Present address: Centre for Applied Conservation Research, Forest Sciences, 3rd floor, 2424 Main Mall, University of British Columbia, Vancouver BC, Canada V6T 1Z4.
Nest scrape design and clutch heat loss in Pectoral Sandpipers (Calidris melanotos)
Article first published online: 19 JUN 2002
Volume 16, Issue 3, pages 305–312, June 2002
How to Cite
Reid, J. M., Cresswell, W., Holt, S., Mellanby, R. J., Whitfield, D. P. and Ruxton, G. D. (2002), Nest scrape design and clutch heat loss in Pectoral Sandpipers (Calidris melanotos). Functional Ecology, 16: 305–312. doi: 10.1046/j.1365-2435.2002.00632.x
- Issue published online: 19 JUN 2002
- Article first published online: 19 JUN 2002
- Received 14 June 2001;revised 16 October 2001;accepted 31 October 2001
- Construction behaviour;
- cost of incubation;
- egg temperature;
- nest lining;
- optimal behaviour
1. The reasons why birds construct nest scrapes, and the extent to which scrape designs reflect functional optima, are poorly understood. Working on Pectoral Sandpipers (Calidris melanotos, Vieillot), we investigated whether scrapes function to insulate clutches and are efficiently designed to reduce heat loss rates.
2. Excavating a scrape and using lining material reduced the rate at which an object positioned within a scrape lost heat by 9% and 25%, respectively, suggesting that lined scrapes insulate clutches.
3. The rate of heat loss from an object within a scrape increased with scrape depth and decreased non-linearly with lining depth. The extent to which wind increased forced convective heat loss decreased with scrape depth.
4. On average, Pectoral Sandpipers used the minimum lining depth that approximately minimized heat loss through the lining. Mean scrape depth approximately minimized convective cooling in windy conditions while minimizing heat loss to the ground. Pectoral Sandpiper scrapes therefore efficiently reduced heat loss given conflicting environmental thermal pressures.
5. Available lining materials differed in insulative quality when both damp and dry. Pectoral Sandpipers used lining materials that insulated relatively well when damp more than expected given random collection of locally available materials. Linings therefore insulated efficiently given the damp nesting environment.
Individuals of many species build physical structures that extend their ability to control the environment beyond their immediate body (Hansell 1984, 2000), behaviour that can be central to a species’ ecology. While the principal functions of these structures often appear obvious (Hansell 1984), the evolutionary reasons for the construction of some animal artefacts have been much debated (e.g. Humphries & Ruxton 1999; Seidelmann 1999). Further, construction behaviour and the design of the completed structure have been argued to reflect an individual’s genotype (Dawkins 1982). Consequently, over evolutionary time, structural designs might be expected to be shaped by selection to approach functional optima. Although not without its critics, investigation of the extent to which animal behaviours approach empirically determined quantitative optima has provided an important means of testing adaptationist hypotheses in ethology (e.g. Belovsky 1978; Zach 1979; Orzack & Sober 1994; Parker & Simmons 1994). However, in contrast, the extent to which the designs of animal constructions approach quantitative functional optima has seldom been investigated.
Construction behaviour is widespread among birds, where most species build a nest of some description in which to lay their eggs (Collias & Collias 1984; Hansell 2000). Oviparity requires the developmental conditions experienced by offspring to be modulated externally, and parental regulation of the embryos’ thermal environment may be a particularly crucial element of a successful breeding attempt (Lundy 1969; Webb 1987). However, as energy is required both to maintain eggs at suitable equilibrium temperatures (Williams 1996) and to rewarm cool clutches (Vleck 1981; Biebach 1986), egg temperature regulation can be energetically demanding for parents (reviewed by Williams 1996). The demand of brooding young chicks may also be far from insignificant (Pearson 1994). Such demands can be sufficient to constrain parental investment patterns and thus fitness (Reid, Monaghan & Nager 2002), while allowing embryos and chicks to chill may also affect their survival directly (Lundy 1969; Webb 1987). Consequently, there is likely to be selection for mechanisms that reduce rates of heat loss from eggs and chicks. As in other taxa, the construction of an avian nest has been suggested to function at least partly to insulate offspring (Collias & Collias 1984; Redman, Selman & Speakman 1999; Weisrock & Janzen 1999; Hansell 2000).
