Our results support the hypothesis that clutch size in shorebirds can be limited by the incubation ability of the parents. We found both a substantial overall cost (fewer young raised to fledging) and several subtle costs (higher hatching asynchrony, marginally lower egg hatchability, fewer prey on the feeding territories) for pairs incubating enlarged clutches. Our data show that the subtle costs may not add up to an overall cost by the end of incubation, because more young hatched from enlarged clutches than from control clutches. However, results from the chick-rearing phase suggest that extra incubation costs may have an effect later, and that the subtle costs may interact synergistically towards the overall cost (lower annual reproductive success) as suggested by Arnold (1999).
This study is the first experimental test of the ILH in which the annual reproductive success of pairs until the fledging of young was measured. Previous studies that did not monitor broods from manipulated clutches could not possibly detect the longer-term, more ‘cryptic’ costs found here. Reliable estimates of incubation costs to be used in life-history theory require equal attention to the incubation phase as well as the chick-rearing phase (Heaney & Monaghan 1996). In passerine birds, for example, clutch size is often limited by how many young parents can rear to fledging (‘Lack’ clutch size; Godfray et al. 1991; VanderWerf 1992), suggesting that costs during brood-rearing can lead to adaptations limiting clutch size. Our results, therefore, clearly support the ILH and reflect to previous calls (Sandercock 1997; Arnold 1999; Wallander & Andersson 2002) for more thought on clutch size limitation in shorebirds.
Whether the extra costs of rearing more chicks hatching from enlarged clutches contributed to our results remains an open question. However, such a scenario is unlikely. First, pairs incubating enlarged clutches had poorer feeding territories and fledged fewer young regardless of whether they cared for more chicks (when the extra egg hatched) or for the number of chicks corresponding to their natural clutch size (when the extra egg did not hatch). Second, both prey abundance on the feeding territory and the number of young surviving to fledging increased with the number of young hatched from non-experimental nests (Lengyel 2006, 2007), and pairs adopted alien chicks frequently (Lengyel 2002), which are not expected if parental care is costly. Therefore, the costs of rearing extra chicks are likely to be low in pied avocets, and those costs should be greatly exceeded by the benefits of a larger brood size. The observation that pairs with broods from enlarged clutches, which produced more hatchlings, could not exploit these benefits further reinforces the idea that the costs of extra incubation had a prolonged cryptic effect on the pairs.
costs of extra eggs during incubation
Avocets appeared to be less affected by the costs of incubating enlarged clutches during nesting. The estimated number of young hatched (cumulative reproductive value, Arnold 1999) was 17% higher for enlarged clutches than for controls (Table 3). This value was +13% in the closely related American avocet, +9% in the spur-winged plover (Vanellus spinosus), and ranged between −55% and +1% in seven other shorebirds (Arnold 1999). The positive values show no major costs of incubating enlarged clutches until hatching and suggest that such birds would benefit from laying one extra egg. We found evidence for only two types of costs during the incubation phase. First, hatching asynchrony increased in enlarged clutches compared to controls, which was also found previously in calidridine sandpipers (Hills 1983; Sandercock 1997). Second, statistically nonsignificant lower hatchability of eggs in enlarged clutches has been found in all but one previous experiment (Hills 1983; Shipley 1984; Delehanty & Oring 1993; Székely et al. 1994; Yogev et al. 1996; Sandercock 1997; Larsen et al. 2003, but see Wallander & Andersson 2002). Lower egg hatchability is most often explained by the inability of incubating parents to adequately warm all five eggs (Hills 1983). In our study, lower hatchability in enlarged clutches was largely due to extra eggs, which hatched in smaller proportions than did the natural eggs. Although increased failure of extra eggs can be related to our transport and handling, this seemed unlikely because most (15 of 19) of the extra eggs that failed were collected as fresh (before or during week 1 of incubation), at which stage the eggs are normally less sensitive to handling. A developed embryo was found in all six extra eggs that were opened after the natural eggs had hatched, which indicated that embryo development continued for some time after transport (the remaining 13 eggs were not opened). These embryos most likely died during incubation as a result of inefficient heat transfer (Hills 1983), which may occur, for example, if parents discriminate between an extra egg and their own natural eggs. Nevertheless, whether the extra egg hatched or not did not affect response variables during chick rearing, therefore, lower egg hatchability in enlarged clutches was not likely to affect our major conclusions.
