Article

Every-Other-Day Clutch-Initiation Synchrony In Ring-Billed Gulls ( Larus Delawarensis )

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Abstract

Fraser Darling suggested that reproductive synchrony enhances reproductive success of colonial seabirds as a result of predator satiation. However, the cost of yearly reproductive synchrony is high for colonial species for which intraspecific predation is the primary cause of egg and chick loss. A few studies indicate that egg-laying synchrony on a daily time scale within the annual breeding pulse may be an adaptive response to intraspecific predation. Here we report every-other-day clutch-initiation synchrony in densely nesting cohorts of Ring-billed Gulls (Larus delawarensis). This is the second known case of clutch-initiation synchrony on a daily time scale in larids, the first being with Glaucous-winged Gulls (L. glaucescens). In both Ring-billed Gulls and Glaucous-winged Gulls, the degree of clutch-initiation synchrony is inversely related to nearest neighbor distance. Further studies are needed to test whether clutch-initiation synchrony in Ring-billed Gulls is adaptive in the presence of cannibalism, or if it is simply a neutral byproduct of colonial nesting.

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... The data from the daily egg counts from the socially coherent neighborhoods described above were evaluated to determine if egg-laying synchrony occurred in those socially coherent neighborhoods. The methodology was previously detailed in Henson et al. (2010Henson et al. ( , 2011 and Sandler et al. (2016). ...
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Increased sea-surface temperatures lead to increased egg cannibalism in Glaucous-winged Gulls (Larus glaucescens). Under these conditions, female gulls, which lay an egg approximately every 2 d, can synchronize egg laying with other females on an every-other-day schedule. Eggs that are laid synchronously are less likely to be cannibalized. The mechanism for synchronization has remained unknown. We studied the relationship between egg laying and mounting in a colony of Glaucous-winged Gulls on Protection Island, Washington, for clues to a synchronizing mechanism. We found that for an individual female an oviposition event reduced the likelihood of mounts for that day as compared to the day before, and that for sampled areas of the colony, total numbers of mounts and eggs laid occurred in an out-of-phase rhythm. These findings support the following conceptual model: early in the breeding season, individual females that have begun laying exhibit a daily alternation of higher and lower mounting activity caused by their natural 2 d oviposition oscillation. By social facilitation, these mounting oscillations of early layers synchronize mounting across the colony, including mounting events involving females that are not yet laying. Mount synchronization eventually leads to every-other-day egg laying synchronization.
... The temporal and spatial clustering of copulation by Glaucouswinged Gulls we demonstrated is consistent with this hypothesis and may suggest the occurrence of reproductive synchrony on an even shorter temporal scale. When examined on a daily timescale, the rises and falls of courtship beg and copulation frequencies found in Glaucous-winged Gulls (Fig. 1) resemble the every-other-day egg-laying synchrony demonstrated for both this species (Henson et al. 2010) and for Ring-billed Gulls (Sandler et al. 2016). Moreover, Atkins et al. (2017) demonstrated that broadcast of a simulated copulation call coordinated the timing of subsequent headtossing and mounting behaviors among Glaucous-winged Gulls such that these behaviors tended to directly follow broadcast of the call; frequencies of head toss and mount gradually declined. ...
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The effects of social stimuli on avian reproductive behaviors such as breeding schedules and courtship behaviors are well known due to numerous field studies. However, studies that have simultaneously examined the effects of social stimuli on reproductive behavior and the mediating endocrine mechanisms have been largely restricted to captive populations, which may not be representative of free-living populations. This study, conducted over two breeding seasons, aimed to simultaneously measure the effects of experimentally increasing auditory stimuli on the breeding schedule and endocrinology (levels of total androgen, estradiol, progesterone and prolactin) on free-living yellow-eyed penguins (Megadyptes antipodes). The yellow-eyed penguin is the least colonial of all penguins, nesting far apart from each other under dense vegetation, and, therefore, is presumed to experience much lower levels of social stimuli than other penguins. Egg laying was significantly more synchronous and tended to be earlier when birds were exposed to playbacks of the calls of conspecifics in 1 year of the study. We also found that levels of total androgen and estradiol of males in 1 year, and prolactin in another year, were proportionally higher among treated birds compared control birds that received no artificial auditory stimuli. These results show that even among supposedly solitary nesters, social stimuli could still play a role in influencing reproductive behavior and physiology. For the first time in free-living seabirds, we have demonstrated that behavioral responses to increased social stimuli are associated with hormonal changes.
A tangerine-scented social odour in a monogamous seabird
  • J C Hagelin
  • I L Jones
  • L E L Rasmussen
HAGELIN, J. C., I. L. JONES, AND L. E. L. RASMUSSEN. 2003. A tangerine-scented social odour in a monogamous seabird. Proceedings of the Royal Society of London, Series B 270:1323-1329.
Surrey Beatty and Sons
  • I Dann
  • P Norman
  • Reilly
Dann, I. Norman, and P. Reilly, Editors). Surrey Beatty and Sons, Chipping Norton, Australia.
Ovulation synchrony as an adaptive response to egg cannibalism in a seabird colony
  • S Weir
WEIR, S. 2015. Ovulation synchrony as an adaptive response to egg cannibalism in a seabird colony. Honors Thesis. Andrews University, Berrien Springs, Michigan, USA.