50 Wader Study Group Bulletin Egg-laying intervals in shorebirds MARK A. COLWELL Wildlife Department, Humboldt State University, Arcata, CA 95521 USA. [email protected] Colwell, M.A. 2006. Egg-laying intervals in shorebirds. Wader Study Group Bull. 111: 50–59. Keywords: Shorebird, wader, egg laying interval, breeding phenology. The interval between consecutive eggs laid in a clutch by female birds is highly variable, ranging from one day to several weeks. I summarize data for 71 species of shorebird and examine relationships between mini- mum egg-laying intervals and constraints imposed by: 1) time, represented by breeding latitude and length of breeding season; 2) energy, as gauged by relationship between egg mass and female mass; and 3) risk of losing a clutch, measured by whether a species conceals eggs in a nest amidst vegetation or nests in the open. Among shorebirds, the interval is either one (e.g., most sandpipers) or two days (principally plovers, thick-knees and oystercatchers). There was no evidence that longer intervals correlate with greater female investment in egg (or clutch) mass. However, species breeding in more northerly latitudes (with shorter breeding seasons) are more likely to lay at daily intervals than species occupying temperate or tropical environs. A greater percent- age of species that nest in vegetation that conceal eggs and incubating adults laid eggs at daily intervals compared with species nesting in open habitats. These latter two relationships are, however, confounded by taxonomy because sandpipers, which have a northerly breeding distribution and conceal nests, differ from plovers, thick-knees and oystercatchers, which principally breed in open habitats of temperate and tropical latitudes. Nevertheless, it is plausible that in addition to long breeding seasons, longer laying intervals in open- nesting species have evolved as a response to frequent clutch loss owing to predators or the environment. INTRODUCTION (Carey 1996, Lack 1968). Interestingly, egg-laying intervals for these taxa are never as short as 24 h. Consequently, it Among vertebrates, birds are the most uniform in reproduc- appears that virtually all birds can be categorized into one of tive biology: all species are oviparous. Despite this uniform- two groups based on the shortest (hereafter minimum) laying ity, remarkable variation exists across taxa and among interval, species that: 1) regularly lay at intervals of one day, individuals within species in various facets of oviparity or 2) rarely or never lay at intervals of one day. It is true, (Carey 1996). A relatively unexplored facet of egg-laying is however, that within both groups energy (or nutrient) short- the interval between successive eggs in a clutch. The rate at ages can lengthen egg laying beyond this minimum interval which females lay consecutive eggs varies among species, (Carey 1996, Lack 1968). and tends to be slower in larger taxa (Lack 1968, Winkler Variation in egg-laying intervals among and within species 2004) and those with smaller clutches (Johnson 2000, Lack may be related to three principal ecological factors (Carey 1968). Although egg-laying intervals are well known in 1996, Lack 1968): 1) time constraints associated with length commercially exploited taxa, they remain relatively poorly of breeding season, 2) energy costs of forming eggs, and 3) understood in wild birds, probably owing to the difficulty of risk of clutch loss to predators. Species that breed at high recording precisely the timing of oviposition (Shubert 1990). latitudes (or elevations) lay eggs quicker owing to the need In the domestic chicken Gallus domesticus, a single func- to complete breeding in a shorter season, compared to taxa tional left ovary ovulates at approximately 24-h intervals and at southerly latitudes (Morton 1976). The availability of food oviposition occurs at slightly greater than this interval (energy) or nutrients (e.g. calcium) serve as proximate con- (Johnson 2000). However, even in the chicken, where a trols of egg laying, as evidenced by experimentally length- sequence (synonymous with clutch) may vary from 2–9 eggs, ened intervals in female Mallards Anas platyrhynchos denied the rate of egg production (laying) ranges from 25–28.5 h, food during the period of rapid follicular growth (Johnson and this correlates negatively with number of eggs laid 2000). And, in wild species that rely on exogenous energy (Johnson 2000). sources to form eggs, egg-laying intervals commonly exceed For wild birds, even those taxa with two functional ovi- the minimum during periods of inclement weather (Carey ducts (e.g. some Falconiformes, Apterygiformes), females 1996, Lack 1968, Wiebe & Martin 1995). Food also may be never lay eggs at shorter than 24 h intervals (Winkler 2004). an ultimate factor, interacting with mode of development Many species lay eggs daily, including most passerines, (precocial vs altricial) to shape egg-laying intervals. Species waterfowl, and many shorebirds (Lack 1968). By contrast, that lay disproportionately large eggs (relative to female body other