Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems

Biological Journal of the Linnean Society (2001), 74: 549–555. With 2 figures doi:10.1006/bijl.2001.0593, available online at http://www.idealibrary.com on

Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems DONALD BLOMQVIST∗, JOHAN WALLANDER and MALTE ANDERSSON Department of Zoology, Animal Ecology, Go¨teborg University, Box 463, SE-405 30 Go¨teborg, Sweden Received 8 February 2001; accepted for publication 1 August 2001

Production of successive clutches within the same breeding season has received less attention than many other aspects of avian reproduction. Waders are of particular interest because in these birds, multiple clutches are associated with at least three different breeding systems: double-clutching (uniparental care), monogamous doublebrooding (biparental care) and polyandry (uni- or biparental care). Data from eight species and twelve breeding populations suggest that early second clutches, and thus brood overlap, are associated with parental role division and uniparental care, whereas species or populations with biparental care tend to have long intervals between successive clutches. We suggest that ecological factors influencing the relative timing of the second clutch will have consequences for the parental care system. In particular, conditions that favour early laying of the second clutch (large brood overlap) are likely to lead to parental role division, as found in double-clutching species. Factors determining the timing of second clutches are discussed, as are possibilities for testing these ideas.  2001 The Linnean Society of London

ADDITIONAL KEY WORDS: brood overlap – parental care – double-clutching – double-brooding – shorebirds.

(Burley, 1980; but see e.g. Tinbergen, 1987; Linde´n, 1988; Verhulst & Hut, 1996). Here, we review parental care of multiple clutches in waders, suggesting possible reasons for an interesting pattern – parental role division between successive clutches is associated with early laying of the second clutch. Conversely, there is a long time interval between clutches in species or populations with biparental care. Early laying of the second clutch may be adaptive when biparental care of each clutch is not essential for offspring survival, and resources permit rapid production of several clutches.

INTRODUCTION Patterns of parental care vary widely among animal taxa, often also between closely related species (Clutton-Brock, 1991). Much of this variation can be found within waders (Aves: Charadrii): in some species both sexes tend the eggs and chicks, whereas only one parent, either the male or the female, provides care in others (e.g. Sze´kely & Reynolds, 1995). Owing to the great variation in parental care and mating systems among waders, this group has played a prominent role in studies of the evolution of such systems (e.g. Erckmann, 1983; Oring, 1986; Larsen, 1991; Sze´kely & Reynolds, 1995; Larsen, Sordahl & Byrkjedal, 1996; Whitfield & Tomkovich, 1996). Rearing of several broods or litters during one season occurs in birds (e.g. Burley, 1980), mammals (e.g. Mendl, 1988) and fish (e.g. Potts & Wootton, 1984). Even if many birds, including some waders, produce successive clutches, this tactic has received less attention than many other aspects of avian reproduction

MATERIAL AND METHODS We collected the data from both published and unpublished sources (see Table 1 and Appendix). We included two polyandrous species showing variation in parental roles: Kentish plover Charadrius alexandrinus and spotted sandpiper Actitis macularia. Parental care is highly variable in Kentish plovers, ranging from biparental care of eggs and chicks to brood desertion by either sex (e.g. Amat, Fraga & Arroyo, 1999). In spotted sandpipers, parental care is usually shared at low or medium breeding densities.

∗ Corresponding author. Present address: Konrad Lorenz Institute for Comparative Ethology, Austrian Academy of Sciences, Savoyenstrasse 1a, A-1160 Vienna, Austria. E-mail: [email protected] 0024–4066/01/120549+07 $35.00/0

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Female care is more variable at high breeding densities, but polyandrous females often help their secondary mates incubate (Oring, 1986). Also in the polyandrous Eurasian dotterel Charadrius morinellus, females sometimes participate in incubation of second or late clutches (Cramp & Simmons, 1983), but we did not find sufficient data on inter-clutch intervals for this species. In other polyandrous waders, females usually do not perform parental care (see below). For each species or population, we calculated the relative length of the time interval between successive clutches as the number of days between completion of egg-laying in the first clutch and start of the second one, divided by the duration of incubation plus chickrearing. In both spotted sandpipers and Kentish plovers, females typically desert their first brood and mate with new males (Oring, 1986; Amat et al., 1999). We therefore used data on time intervals between successive clutches produced by polyandrous females in these species.