Nestbuilding behaviour is likely to be influenced by multiple ecological factors (Møller 1984, 1990; Hansell 2000). Indeed, the location and design of arboreal and woven nests has frequently been suggested to reflect the resolution of trade-offs between a range of selective pressures (e.g. Gotmark et al. 1995; Ramsay, Otter & Ratcliffe 1999). However, there is mounting evidence that the need to control the thermal environment may greatly influence the construction of such nests (Collias & Collias 1984; Hansell 2000). For example, nest design and location can be modulated in response to local climatic conditions (Schaefer 1980; Inouye, Huntly & Inouye 1981; Walsberg 1981; Collias & Collias 1984; Kern 1984; Møller 1987a; Franklin 1995; Hooge, Stanback & Koenig 1999), although such relationships have been qualitatively rather than quantitatively assessed. However, many birds nest on the ground, constructing nest scrapes in which to accommodate their eggs. Scrapes range from simple shallow hollows in the substratum to deeper structures that contain quantities of multiple lining materials, including grass, moss, lichens and even pebbles, shells and sheep droppings (Kull 1977; Cramp & Simmons 1983; Solis & DeLope 1995; Byrkjedal & Thompson 1998; S. Lengyel & T. Székely, unpublished data). Despite debate (Summers & Hockey 1981; Solis & DeLope 1995; Byrkjedal & Thompson 1998), the principal functions of nest scrapes and thus the selective pressures favouring their construction and the determinants of their design are poorly understood. Indeed, scrape design was scarcely mentioned within a recent review of avian nest design and construction behaviour (Hansell 2000).
Working on Pectoral Sandpipers (Calidris melanotos, Vieillot), we investigated the hypothesis that using a lined nest scrape might reduce the rate of heat loss from a clutch. Thus we discuss whether scrape construction can be interpreted as a mechanism for regulating the thermal conditions experienced by developing offspring. Further, by experimentally investigating relationships between scrape dimensions and heat loss rates and relating patterns of lining material use to materials’ insulative qualities, we investigate how efficiently Pectoral Sandpiper scrapes reduce heat loss rates, and discuss the extent to which scrape design approaches a functional optimum.
Materials and methods
We studied Pectoral Sandpipers breeding on Arctic tundra in Barrow, Alaska (72° N, 156° W) during June 2000. Male Pectoral Sandpipers did not assist females with incubation, and clutches were consequently left unattended during females’ frequent foraging breaks (Norton 1972; J. M. Reid et al., personal observation). During the study period, air temperature averaged 8·7 ± 0·8 °C and conditions were frequently damp and breezy (mean wind speed of 3·2 ± 0·8 m s−1). Unattended clutches are therefore likely to have lost heat rapidly by forced convection. Further, as ground temperatures did not exceed 7 °C and declined down to the subsoil permafrost layer, clutches are likely to have experienced rapid heat loss to the ground. Given these conditions, selection for mechanisms that reduce the rate of heat loss is likely. As Pectoral Sandpiper chicks leave the nest soon after hatching, their posthatching requirements are unlikely to influence the conditions that parents provide in the nest.
Pectoral Sandpipers built steep-sided scrapes that contained considerable volumes of lining material. To quantify a scrape’s insulative quality, the rate at which a standard object placed inside the scrape lost heat was measured. An artificial egg with dimensions matching real Pectoral Sandpiper eggs was made from Fimo modelling clay (EberhardFaber, Neumarkt, Germany), warmed to 35 °C using a battery operated heating mat (Radio Spares, Glasgow) and placed within a scrape. A thermistor embedded in the centre of the artificial egg was connected to a TinyTalk datalogger (Gemini Dataloggers Ltd, Chichester), and temperature was logged every 10 s as the egg cooled towards ambient temperature. Newton’s law of cooling (egg temperature = ambient temperature +[(initial egg temperature – ambient temperature)exp(–C × time)], where C is a positive fitted constant) was fitted to the cooling curve recorded (minimum R2 of 0·985). The value of the exponential cooling coefficient (referred to as C) reflects the rate of heat loss from the egg within the scrape, and depends on the thermal properties of both the egg and its environment. A high C-value reflects rapid equilibration of the warmed egg with the environment and thus, in this case, a rapid rate of heat loss from the egg.