Table 3. Nesting parameters in enlarged and control clutches. Daily survival rate and nest success are calculated as in Mayfield (1975). The cumulative reproductive value (Arnold 1999) is given as R = C × N × P × H. Data from clutches naturally containing four eggs are used only
We did not find evidence for other costs reported in previous studies. There was no evidence of higher rates of abandonment for enlarged clutches (found in Hills 1983; Delehanty & Oring 1993; Székely et al. 1994). Incubation period did not increase in enlarged clutches, which has been reported in most other shorebirds (Hills 1983; Székely et al. 1994; Yogev et al. 1996; Sandercock 1997; Wallander & Andersson 2002; Larsen et al. 2003). Enlarged clutches did not suffer from higher predation rates than did controls, in contrast to other studies that reported more frequent losses of single eggs (Hills 1983; Shipley 1984; Delehanty & Oring 1993; Sandercock 1997). Finally, chicks hatching in enlarged clutches were not smaller or did not weigh less than chicks hatching from control clutches. Lower chick body condition, if accompanied by lower chick survival, was suggested as a potential cost of five-egg clutches in northern lapwings (Vanellus vanellus) (Larsen et al. 2003).
costs of extra eggs during chick-rearing
Increased hatching asynchrony and lower egg hatchability did not result in an overall decrease in the number of young hatched from enlarged clutches. Similar patterns were found in American avocets (Shipley 1984) and some other shorebirds of medium to large body size (Wallander & Andersson 2002; Larsen et al. 2003), where more chicks hatched from enlarged clutches than from control clutches. Pairs with supernormal clutches parasitized by other females also hatched more young in another study of pied avocets (Hötker 2000). However, this study shows that the number of chicks hatched may not appropriately reflect the costs of extra incubation.
Incubating larger-than-normal clutches requires higher energy expenditure from the parents due to the larger total egg volume that needs to be kept warm (Piersma & Morrison 1994; Thomson, Monaghan & Furness 1998). Our results suggest that the extra energy expenditure during incubation contributes to lower performance of adults during chick rearing. For example, extra energy expenditure may have resulted in poorer body condition or lower success in competing for territories for pairs incubating enlarged clutches. Behavioural time budgets measured when pairs settled in feeding territories showed that pairs incubating enlarged clutches spent more time (28%, n = 4 pairs) feeding than did pairs incubating control clutches (13%, n = 12); however, the results were inconclusive because feeding occurred in only 4 of 12 time budgets of pairs incubating enlarged clutches and there were no differences in other behaviour types between experimental groups (Lengyel 2001). Our results do show, however, that less food was available for chicks hatching from enlarged clutches than for chicks from controls. Two results suggest that food availability may have influenced the survival of chicks. First, prey abundance was positively related to chick survival in controls. Second, the increased mortality of chicks from enlarged clutches occurred after broods spent some time in their feeding territories of lower-than-average prey abundance (by the end of week 2), and not when chick mortality due to predation is most intense (during week 1, Lengyel 2006).
Alternative mechanisms may also explain lower chick survival in broods from enlarged clutches. First, increased mortality may be partly caused by the incubation environment as suggested by Larsen et al. (2003) and Gorman & Nager (2004). The altered microclimate in enlarged clutches is known to reduce hatching success without any apparent direct costs to the incubating parent (Reid, Monaghan & Ruxton 2000). To separate the effects of incubation costs to parents and embryonic developmental costs to chicks would require cross-fostering, when chicks hatching from unmanipulated clutches are raised together with chicks from enlarged clutches, allowing an intra-brood comparison of chick survival. Second, intra-brood competition for food among chicks may also be higher in larger broods. However, in our study population, there is a positive correlation between brood size and prey abundance on the territory, and chick survival is higher in larger than in smaller broods (Lengyel 2007). Moreover, the experimental addition of an extra chick to broods in which parents incubated four eggs did not influence fledging success at the study site (Lengyel 2007), indicating that the overall effect of intra-brood competition on chick survival is likely to be small in pied avocets. Third, a seasonal decline in food resources is also possible, and may be related to why the number of fledglings depended on season in this study. However, there were no seasonal differences among the experimental groups (Table 1), therefore, seasonal effects do not directly explain lower chick survival in broods from enlarged clutches. Finally, it is possible that food resources are depleted more rapidly on territories of broods from enlarged clutches than on territories of control pairs. Our results do not rule out the possibility that food depletion and subtle seasonal differences may contribute to lower food availability and lead to fewer fledglings in broods from enlarged clutches in avocets. In other shorebirds, one or more of the alternative mechanisms during chick-rearing may also be important in limiting clutch size.