species lay consecutive eggs at periods exceeding 24 h, size; e.g., megapodes, penguins) lay at longer intervals. Lack ranging upwards from 2–3 days (e.g., plovers, seabirds), and (1968), however, noted that among seabirds, which lay 4–8 days (e.g., megapodes, penguins) to 14–30 days (kiwis) disproportionately small eggs relative to female body size, Bulletin 111 December 2006 50 Colwell: Egg-laying intervals in shorebirds 51 egg-laying intervals are long (2–5 days); he suggested that as nesting in one of two categories (open vs concealed) based this was evidence for food limitation at the time of egg lay- on a composite of habitat features and the behavioural ing. Lastly, predation may shape egg-laying intervals via the response of adults to danger posed by potential nest preda- risk of losing a clutch of eggs during the laying process (Lack tors (Gochfeld 1984). Briefly, open-nesting species (e.g., 1968). This reasoning, however, addresses the energetics of plovers, avocets and stilts, oystercatchers, and thick-knees) replacing failed clutches rather than danger to a laying are those that did not use vegetation to conceal eggs in the female. nest or incubating adults. In the presence of potential egg Here, I examine variation in minimum egg-laying intervals predators, incubating adults typically slip off the nest quietly in shorebirds in relation to time, energy and risk of clutch and rely on egg crypsis to evade predators; some species mob failure. Shorebirds are an intriguing group in which to study predators. By contrast, concealed nesters (e.g., sandpipers) egg-laying intervals because they: 1) are diverse and well- are those that nest in vegetation that hides cryptically- studied; 2) breed from the high arctic to tropical latitudes; 3) plumaged adults and eggs. Concealed nesters typically react mostly rely on exogenous food resources (see Lenington at closer distances to the approach of a predator by perform- 1984) to lay small clutches; 4) often experience high, but ing distraction displays (e.g. “mouse run”; Gochfeld 1984). variable, rates of clutch failure (Evans & Pienkowski 1984); Specifically, I predicted that species occupying open habitats and 5) either conceal their clutches in vegetation (e.g., sand- (where clutches are at greater risk of loss) would have longer pipers) or nest in open habitats (e.g., plovers, avocets, thick- laying intervals than taxa nesting in vegetated habitats. I used knees), which correlates with the behaviour of adults disturbed chi-square tests to compare the frequencies of species in dif- from incubation (Gochfeld 1984). ferent categories. METHODS RESULTS I reviewed species accounts (in, for example, Birds of North Summary of egg-laying intervals America, Birds of the Western Palearctic, The Birds of Africa) and original scientific literature summarizing details Nearly all shorebirds could be categorized into one of two on breeding biology to compile information (Appendix) on categories. The first group, primarily sandpipers (40), avocets the following variables. I summarized egg-laying intervals to (4), some plovers (11), and an oystercatcher, consisted of 55 the nearest hour when available. However, owing to the dif- species in which females regularly laid eggs at daily intervals. ficulty in accurately determining egg-laying intervals A second group, comprised of thick-knees (2), plovers (12) (Shubert 1990), many authors described the time between and oystercatchers (2), included 16 species in which females successive eggs in a clutch based on daily intervals. So, I rarely or never laid a clutch at intervals shorter than two days; categorized the interval between successive eggs as daily or for most of these species, the egg-laying intervals often longer. Clutch size was the modal number of eggs laid by a exceeded 2 days. For both groups, however, egg-laying female. Fresh mass (g) of eggs and females came from spe- intervals occasionally exceeded the minimum, especially cies accounts or Dunning (1993). during periods of food shortage or inclement weather. For To evaluate time constraints, I compared the frequency example, Nethersole-Thompson & Nethersole-Thompson with which species laid at one day or longer intervals across (1979) recorded precisely Greenshank laying intervals (h) at four latitudinal categories (tropical, temperate, boreal and 26 nests and noted that the usual 2-day (c.44 hour) interval arctic) corresponding to decreasing length of the breeding often lengthened during cool, wet weather. This was true for season. Specifically, if time constrained laying, then a greater other species that laid at longer intervals. For example, the percentage of northerly taxa should have daily egg-laying time between consecutive eggs laid by female Snowy (Kent- intervals compared to those breeding at temperate or tropi- ish) Plovers often lengthened from 2 to 3–5 days during cal latitudes. As another measure of time constraints, I char- periods of cool, wet weather of March and April in coastal acterized length of breeding season (number of weeks) over northern California (Page et al.