When a nest scrape was located, the clutch was temporarily removed and placed in a secure insulated box, and the cooling coefficient of a warmed egg placed within the scrape was measured. The cooling coefficient of an egg placed in a randomly selected position immediately adjacent to the scrape was measured simultaneously, using identical equipment and protocol. To investigate the thermal consequences of lining a scrape, lining material was temporarily removed, and the cooling coefficient of an egg placed within the empty scrape was measured. Removed linings were separated into their component materials and the proportion of the lining volume that was made up of each material was estimated. The maximum diameter of each scrape and the depth from ground level to the lining surface and to the scrape floor were measured to the nearest millimetre. The entire experimental procedure took approximately 20 min, a duration that is within the range of female Pectoral Sandpipers’ natural absences from the nest (Norton 1972; J. M. Reid et al., personal observation). Linings and clutches were returned to scrapes as soon as measurements had been completed and all females readily recommenced incubation.
To investigate whether Pectoral Sandpipers used lining materials in the proportions expected from local availability, we estimated the proportion of the vegetation comprising each lining material within a 30-cm radius of a scrape. As waders typically collect lining material from immediately around their scrape, often gathering material while sitting within the scrape itself (Nethersole-Thompson 1973; Ratcliffe 1976; Nethersole-Thompson & Nethersole-Thompson 1981, 1986; Byrkjedal & Thompson 1998; J. M. Reid et al., personal observation), a material’s abundance within 30 cm of a nest is likely to be a reasonable estimate of its availability as lining (Byrkjedal & Thompson 1998). Paired t-tests on arcsine transformed data were used to compare the proportions of the lining and the local vegetation for which each material accounted. Feathers were recorded as present or absent within 30 cm of each nest.
To investigate how the rate of heat loss from an object within a scrape varied with scrape depth and wind speed, artificial scrapes varying in depth between 3 cm and 12 cm (in 5-mm increments) were constructed in Pectoral Sandpiper breeding habitat. Lining material of a composition similar to that used by Pectoral Sandpipers (approximately 50% grass, 30% leaves and 20% lichens) was collected, and 2 cm was placed in each artificial scrape, creating completed scrapes of depths between 1 and 10 cm. Multiple scrapes of each depth were constructed, and egg cooling coefficients were estimated under varying wind speeds. Scrapes were sheltered from wind during two measurements at each depth.
Artificial scrapes were also used to investigate the relationship between heat loss rate and lining depth. Scrapes were filled with between 0 and 11 cm of lining such that for each depth, cooling eggs rested 3 cm below ground level. Variation in egg cooling coefficient was therefore due to variation in lining depth rather than in egg position. Scrapes were covered with polystyrene blocks during these experiments to ensure that heat was lost predominantly through the lining rather than through the air. Air and ground temperatures were recorded during each cooling coefficient measurement, and surface wind speed was recorded using a Kestrel handheld anenometer (Nielson-Kellerman, Chester, PA, USA).
Artificial scrapes were used in these experiments to avoid disturbing breeding birds. Artificial scrape diameters did not differ from those of real scrapes (means ± 1 SE of 90 ± 1 mm and 91 ± 1 mm, respectively, t44 = 0·4, P = 0·69). When artificial scrape and lining depths approximately matched those of real scrapes, egg cooling coefficients measured within the two did not differ either when the lining was present (mean C-values ±1 SE of 6·4 ± 0·2 × 10−3 and 6·2 ± 0·2 × 10−3 s−1, respectively, t31 = −0·53, P = 0·60) or absent (means ±1 SE of 7·8 ± 0·5 × 10−3 and 8·2 ± 0·4 × 10−3 s−1, respectively, t36 = 1·09, P = 0·28). Thus artificial scrapes accurately reflected the thermal properties of real Pectoral Sandpiper scrapes of similar dimensions.
