Laying Plasticity in an Avian Brood Parasite

Abstract

Females of some bird species “steal“ the parental care of other breeding individuals by laying eggs parasitically in their nests. In most populations, conspecific brood parasites lay parasitically before laying in their own nests. By contrast, in a young and expanding Common Moorhen (Gallinula chloropus) population, 17.4% (n = 8) of brood parasites laid parasitically when their own clutches were currently being incubated, and 13.1% (n = 6) laid parasitically when they were tending to their young. This result differs from previous data on conspecific brood parasitism in this (and other) avian species and suggests that sitespecific ecological conditions exert differing selective influences on the behavioral development of populations. The behavior adopted by individual vertebrate species may not, therefore, be rigidly fixed throughout their geographic range.

Resumen

Plasticidad en la Puesta de Huevos en un Ave Parásita de Cría

Las hembras de algunas especies de aves “roban“ el cuidado parental de otros individuos al parasitarles los nidos con sus huevos. En la mayoría de las poblaciones, las aves parásitas coespecíficas realizan una puesta parásita antes de poner huevos en sus propios nidos. En contraste, en una población joven y en expansión de Gallinula chloropus, el 17.4% (n = 8) de las aves parasitaron nidos cuando sus propias nidadas estaban siendo incubadas, y el 13.1% (n = 6) parasitaron nidos cuando estaban atendiendo a sus pichones. Este resultado difiere de los datos anteriores de parasitismo de cría para aves coespecíficas en esta y otras especies, y sugiere que las condiciones ecológicas específicas de los sitios ejercen influencias selectivas diferentes en el desarrollo del comportamiento de las poblaciones. Por lo tanto, el comportamiento adoptado por cada especie de vertebrado podría no estar fijado de modo rígido a través de su rango geográfico.

Conspecific brood parasitism (CBP), in which a female lays eggs in conspecifics’ nests, occurs in more than 230 avian species and attracts considerable interest from behavioral ecologists (Brown 1984, Davies 1988, Petrie and Moller 1991, Tov 2001). This additional reproductive output can increase the lifetime fitness of CBP strategists as they exploit the parental care of other breeding groups, leaving more time and resources for the care of their own broods (Brown and Brown 1989, 1998). Conspecific brood parasitism is frequently reported in avian species (namely the Anseriformes) in which females predominantly provide parental care and young do not require parental provisioning (Andersson 1984, Lank et al. 1989). Conspecific brood parasitism also occurs in populations of some semi-precocial (with semi-dependant young) and altricial (with fully dependent young) species in which parental care is provided by both males and females (Tov 1980, Petrie and Moller 1991). Detailed studies of the laying behavior of brood parasites, amassed from a wide diversity of avian families, have revealed that females lay parasitically before laying in their own nests (Brown and Brown 1989, Alhund and Andersson 1991, Wiegmann and Lamprecht 1991, Sorenson 1993). An exception to that CBP laying trend occurs following nest predation in some species, when females respond to the loss of their own clutches by laying “replacement eggs“ in the nests of conspecific females (Feare 1991, Lyon 1993, McRae 1997b). Given the consensus of empirical evidence on the laying behavior of brood parasites, several evolutionary advantages to females laying eggs parasitically before attempting to lay in their own nests have been postulated (Petrie and Møller 1991). Locating and laying in a conspecific’s nest after laying their own eggs may expose brood parasites’ own clutches to an increased risk of parasitism and predation. Also, females may more effectively locate and monitor potential host nests if they do not have to balance the demands of laying eggs in their nests with those of pursuing a parasitic strategy (Brown and Brown 1989, Petrie and Møller 1991). To test those hypotheses, the CBP laying behavior of Common Moorhens (Gallinula chloropus; hereafter “moorhens“) was studied in a rapidly expanding but high-density population (Forman 2001, Forman and Brain 2004).

Methods

The study was conducted on a 10-year-old, color-ringed population of 200 moorhens at the National Wetlands Centre Wales, in Llanelli, South Wales, between 1997 and 1999 (Forman 2001). Daily nest searches were conducted in suitable habitat, and eggs were individually marked using an indelible pen on the day they were laid. The weight (in grams), length (in millimeters), and width (in millimeters) of individual eggs were also measured at that time, using a 50-g Pesola spring balance and a vernier caliper. Once located, nests were revisited to determine the fates of all eggs. Moorhens usually lay eggs at the rate of one per day (Gibbons 1986, McRae and Burke 1996). To accurately identify CBP events, two criteria were used (after McRae 1994). Conspecific brood parasitism was deemed to have occurred if (1) two or more eggs appeared in a nest within a 24-h period and (2) if an egg was laid in a nest two or more days after the host female had stopped laying. Those criteria have been positively validated in this species through multilocus DNA fingerprinting (McRae 1994, McRae and Burke 1996). A total of 588 nests (86%) was found either before laying had commenced or within one day of clutch initiation. Nests in which the exact laying dates of individual eggs were unknown were excluded from the analysis.

