentially before a "pause day"). These demands induce vitamin D metabolism and expression. The metabolism of vitamin D is also altered indirectly, by other processes associated with increased demands for calcium, such as growth, bone formation and egg production. A series of intestinal, renal or bone proteins are consequently expressed in the target organs via mechanisms involving a vitamin D receptor. Some of these proteins (carbonic anhydrase, calbindin and calcium-ATPase) are also found in the uterus (eggshell gland) or are believed to be involved in calcium transport in the intestine or kidney (calcium channels). The present review deals with vitamin D metabolism and the expression of the above-mentioned proteins in birds, with special attention to the strongly calcifying laying bird.     

Determining Great Bittern Botaurus stellaris laying date from egg and chick biometrics

Capsule Great Bittern breeding phenology can be estimated from egg and chick biometrics.

Aims To estimate egg or chick ages in order to back-calculate egg-laying dates.

Methods Bittern nests were searched for in six French and three Belarussian sites between 1999 and 2004. Eggs and chicks were measured at each visit. By using a subsample of nests with known egg-laying (or hatching) dates, regression equations are determined using egg density and tarsus length in order to estimate, respectively, egg and chick ages. Additionally in Belarus, the ‘water test’ was used to estimate the incubation stage of the clutch.

Results A total of 141 Bittern nests were found. Egg density decreased linearly from 1.063 at laying to 0.915 the day before hatching. A regression equation therefore allows estimation of egg age from its density. A scale was also constructed to estimate egg age from its position in water, and the accuracy of the two methods is compared. Chick growth rates were similar between the two countries. Before the age of 25 days, chicks are best aged by tarsus length compared to other measurements (weight, bill length). No data were available after that age because chicks were no longer found on nests.

Conclusions Egg-laying date can be estimated to within ±3 days using egg density, and to within ±5 days, using the ‘water test’. Tarsus length can be used until the age of 25 days to age chicks to within ±2 days. These simple measurements provide efficient and accurate methods to record the breeding calendar of this endangered species.     

Rapid laying by Brown-headed Cowbirds Molothrus ater and other parasitic birds

We compared the length of time parasitic and nonparasitic female birds spent on nests while laying eggs (laying bouts) to evaluate the hypothesis that rapid laving by parasitic Brown-headed Cowbirds Molothrus ater and other parasitic birds is a specialization for brood parasitism. Brown-headed Cowbirds typically spent less than 1 min on host nests while laying (41.0 ± 4.58 [mean ± s.e.] s, n = 21). In contrast, mean laving bouts of six nonparasitic icterine species ranged from 21.5 min to 53.4 min, and laying bouts of 13 other passerine species ranged from 20.7 min to 103.7 min. By spending only a few seconds on the nest while laying, brood parasites probably increase their chances of parasitizing nests unnoticed by hosts or, if noticed, are harassed by hosts for less time. Rapid laying may be adaptive if aggression by hosts can thwart attempted parasitism by chasing away the parasite, preventing the parasite from entering the nest or injuring the parasite. Rapid laying may increase the likelihood that the parasitic egg will be accepted. We tested some of these hypotheses by recording the responses of three frequently parasitized species to a stuffed female cowbird placed on their nests for 1 min. All species attacked the model vigorously; however, the mean time for discovery of the model ranged from 3 min to 17 min, ample time for female cowbirds to parasitize the nests. We concluded that rapid laying by parasitic birds is an adaptation for parasitism and, in Brown-headed Cowbirds, reduces the chances that the parasite will be attacked by hosts.     

Rapidly advancing laying date in a seabird and the changing advantage of early reproduction

1. Bird ringing schemes have collected immense amounts of data on timing of breeding for over 100 years. These data provide an unexploited source of information on temporal change in breeding date. 2. We investigated changes in breeding date of the Arctic tern Sterna paradisaea Pont. in Denmark during 1929-98, using information on ringing date of young. 3. Mean ringing date advanced by over 18 days during 70 years, while there was no temporal change in variance in date. 4. Advanced mean ringing date was explained by an increase in mean temperature during April and May and an increase in North Atlantic Oscillation (NAO) index for May. 5. Variance in ringing date increased in years with high temperatures in April and high NAO index values in April. 6. There was changing temporal patterns of selection for early breeding as reflected by analyses of the difference in mean ringing date for Arctic tern young that were subsequently recorded as survivors and mean ringing date for all young. The intensity of selection on breeding date changed from favouring late breeding in the 1930s to favouring early breeding during the 1990s. 7. Analyses of bird ringing information for millions of offspring of hundreds of bird species deposited in national ringing schemes may provide unlimited access to long-term time series of reproductive variables.     