To measure the insulative properties of possible lining materials, fresh materials were collected from the breeding habitat and surface dampness was allowed to dry. Some 300 cm3 of a dry material was placed in a sealed plastic container and allowed to equilibrate with air temperature. The cooling coefficient of an artificial egg placed in the centre of the material was measured. The volume of material used was sufficient to surround the egg by 2·5 cm on each side, ensuring that heat loss was predominantly through the lining material rather than through the air. Materials were then thoroughly mixed with 200 ml of water that had equilibrated with air temperature, excess water that had not been absorbed after 5 min was drained away, and the cooling coefficient of a warmed egg placed within the damp material was measured as before. This process was repeated for six batches of each lining material.
All statistical tests were two-tailed, and means are presented ±1 standard error.
Twenty-five Pectoral Sandpiper nest scrapes were studied. Mean scrape diameter was 91 ± 1 mm, and mean depth was 31 ± 1 mm with the lining present and 52 ± 2 mm with the lining absent. Scrapes therefore contained 21 ± 2 mm of lining material on average.
Egg cooling coefficients averaged approximately 9% lower when eggs were placed in nest scrapes from which linings had been removed than when placed adjacent to scrapes (Fig. 1). The presence of the natural lining material within a scrape reduced the egg cooling coefficient by 25% compared with the same scrape without the lining (Fig. 1). Thus overall, using a lined scrape reduced the rate at which an artificial egg lost heat by approximately a third.
With wind excluded, the egg cooling coefficient was correlated with scrape depth: heat was lost more rapidly when eggs were placed within deeper scrapes (Fig. 2). Although there is a suggestion that the gradient of the relationship between scrape depth and egg cooling coefficient may decrease in both shallow and deep scrapes, there were insufficient data to test whether a logistic growth equation provided a better fit than a linear model. However, as predicted by heat transfer theory (Winterton 1997), egg cooling coefficient was tightly inversely correlated with ground temperature (r14 = −0·97, N = 16, P < 0·001), and ground temperature decreased non-linearly with depth down to the permafrost layer (Fig. 2).
When scrapes were exposed to wind, egg cooling coefficient was no longer related to scrape depth across all measurements taken (r87 = 0·16, N = 89, P = 0·14). Instead, as eggs generally lost heat faster in strong winds, cooling coefficient was correlated with wind speed (r87 = 0·704, N = 89, P < 0·001). However, the nature of the relationship between wind speed and egg cooling coefficient varied with scrape depth. Cooling coefficient increased markedly with wind speed in shallow scrapes, but was not significantly related to wind speed in scrapes deeper than 7 cm. Indeed, the gradient of the relationship between wind speed and cooling coefficient was correlated with scrape depth (Fig. 3), suggesting that deeper scrapes protected eggs from the cooling effect of the wind. Egg cooling coefficient also varied non-linearly with lining depth (Fig. 4). Adding a small amount of lining material to an empty scrape greatly reduced heat loss rate, while adding more than approximately 2 cm of lining had little further effect.
Seven categories of potential lining materials were available in the breeding habitat: grass, moss, Salix (willow) leaves, feathers and three different foliose lichens, Dactylina arctica, Cetraria cucullata and Thamnolia vermicularis. Cooling coefficients varied significantly between eggs surrounded by different dry materials (one-way anova, F6,38 = 30·35, P < 0·001, Fig. 5). Mean cooling coefficient was lowest in feathers, followed by Salix leaves, Dactylina, grass, Thamnolia, Cetraria and moss. Post-hoc tests showed that mean cooling coefficient was significantly lower in feathers and higher in moss than in all other materials. Other significant differences lay between leaves and Thamnolia, and Dactylina and Cetraria.
Egg cooling coefficient increased significantly with wetting for all materials, although the magnitude of the increase varied among materials (Table 1). Thus although cooling coefficients still differed significantly when eggs were surrounded by different damp materials (one-way anovaF6,35 = 20·2, P < 0·001), wetting altered their relative values (Fig. 5). Mean cooling coefficient was still greatest when eggs were surrounded by moss, but was now second highest in feathers, followed by Cetraria, grass, Thamnolia and Salix leaves. Cooling coefficient was lowest in Dactylina. Post-hoc tests showed that significant differences lay between Thamnolia and Cetraria, grass and feathers, and Cetraria and moss.
|Lining material||% change in cooling coefficient C from dry to wet||Paired t-test|
Pectoral Sandpipers did not use lining materials in the proportions expected from their local abundance (Fig. 6). Dactylina arctica and Salix leaves were used more than expected and there was also a strong trend towards over-representation of Thamnolia vermicularis. Cetraria cucullata and moss were used less than expected. Grass was used in direct proportion to its local availability. Feathers were present within 30 cm of 14 of 25 scrapes but occurred in the lining of only one, where they accounted for less than 1% of the lining volume.