RESULTS AND DISCUSSION MULTIPLE CLUTCH SYSTEMS IN WADERS

Waders often produce a replacement clutch if the first clutch or brood is lost (see e.g. Cramp & Simmons, 1983). In addition, proper multiple clutches (produced even though the previous clutch has not failed) occur in some species. They are associated with at least three different breeding systems (see Reynolds, 1996): double-clutching, monogamous double-brooding and polyandry. Double-clutching, which may involve elements of polygamy by both sexes, means that the female lays two clutches in rapid succession. There is a distinct parental role division between the clutches: the first one is tended by the male and the second by the female (Table 1). In contrast to polyandrous species (see below), the sexes therefore contribute about equally to parental care (Erckmann, 1983). Double-clutching has only been demonstrated in two waders; Temminck’s stint Calidris temminckii and mountain plover Charadrius montanus, but it may occur also in little stint Calidris minuta and sanderling C. alba (e.g. Oring, 1986). Double-brooding refers to the same pair rearing two broods in succession: after successfully raising one brood, the pair produces a second in the same season (Table 1; see Erckmann, 1983 for definition). It seems to be relatively uncommon among waders, occurring mainly in temperate and tropical charadriine plovers (Erckmann, 1983). Polyandry has been recorded in 12–16 species, belonging to five different families (Erckmann, 1983; Oring, 1986). In these species, females produce multiple clutches by mating simultaneously or sequentially

with different males. Polyandrous waders usually show sex-role reversal, with reduced or no parental care by females (Erckmann, 1983; Oring, 1986). Since our aim is to examine variation in parental roles, this review does not deal further with polyandrous species in which females rarely or never perform parental care (e.g. jacanas and phalaropes; see Erckmann, 1983; Oring, 1986).

ONE OR TWO PARENTS?

Recent studies of the lapwing Vanellus vanellus show that consecutive clutches may be associated with quite different patterns of parental care. Cases reported from northern England probably represent traditional double-brooding with biparental care of both clutches (Parish, Thompson & Coulson, 1997a,b). In southwestern Sweden, however, lapwings tending successive clutches show clear parental role division, and the breeding system may be described as intermediate between double-brooding and double-clutching (Table 1). Recently, Liker & Sze´kely (1999) showed that biparental as well as uniparental care by either sex also occur among lapwings in Hungary. This variation is interesting in relation to the suggestion that doubleclutching has evolved via brood overlap in doublebrooding species (Pienkowski & Greenwood, 1979; Erckmann, 1983; Blomqvist & Johansson, 1994). Available data suggest that waders with parental role division between successive clutches also have shorter time intervals between them than those with biparental care of both clutches (Fig. 1). For example, lapwings in Sweden began laying second clutches about the time of hatching of their first clutches, on average almost two weeks earlier than in England (Fig. 1, Appendix). Thus, the relative timing of the second clutch may play a proximate role for whether the parental behaviours typical for double-clutching or double-brooding will occur (Fig. 2). Even if a pair produces overlapping clutches, parents need not necessarily adopt different roles. An alternative is that each parent divides its care between incubating one clutch and tending chicks in an earlier brood. Common pigeons Columba livia, for example, often produce two clutches in nearby nests, sometimes with considerable time overlap between them (approaching 100%). The male may tend the first brood as well as participate in incubation of the second clutch (Burley, 1980). Such splitting of care is, however, probably inefficient in waders and other precocial species. In lapwings, for instance, the second nest is placed 50–100 m from the first one (Blomqvist & Johansson, 1994), and broods may move several hundred metres between nests and foraging areas (Johansson & Blomqvist, 1996). The incubating parent therefore has less knowledge of the present whereabouts of the chicks

SUCCESSIVE CLUTCHES AND PARENTAL ROLES

551

Table 1. Parental roles in some waders laying multiple clutches. B=both parents, M=male only, M+=predominantly the male, F=female only First clutch

Second clutch

Species

Study area Breeding systema

Incubation

Chickrearing

Incubation

Chickrearing

Ref.b

Temminck’s stint Calidris temminckii Mountain plover Charadrius montanus Spotted Sandpiper Actitis macularia Lapwing Vanellus vanellus

Finland/Norway DC Central USA DC North America SP England DB Sweden DC/DB Europe SP New Zealand DB Sweden DB England DB

M

M

F

F

I, II

Mc

M

F

F

III

M+

M+

M+

M+

IV

B

B

–d

–d

V

B

M

F

F

VI

B

M+

B

–d

VII, VIII, IX

B

B

B

B

X

B

B

B

B

XI

B

B

B

B

XII

Kentish plover Charadrius alexandrinus New Zealand dotterel Charadrius obscurus Ringed plover Charadrius hiaticula Stone curlew Burhinus oedicnemus a