The effect of food on laying date and clutch-size in Tengmalm's Owl Aegolius funereus

The breeding of Tengmalm's Owl Aegolius funereus was studied at Umeå, Sweden, during the 1984–85. Mean clutch-size was one egg larger in 1984 than in 1985 despite the later laying in 1984. The difference in clutch-size was related to a better food supply in 1984. Daily weight increase of females during the prelaying period showed a high negative correlation with laying date in 1985, and a high positive correlation with clutch-size independently of laying date in 1984–85. This suggested that food eaten before and during laying had a great and direct influence on both laying date and clutch-size. Many females increased in weight during laying and most others decreased only moderately (relative to egg weight), suggesting that body reserves were not a main source for egg production.
Late breeding females were provided with extra food during the prelaying and laying periods in 1985. Fed females weighed more, bred eight days earlier and laid one more egg than controls. At the same laying dates in mid season, and after heavy snow-fall, clutch-size and female weight were larger in the fed birds than in controls, but this was not so near the end of the laying season. Although the earliest of the fed late breeders weighed more, and probably were less restricted by food availability just before or during laying, they did not lay more eggs than did early breeders. This result suggested some limitation on clutch-size that could not be overcome by the supplementary feeding. Weights of females during laying did not show any consistent relationship with clutch-size during successive laying date intervals, suggesting that clutch-size was not directly related to body condition.     

Body size and determinants of laying date variation in the Snow Petrel Pagodroma nivea

We studied several determinants of laying date variation and the relationship between laying date and reproductive success in the Snow Petrel Pagodroma nivea . The effects of female body size and condition, year, individual laying period, colony size, mate fidelity, previous reproductive success, and duration of the pre-laying exodus on laying date, were investigated during a 3-year study. The average laying date was 4 December. The laying period was compressed into 10–16 days and was very constant from year to year, both for the population as a whole and for individual females. The laying period of individual females varied from year to year on average by less than one day. Body size explained 24% of the variation in laying dates, with large females laying their egg later than small ones. Laying in large colonies occurred c. 2 days later than in small colonies, mainly because a higher proportion of large females bred in large colonies. There was no effect of mate fidelity, age, body condition and previous reproductive success on laying date, but the duration of the pre-laying exodus was strongly correlated with laying date. Smaller females had shorter pre-laying exodus (c. 17.7 days) than larger ones (c. 20.4 days). During the three years of the study reproductive success either increased, decreased or did not vary with laying date. Although body size is not maintained by selection on laying date alone, the genetic body size component of this species suggests that balancing selection on body size may act through laying date.     

Factors determining the laying date of the Waved Albatross Diomedea irrorata

The Waved Albatross laying period is between mid-April and the end of June. This paper investigates the factors determining when, during this period, a female lays. It is shown that birds breeding for the first time lay relatively late. For older birds, the laying date depends on date and outcome of the previous year's attempt: females that bred successfully in the previous year lay slightly later than in that year, while birds that failed lay earlier. A corresponding difference exists in the dates of arrival at the breeding grounds of successful and failed males. It is argued that one calendar year is not quite sufficient for pairs that have reared a chick successfully to regain breeding condition, while failed breeders can choose the laying date more freely.
Under catastrophic El Niño weather conditions in 1983, all albatrosses arrived late at the breeding grounds, but still the birds that had failed in 1982 were clearly earlier than those that had reared a chick.     

Mating system and brain size in bats

The contribution of sexual selection to brain evolution has been little investigated. Through comparative analyses of bats, we show that multiple mating by males, in the absence of multiple mating by females, has no evolutionary impact on relative brain dimension. In contrast, bat species with promiscuous females have relatively smaller brains than do species with females exhibiting mate fidelity. This pattern may be a consequence of the demonstrated negative evolutionary relationship between investment in testes and investment in brains, both metabolically expensive tissues. These results have implications for understanding the correlated evolution of brains, behaviour and extravagant sexually selected traits.     

Nest-building activity and laying date influence female reproductive investment in magpies: an experimental study

Nest size or nest-building activity has recently been hypothesized to be a postmating sexually selected signal in monogamous birds: females may assess a male's parental quality and willingness to invest in reproduction by his participation in nest building. Females may thus adjust their reproductive effort (i.e. clutch size) not only to their own abilities but also to those of their mates. We investigated whether female magpies, Pica pica, use nest-building activity rather than nest size to adjust their reproductive effort during replacement breeding attempts. After we removed their first clutch, high-quality pairs that built a large nest for the first clutch were more capable of building a replacement nest and females adjusted their clutch size in relation to the time it took to build the nest rather than nest size. We also found support for the hypothesized trade-off between clutch size and egg size in magpies. In replacement clutches females decreased clutch size and increased egg volume, thereby probably improving the survival probability of their offspring in less favourable conditions.Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

A matter of timing: changes in the first date of arrival and last date of departure of Australian migratory birds