Our results suggesting a relationship between food availability and chick survival refine the general view that increased predation risks in larger, more conspicuous broods is primarily important in limiting brood and clutch size in shorebirds. Safriel's (1975) early work in semi-palmated sandpipers (Calidris pusilla), a small-sized, arctic-nesting shorebird with uniparental care showed that chick survival was significantly lower in broods enlarged to five chicks (n = 27 broods in 2 years) than in four-chick control broods (n = 39). He proposed that a greater foraging effort by food-stressed chicks in large broods makes them more conspicuous to predators, which results in their lower survival. Although broods larger than four chicks might be more prone to predation in the studied population of avocets as well, our previous findings showed that more chicks survived to fledging in larger broods, and that increasing brood size by natural adoption was almost a pre-requisite to rear filial young to fledging in high-predation areas (Lengyel 2007). Our previous and current findings indicate that greater vulnerability to predation resulting from higher chick activity in large broods may not directly affect chick survival in avocets. Furthermore, no other experiment in precocial birds has ever reported greater mortality of chicks in larger broods (Rohwer 1985; Lessells 1986; Milonoff & Paananen 1993; Sandercock 1994; Williams, Loonen & Cooke 1994), and one study (Loonen et al. 1999) found that adult Barnacle Geese (Branta leucopsis) with broods enlarged after hatching occupied better feeding territories and fledged more young than did adults with control or experimentally reduced broods. These studies suggest that a mechanism other than greater predation on large broods is necessary to explain clutch size limitation in shorebirds. Our results point to poor body condition or reduced competitive ability of parents and lower food abundance on territories of pairs incubating enlarged clutches as a likely explanation.
Two aspects of this study need to be mentioned for the correct interpretation of the results. First, pairs were allocated lower extra incubation costs in our study than in previous ones. Clutches in most previous experiments were enlarged at egg laying and experimental eggs were present throughout incubation. In contrast, several rescued eggs used here were already some days into incubation, preventing the allocation of full costs to all pairs in this study. It appears plausible that had the full costs been allocated to all pairs, other costs would have been found during the nesting phase or the costs of incubating enlarged clutches detected would have even been larger. Second, we did not exchange eggs in control clutches. A study in which eggs are swapped among nests but clutch size is kept constant would have been a more effective control for the manipulation during clutch enlargement. Egg swapping has been studied previously and concluded to have no effect on egg hatchability in one of the eight previous shorebird clutch manipulations (Wallander & Andersson 2002). We did not use such a control because it was essential to collect baseline information on annual reproductive success in a reliably large sample of unmanipulated nests that may allow for frequent clutch failure and low chick survival (50, 31%, respectively, Lengyel 2006). Moreover, conducting egg-swapping in a meaningful sample size would have presented considerable logistical challenges and would have increased disturbance to nesting colonies, potentially leading to artefacts such as increased rates of clutch abandonment. Because eggs were not swapped, we cannot conclusively exclude the possibility that transport and handling led to lower hatchability of extra eggs. However, this possibility seemed small relative to the differences found. If the extra eggs (n = 56) had had similar hatchability as the natural eggs (92%), 15 chicks would have hatched in addition to those that did hatch (n = 37), which, assuming chick survival at 21%, corresponds to three additional fledglings or to an increase from 0·7 to 0·8 in the mean number of fledglings in broods from enlarged clutches (n = 47). This value (0·8) is still considerably smaller than that in broods from control clutches (1·2), indicating that lower hatchability of extra eggs was not likely to contribute much to the lower overall success for pairs incubating enlarged clutches.
In conclusion, our results support the hypothesis that the incubation of extra eggs causes an energetic cost to parents and that this cost manifests at a later time, during chick rearing. The exhaustion of parents due to the extra incubation costs may prevent pairs from occupying better territories and fledging more young. Extra incubation costs are related to an overall decrease in chick survival, and thus, in the parents’ annual reproductive success. Therefore, our study provides evidence that the invariant clutch size of shorebirds can be explained by limitations in the incubation ability of parents (Lack 1947). Other costs, detectable on longer time-scales (e.g. juvenile survival to breeding, recruitment rate, adult survival and future reproductive success) will also need to be measured for a full understanding of clutch size evolution in shorebirds.