Host selection in this species is spatially restricted to within two or three breeding territories (McRae 1994). Therefore, parasitic eggs were compared directly—or indirectly, using a photographic reference collection (Forman 2001)—with those of females from adjacent territories, and the laying history of every nesting female was examined carefully and in detail. Females known to have laid in their own nests on the same evening that an CBP event occurred were eliminated as possible mothers of the parasitic eggs. There is significant interfemale variation in size (weight, width, length, and volume) of eggs produced annually by moorhens, whereas intraclutch variation in egg size is more predictable (Forman 2001). Therefore, eggs laid parasitically were compared with eggs that suspected brood parasites produced in their own clutches, to determine whether they fell within the normal ranges of egg size for specific females (see also McRae 1997a). This multicriterion approach to identification of moorhen brood parasites has been positively validated as robust, reliable, and accurate (see McRae and Burke 1996). Temporal occurrence of eggs laid parasitically was related to individual females’ specific laying behavior; eggs were rated as having been laid before, during, or after each hen had laid her own clutch.

Results

A variable number of females (14–30%) adopted a CBP strategy annually during the study. Remarkably, parasitism in this population was equally likely to be undertaken by females before (n = 22 females) or after (n = 24 females) laying their own clutches (G-test, G = 0.19, df = 1, P > 0.05), and eggs were laid parasitically in similar numbers before (n = 55 eggs) and after (n = 46 eggs) females had laid their own clutches (G-test, G = 0.40, df = 1, P > 0.05). Only 2.9% (n = 3) of eggs were laid parasitically during the clutch production period. Of the females that laid parasitically after completing their own clutch, 10 (17.4% of CBP females) laid after clutch loss, 8 (13.1%) during incubation, and 6 (21.7%) during the chick-rearing phase of parental care. Those females were as likely to be engaged in incubation and chick rearing as they were to have lost their clutches to a predator (G-test, G = −0.91, df = 2, P > 0.05). Over the study’s duration, females were flexible in their ability to parasitize, in relation to the timing of their own clutch production; 36.7% (n = 18) of individuals switched between laying eggs parasitically before and after laying in their own nests. Of the brood parasites that laid parasitically after producing their own clutches, none lost its own nest to predation when laying parasitically. I recorded only two instances in which brood parasites’ own clutches were parasitized within 24 h after they laid eggs parasitically.

Discussion

Whereas most avian species are limited in their ability to lay parasitically after the production of their own clutches, moorhens in the current study were extremely flexible brood parasites when not engaged in the process of laying their own clutches. In both instances where females laid parasitically while laying their own clutch, incubation had not yet commenced. Such findings are in agreement with the view that females that have commenced incubation are restricted in their ability to parasitize. Staggered laying patterns can result in an exaggerated hatching period, which has been linked to reduced parent and offspring fitness in birds (Nilsson 1993).

Occurrence of parasitism after clutch completion has been documented in American Coots (Fulica americana), a species related to moorhens, in which biparental care also occurs (Lyon 1993). In that species, however, the behavior occurred at a significantly lower incidence and with less-remarkable laying plasticity than reported here (only 1% of eggs were laid parasitically by American Coot females after clutch completion, compared with 44% for moorhens in the present study). Moorhens laid eggs parasitically shortly before and after laying in their own nests, and females “switched“ between the two laying strategies. Eggs that moorhens lay parasitically are produced in addition to those laid in their own nests (McRae 1998), a factor related to the putative low relative cost of egg production in this and related species. The results of the present study strongly suggest that moorhens may have the capacity to finely control egg and clutch production within the constraints of their proximate nutritional status and ecological circumstances (see also Lyon 2003). Moreover, by laying opportunistically after their own laying sequence, females at the study location appear to be demonstrating considerable physiological and hormonal flexibility—though detailed, long-term research is required to confirm that remarkable possibility.

Females from a well-established, high-density moorhen population in Cambridgeshire, United Kingdom, were previously reported to exclusively lay parasitically before laying their own clutches and after clutch loss (Gibbons 1986, McRae 1995). In contrast, incubation and chick-rearing demands did not, in the present study, prevent females from locating and laying in a conspecific’s nest. The risk of each brood parasite’s clutch being depredated or parasitized while she was engaged in laying parasitically was extremely low in the present study (no CBP females’ clutches were depredated during the time they were laying parasitically). It is possible that differing selective pressures operating in each study population account for those geographically derived discrepancies in laying behavior (Foster 1999, Foster and Endler 1999).

In moorhens, males do most of the incubating (Siegfried and Frost 1975). Therefore, in instances in which females have laid their own clutches, males are often in attendance at the nest. That, coupled with the specific ecological conditions present at the study site (see Forman and Brain 2004), may enable females to actively pursue CBP when suitable opportunities arise, without substantially increasing the risk to their own clutch investment. The close packing of breeding groups in well-established populations increases the opportunity for CBP and also results in local high frequencies of nest failure in moorhens (McRae 1995, 1997b). The biotic and abiotic environment and management regime at the Cambridgeshire site is approximately the same as that found in the current study. Intriguingly, it may, therefore, be possible to investigate the influence of predation pressure and CBP risk on the temporal occurrence of different CBP laying and associated behaviors in the current study population as it matures.

Acknowledgments

Many thanks to the Wildfowl and Wetlands Trust, Llanelli, for allowing this study to be undertaken on their site. I also thank E. K. Bollinger and two anonymous referees for their valuable comments.

Literature Cited