DC: double-clutching, DB: double-brooding, SP: sequential polyandry. I: Hilde´n, 1975; II: Breiehagen, 1989; III: Graul, 1973; IV: Oring, 1986; V: Parish et al., 1997a,b; VI: Blomqvist & Johansson, 1994; VII: Lessells, 1984; VIII: Amat et al., 1999; IX: T. Sze´kely, pers. comm.; X: Dowding et al., 1999; XI: J. Wallander, unpubl.; XII: R. E. Green, unpubl. c Some females may participate in incubation (Graul, 1973). d No conclusive data. b

than has the parent that tends the brood. This may favour role division, with one parent caring for the first clutch and the other for the second. Egg-laying necessarily associates the female with the second clutch and should therefore predispose her to taking care of it (Table 1). Such role division is often found in passerines with successive clutches: the male tends the young from the first clutch while the female lays and incubates the new one (e.g. Haftorn, 1978; Ko¨nig & Gwinner, 1995; Verhulst & Hut, 1996). It is also theoretically possible for birds to have uniparental care and yet produce successive clutches with long time intervals between them. For example, a female could desert her first clutch, leaving it to be cared for by the male alone. She might then spend a relatively long period feeding and preparing for the next clutch, which she can produce with the same or another male and care for herself. We have found no such case among birds, but perhaps it occurs in some other taxon.

WHAT DETERMINES THE INTERVAL BETWEEN CLUTCHES?

Ultimately, the timing of the second clutch should be such as to maximize parental fitness, under constraints set by predation, food availability and other factors. We will address this question at two levels: between and within species (populations), starting with factors that mainly concern differences between species. First, the time available for breeding may be important, with a short breeding season favouring early laying of second clutches. Double-clutching, and thus rapid laying of the second clutch, may occur in some arctic breeding sandpipers with a short breeding season (i.e. little stint and sanderling; Oring, 1986). Double-clutching occurs, however, also in temperate breeding populations of Temminck’s stints (Hilde´n, 1975) and mountain plovers (Graul, 1973). Moreover, Dowding, Wills & Booth (1999) suggested that the occurrence of multiple clutches in New Zealand dot-

D. BLOMQVIST ET AL. 1.6 Uniparental care Uni-/biparental care Biparental care

1.4 1.2 1.0 0.8 0.6 0.4

SCE

RPS

RPG

KPS

NZD

KPF

LWS

LWE

SSN

MPC

0.0

TSN

0.2

TSF

Relative time interval between successive clutches

552

Figure 1. Relative time interval between successive clutches in some waders laying multiple clutches. The relative time interval is the number of days between completion of egg-laying in the first clutch and start of the second one, divided by the duration of incubation plus chick-rearing (mean based on the two range values, see Appendix). A value [1 therefore means no overlap between consecutive broods. Mean and standard deviation are shown, except for Temminck’s stint, Finland (mean and range) and spotted sandpiper (median and range). Species and study areas (sample size), left to right: Temminck’s stint, Finland (12); Temminck’s stint, Norway (5); mountain plover, central USA (2); spotted sandpiper, north USA (sample size not reported); lapwing, England (5); lapwing, Sweden (3); Kentish plover, France (2); Kentish plover, Spain (28); New Zealand dotterel, North Island (5); ringed plover, Germany (3); ringed plover, Sweden (6); stone curlew, England (27). See Appendix for sources and original data.

Incubation

Chick-rearing

Start of laying of second clutch

Uniparental care (double-clutching)

Biparental care (double-brooding)

Figure 2. Relationship between parental care and timing of successive clutches in waders. The likelihood of parental role division and uniparental care (degree of shading of the arrow indicating start of laying of the second clutch) is higher the earlier the second clutch is produced. When it is laid around the time of hatching of the first clutch, form of care is less predictable. When the second clutch is laid closer to or after independence of the chicks of the first brood, biparental care of both clutches is more likely. Factors that influence the timing of laying are discussed in the main text.

terels is not primarily a response to the time available for breeding (see also Erckmann, 1983). Second, we suggest that the abundance and/or temporal distribution of food is important. When food is plentiful, females may be able to produce a second

clutch more quickly, and uniparental care should also be more successful than when food is less abundant. Experimental studies show that some passerine birds are more likely to produce multiple clutches when offered supplemental food during the breeding season