To assess whether differences between observed and expected lining material use were related to the cooling coefficient of an egg placed within each material, the ratio of the average proportion of a nest lining that consisted of each material to its mean abundance within the habitat was plotted against the respective cooling coefficient (Fig. 7). This ratio could not be calculated for feathers, as feather abundance was not estimated as a proportion of either lining or habitat composition. However despite being available, feathers were extremely rarely used as lining material. Their use to abundance ratio was therefore set to zero, and analyses were repeated with and without the inclusion of this data point. After individual arcsine transformation of each proportional data set, the mean extent to which a lining material was used relative to its local abundance was significantly correlated with its insulative quality when damp but not when dry (Fig. 7). This result was not affected by the removal of the feather data point.
Pectoral Sandpipers typically lay a clutch of four eggs (Norton 1973; J. M. Reid et al., personal observation). Thus the thermal properties of the artificial eggs that were used to estimate heat loss rates are unlikely to have been identical to the thermal properties of real Pectoral Sandpiper clutches. The measured heat loss rates are consequently unlikely to have equalled the rates at which real clutches would have lost heat under similar conditions. However, variation in egg cooling coefficient with wind speed and scrape depth reflects variation in the rate of heat loss from within a scrape that results from these conditions. Such variation arises as a function of the scrape’s physical properties and may be expected, within limits, to affect rates of heat loss from different objects consistently (Winterton 1997). We therefore assume that the scrape and lining depths that minimized artificial egg cooling coefficients approximate the dimensions that would minimize the rate of heat loss from real Pectoral Sandpiper clutches.
Artificial eggs lost heat 9% more slowly in bare nest scrapes than when placed immediately adjacent to scrapes. The presence of the natural lining reduced heat loss rate by an additional 25% on average. Thus by constructing a lined nest scrape, sandpipers are likely to substantially reduce the rate at which their clutch loses heat. Such a reduction may improve the thermal conditions experienced by developing offspring and reduce the energetic demand that incubation imposes upon parents, changes that may increase offspring and parental fitness (Webb 1987; Williams 1996; Reid et al. 2002). Both nest scrape excavation and the use of lining material can therefore be viewed as adaptations by which parents can insulate their clutch, although the possibility that scrapes serve other important functions is not excluded.
As the rate of heat loss from artificial eggs varied with both scrape depth and lining depth, the rate of heat loss from a real clutch is likely to depend on both these dimensions. However, the scrape dimensions that it would be absolutely optimal for a parent to construct cannot be deduced from our data. This would require an understanding of the overall fitness costs and benefits of digging slightly deeper scrapes or collecting slightly more lining material. Knowledge of relationships between scrape dimensions and heat loss rates does however, allow the likely thermal consequences of observed scrape designs to be quantitatively assessed.
Pectoral Sandpiper scrapes contained 21 ± 2 mm of lining material on average, a depth at which the addition of more lining material provided little further reduction in the rate of heat loss. Pectoral Sandpipers therefore used approximately the lining depth that minimized heat loss through the lining, while minimizing the amount of material used.
As scrapes averaged 52 ± 2 mm deep, with the natural lining in position, clutches rested approximately 31 mm below ground level. At this depth, clutches are likely to have been poorly protected from forced convective cooling, and to have lost heat rapidly when left unattended on breezy days. Wind speeds during the fieldwork period averaged 3·2 m s−1, a speed that doubled the rate of heat loss from an egg in a 30-mm artificial scrape. As egg cooling coefficient did not increase with wind speed in deep scrapes, Pectoral Sandpipers could have reduced forced convective cooling by positioning their clutches deeper below the ground. However, Pectoral Sandpipers breeding on the tundra faced conflicting thermal pressures, since eggs positioned deeper experienced cooler ground temperatures. The rate of conductive heat loss from any object depends on the temperature gradient between it and its environment (Winterton 1997) and indeed, the rate of egg cooling in still air was tightly correlated with ground temperature. Consequently, as 30 mm is approximately the maximum depth at which ground temperature remained relatively high, this is the maximum depth at which the rate of heat loss to the ground would have remained low. Pectoral Sandpipers therefore positioned their eggs at approximately the depth that is likely to have minimized forced convective cooling while minimizing the rate of heat loss to cold ground.