Although there is substantial evidence that Northern Hemisphere species have responded to climatic change over the last few decades, there is little documented evidence that Southern Hemisphere species have responded in the same way. Here, we report that Australian migratory birds have undergone changes in the first arrival date (FAD) and last date of departure (LDD) of a similar magnitude as species from the Northern Hemisphere. We compiled data on arrival and departure of migratory birds in south‐east Australia since 1960 from the published literature, Bird Observer Reports, and personal observations from bird watchers. Data on the FAD for 24 species and the LDD for 12 species were analyzed. Sixteen species were short‐ to middle‐distance species arriving at their breeding grounds, seven were long‐distance migrants arriving at their nonbreeding grounds, and one was a middle‐distance migrant also arriving at its nonbreeding ground. For 12 species, we gathered data from more than one location, enabling us to assess the consistency of intraspecific trends at different locations. Regressions of climate variables against year show that across south‐east Australia average annual maximum and minimum temperatures have increased by 0.17°C and 0.13°C decade^?1 since 1960, respectively. Over this period there has been an average advance in arrival of 3.5 days decade^?1; 16 of the 45 time‐series (representing 12 of the 24 species studied) showed a significant trend toward earlier arrival, while only one time‐series showed a significant delay. Conversely, there has been an average delay in departure of 5.1 days decade^?1; four of the 21 departure time‐series (four species) showed a significant trend toward later departure, while one species showed a significant trend toward earlier departure. However, differences emerge between the arrival and departure of short‐ to middle‐distance species visiting south‐east Australia to breed compared with long‐distance species that spend their nonbreeding period here. On average, short‐ to middle‐distance migrants have arrived at their breeding grounds 3.1 days decade^?1 earlier and delayed departure by 8.1 days decade^?1, thus extending the time spent in their breeding grounds by ～11 days decade^?1. The average advance in arrival at the nonbreeding grounds of long‐distance migrants is 6.8 days decade^?1. These species, however, have also advanced departure by an average of 6.9 days decade^?1. Hence, the length of stay has not changed but rather, the timing of events has advanced. The patterns of change in FAD and LDD of Australian migratory birds are of a similar magnitude to changes undergone by Northern Hemisphere species, and add further evidence that the modest warming experienced over the past few decades has already had significant biological impacts on a global scale.     

Habitat and laying date of Great and Blue Tit Parus major and P. caeruleus

Using 19 year's data from nine study areas at Ghent we investigated the effect of habitat on laying date, and found it to be quite different for Great and Blue Tits. In Great Tits we found a clear gradient in laying dates from urban over suburban to rural habitats. Blue Tits laid earliest in a suburban habitat and latest in a rural habitat. All other areas, including urban, suburban and rural ones, formed one intermediate group. The overall average laying date for the Great Tit, 18.9 April, was slightly earlier than that of the Blue Tit, 19.4 April. In urban areas Great Tits laid significantly earlier than Blue Tits, in optimal oak habitat and in one suburban area Blue Tits laid earlier, whereas in the five remaining areas no significant differences between the two species were found.
We argue that the differences in laying dates, although correlated to temperature, are probably caused by differences in the timing of food availability. We suggest that differences in laying dates of Great and Blue Tits are caused by a different response to environmental variations through differences in feeding ecology.     

Effect of food abundance on laying date and clutch size in the White Stork Ciconia ciconia

CapsuleFood independently affects both laying date and clutch size, suggesting that seasonal decline in clutch size is related to a decrease in food availability.

Aim To test the effect of food abundance on laying date and clutch size of the White Stork and identify the cause of seasonal decline in the number of eggs laid.

Methods During 1991 and 1996 we recorded clutch size and laying date of pairs breeding next to rubbish dumps (food abundant and constant throughout the breeding season) and birds breeding far from rubbish dumps (using natural food sources).

Results In 1991 there was no difference in mean laying date between pairs nesting at rubbish dumps and control pairs. Clutch size was significantly larger at rubbish dump nests. In contrast, mean laying date was earlier in control pairs in 1996 and there was no significant differences in clutch sizes, even when controlling for laying date effect.

Conclusion The results support the hypothesis that food availability independently affects both laying date and clutch size. The seasonal decline in clutch size close to rubbish dumps was negligible (1991) or much smaller than in the control zone (1996) suggesting that a progressive deterioration of natural food sources is the most probable reason for a decline in clutch size as the season advances.     

Climate change, migratory connctivity and changes in laying date and clutch size of the pied flycatcher

We examined long-term (1943–2003) variability in laying dates and clutch sizes in a Finnish population of the pied flycatcher Ficedula hypoleuca Pallas, and analysed whether potential changes were explained by changes in climatic factors at the wintering area in Africa, at migration route or at breeding grounds. Among-year variation in both mean and skewness of laying dates increased, which for mean laying date appeared to be explained by variability of temperatures at the breeding grounds and for skewness by variable temperature trends along the migration route. Pied flycatchers bred earlier in warm springs, but despite a warming trend in pre-laying temperatures, the laying dates tended to delay. Laying dates became continuously later in relation to the phenology of the environment. Mean clutch size decreased with time when mean laying date was controlled for, but the climatic factors did not appear to explain the decrease. The advancement of spring phenology may have shifted some food sources needed for egg-laying, thus leading to later laying and smaller clutches. Variation in clutch size increased when wintering conditions were favourable so that clutch size distribution was skewed with a tail of small clutches when there had been lot of rainfall (more vegetation and insects) in the wintering area. We suggest that when ecological conditions during winter were good, the tail of small clutches represented low-quality individuals that were not able to breed after bad winters. Our analyses demonstrate that measures of spread and symmetry give different information about population level changes than means, and thus complement the understanding of the potential influences of climate change on populations.