SUCCESSIVE CLUTCHES AND PARENTAL ROLES

(Davies & Lundberg, 1985; Arcese & Smith, 1988) and moorhens, Gallinula chloropus provisioned with extra food produce consecutive clutches with shorter time intervals between them (Eden, Horn & Leonard, 1989). While a rich food supply may not be necessary for production of multiple clutches in waders, food availability generally affects the timing of laying and the interval between successive eggs and clutches (Erckmann, 1983). Third, in several birds there is a trade-off between the number of young in the first brood, and the timing and occurrence of consecutive clutches (e.g. Verhulst & Hut, 1996). Even if waders have a small clutch size (Maclean, 1972), it is possible that the number of chicks in the first brood (and associated costs of parental care) may influence parental timing of the second. If so, we would expect a positive relationship between the number of young raised to fledging and the relative time interval between successive clutches. Experimental reductions of brood size have resulted in shorter inter-clutch intervals in several bird species (e.g. ten Cate & Hilbers, 1991). Assuming the relationship in Figure 2, the optimal timing of the second clutch also depends on the relative success of uniparental versus biparental care. For example, Erckmann (1983) and Larsen (1991) suggested that biparental care is most advantageous in relatively large waders that can defend their offspring by aggressive behaviour. Combined efforts from two parents may then be particularly effective. If so, large waders may be unlikely to evolve double-clutching. Such a constraint against double-clutching is lacking in small waders, the species among which strict double-clutching occurs (see Erckmann, 1983; Oring, 1986). Additional factors may also be important. For instance, parents will be under selection to produce the second clutch early if there is a seasonal decline in the reproductive value of a clutch (e.g. Smith, Ka¨llander & Nilsson, 1989). Within populations, at least two factors may influence variation in the timing of successive clutches. Since the ability to rear overlapping clutches increases as birds gain breeding experience (Burley, 1980), experienced parents should be able to produce second clutches more quickly than less experienced ones. Moreover, parents may initiate a second clutch as a response to a substantial reduction of their first brood; Parish et al. (1997a,b) recorded five lapwing pairs producing second clutches, and in each of these cases only one chick remained in the first brood. Second clutches may be laid early when chick losses, due to predation or other causes, occur soon after hatching. CONCLUDING REMARKS

We suggest that ecological factors affecting the timing of successive clutches will also influence the parental

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care system. The factors that determine whether second clutches will be laid early or late are, however, insufficiently known and deserve attention in future studies. Due to limited data we were unable to control for phylogeny (e.g. Harvey & Pagel, 1991), which is desirable in future tests as data from more waders become available. Our hypothesis may also be testable in other groups with multiple clutches and variable parental roles.

ACKNOWLEDGEMENTS We thank R. E. Green and T. Sze´kely for kindly providing unpublished data, and the Behavioural Ecology Group at the Zoological Museum in Oslo, as well as B. Kempenaers, T. Larsen, D. Parish, M. Taborsky, S. Tebbich, J. Walters and anonymous reviewers for valuable comments on different versions of the manuscript. This paper was begun while D.B. visited the Zoological Museum in Oslo, supported by a post-doctoral scholarship from the Nordic Academy for Advanced Study (NorFA).

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APPENDIX Duration of incubation and chick-rearing (days), and time interval between successive clutches (number of days between completion of egg-laying in the first clutch and start of the second one) in some waders laying multiple clutches. When available, time intervals are given separately for different populations

Duration (days) of

Time interval (days) between successive clutches

Species

incubationa

chick-rearinga

Mean (n)

Temminck’s stint

21–22

15–18

Mountain plover Spotted sandpiper

28–31 19–24

33–36 18–21

Lapwing

25–28

35–40

Kentish plover

24–27

27–31

New Zealand dotterel Ringed plover

28–32 23–25

36–46 24

Stone curlew

24–26

36–42

3.0 (12) 6.9 (5) 12.0 (2) 8.0d (not reported) 35.3 (3) 47.0 (5) 47.5 (2) 57.3 (28) 73.6 (5) 42.7 (3) 53.8 (6) 77.3 (27)

SD 2.3–4.0c 3.1 1.4 1–28c 9.6 4.0 9.2 12.4 11.4 10.3 10.0 9.9

Ref.b I II III IV V VI VII VIII IX X XI XII

a Data from Cramp & Simmons (1983), except for mountain plover, spotted sandpiper (del Hoyo, Elliot & Sargatal, 1996) and New Zealand dotterel (Dowding et al., 1999). b I: Glutz von Blotzheim, Bauer & Bezzel, 1975; II: Breiehagen, 1989; III: Graul, 1973; IV: Lank, Oring & Maxson, 1985; V: Blomqvist & Johansson, 1994; VI: Parish et al., 1997a; VII: Lessells, 1984; VIII: Amat et al., 1999; IX: Dowding et al., 1999; X: Cramp & Simmons, 1983; XI: J. Wallander, unpubl.; XII: R. E. Green, unpubl. c Range values. d Median.