Although heat loss due to forced convection may be rapid in strong winds, clutches can only cool by this means while left unattended (12–15% of the day in Pectoral Sandpipers, Norton 1972, J. M. Reid et al., personal observation). Contrastingly, heat loss to the ground is likely to continue throughout the incubation period. Parents incubating in poorly insulated scrapes are therefore likely to experience continually high energetic demands while maintaining both clutch and body temperature (Andreev 1999). Thus, although the relative cost of allowing heat loss to the ground and to the air depends on a parent’s nest attendance schedule, overall thermoregulatory demands may often be minimized by reducing heat loss through the lining. In addition, females may be able to negate convective cooling behaviourally, for example, as observed in White-Rumped Sandpipers, by incubating more in windy weather (Cartar & Montgomerie 1985). Thus, although scrape dimensions may be influenced by multiple selective pressures, observed Pectoral Sandpiper scrape and lining depths represent efficient responses to reducing clutch heat loss given the conflicting thermal pressures experienced in the tundra habitat.
A lining material might appear to be present within a scrape more than expected from apparently available stocks if, while gathering lining materials, birds depleted the immediate area of that material. However, as the quantities of lining materials within scrape linings were generally small relative to those remaining around the nest, any depletion effect is likely to have been minor. Apparent material preferences might also arise because materials differ in the ease with which they can be collected. However, collection costs seem unlikely to differ greatly among lichen species and are therefore unlikely to explain their markedly different patterns of use. We suggest that Pectoral Sandpipers selectively used Salix leaves and Dactylina arctica and possibly Thamnolia vermicularis in their nest linings, and avoided moss, Cetraria cucullata and possibly feathers. Indeed, waders have previously been experimentally demonstrated to select specific lining materials (Kull 1977), and selection of lichens and avoidance of moss has been suggested (Byrkjedal & Thompson 1998). Further, the extent to which lining materials were used relative to their local abundance was correlated with their insulative quality when damp. Although scrapes were typically located on relatively dry areas within the marshy tundra (Pitelka 1959; J. M. Reid et al., personal observation), linings remained damp to the touch throughout the season. Thus we suggest that Pectoral Sandpipers selected lining materials that minimized heat loss from the clutch to the ground, given their damp environment. The design of Pectoral Sandpiper scrape linings is therefore consistent with the efficient use of local materials to minimize heat loss rates.
Although specific lining materials may have been selected from locally available supplies, lining composition varied between scrapes and was therefore not always optimized absolutely with respect to insulative quality. Dactylina arctica and Salix leaves that insulated well were widely available in the breeding habitat, but Pectoral Sandpipers did not import these materials to areas where they were locally scarce. It is possible that this was because the time and energy demands of importation were greater than those of compensating for more rapid heat loss. However, importing foreign lining materials has elsewhere been suggested to make clutches more vulnerable to visually searching predators (Collias & Collias 1984; Møller 1987b; Solis & DeLope 1995; Byrkjedal & Thompson 1998). As 14% of known wader nests were depredated during our study and a predation rate of 25·8% has previously been reported for Pectoral Sandpipers in the same area (Norton 1973), minimizing predation risk may be an important selective pressure in this system. Overall, Pectoral Sandpiper nest lining composition may therefore reflect the resolution of a trade-off between insulating and camouflaging a clutch. Further work should investigate how scrape design might vary with changes in the intensity of these pressures.
David Norton, Dave Ramey and the Barrow Arctic Science Consortium were of great help during the fieldwork. Jim Dickson and Brian Corpins kindly assisted with lichen identification. Mike Hansell, Geoff Hilton, Pat Monaghan and Tamas Székely provided invaluable discussion of the ideas presented. This work was funded by a British Ecological Society Small Ecological Project Grant and by grants from the Frank M. Chapman Memorial Fund, the British Ornithologists’ Union and the Glasgow Natural History Society to JMR, and by NERC grant GR9/04607 to WC.
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