Reproductive Synchrony: Does the Threat of Predation Drive Reproductive Chronology in Communities?
Writer’s Comment: This paper was driven neither by medical urgency nor personal experience, but by pure scientific interest. I chose to write my paper on one of the most fascinating ecological topics: how predation pressure drives prey species to adapt physiologically: specifically, their reproductive timing. The theoretical background behind reproductive synchrony is rich, and while researching this paper, I was reminded that the thrill of science is that it doesn’t always give a straight answer. There can be multiple answers to the same problem, multiple explanations for the same phenomenon, and multiple approaches to evolve a specific behavior or trait. This paper was intended to be an overview of a community-level phenomenon known as reproductive synchrony, offering contrasting views as to how it developed, why it is still adaptive, and how a combination of forces interacted to drive its evolution.
Instructor’s Comment: This was written as Jennifer’s term paper in Evolution and Ecology 149, “Evolution of Ecological Systems.” This is an upper-division class that examines the community concept in ecology from an evolutionary standpoint. It requires extensive reading and synthesis. Students have wide latitude in choosing term paper topics, which must be approved by me before the midterm exam: the only firm requirement is that the paper must deal with some aspect of inter-specific interaction. Jennifer received an A for the paper and for the class. The paper very nicely demonstrates exactly the synthetic approach the class is meant to nurture.
—Arthur Shapiro, Department of Evolution and Ecology
In a phenomenon known as reproductive synchrony, reproductive events throughout a population or community roughly coincide. This synchrony is theorized to be adaptive since it is so widely observed in a number of taxa. Various explanations for the development of this phenomenon have been posited, and the community-level pressure of predation is among the most elegant. Through predator satiation, predator swamping, group defense, or predator avoidance, prey species can control the timing of their reproduction as an anti-predator strategy. Alternative explanations for reproductive synchrony include sensitivity to climatic seasonality and social factors. The wide variation in the degree of synchrony exhibited by numerous taxa suggests that a combination of ecological and social factors combine to coordinate reproduction.
The threat of predation is one of the strongest selectional pressures acting on organisms due to its direct negative consequences for fitness. Over evolutionary time, predation can drive changes in morphology, behavior, and even reproductive physiology, the proximate determinant of reproductive chronology.
Predation pressure has been theorized to be the driving force behind reproductive synchrony, the temporal clustering of reproductive events. Control of reproductive timing can occur at various physiological and behavioral levels, such as breeding, parturition, ovulation, and estrus (Clarke et al. 1992). This phenomenon has been identified in a broad spectrum of taxa. First described in colonial gulls as a means of reducing nest predation rates (Darling 1938, cited by Ims 1990a), reproductive synchrony is now thought to be characteristic of many temperate and tropical ungulates, some insects, an array of small mammals, and a multitude of perennial plant species. This phenomenon can be referred to as “birth synchrony” in animals, or “mast fruiting” or “seeding” in plants.
Because it is so widely observed in many species, reproductive synchrony is thought to have adaptive significance. A population under the threat of predation can benefit from reproductive synchrony through increased offspring survival and thus increased overall fitness. Predation pressure can operate under four distinct mechanisms to affect an organism’s reproductive timing: predator satiation, predator swamping, group defense, and predator avoidance. These four mechanisms may either favor the tight clustering of reproductive events, or drive these events further apart. A multitude of factors further affect how the reproductive timing of a prey species responds to predation pressure, including the life histories of both the predator and the prey species.
Controversy still exists regarding whether reproductive synchrony is a community-level or a population-level phenomenon. Population-level processes occur in a group of individuals of a single species, while community-level processes incorporate multiple populations or species within a given region. Predation pressure demonstrates that reproductive synchrony has consequences not only for the species in question, but also for other species with which it interacts. Predators can exert selectional pressures on prey species, which can in turn influence the population dynamics of both the prey and the predators. Thus, predation pressure and its effects on reproductive coordination can have vast implications for community structure.
Another explanation for the development of reproductive synchrony is coordinating reproduction with seasonal resource abundance. This strategy allows for optimal maternal and juvenile condition, resulting in increased survival and fitness. While this explanation is often offered as an alternative to predation pressure, it is likely that a combination of ecological, social, and environmental factors selected for and later reinforced the evolution of reproductive synchrony.
The Relationship between Predation and Reproductive Synchrony
Because of their high vulnerability at early stages, young animals are the preferred prey for many predators. Thus, reproductive synchrony may constitute an adaptive response to high juvenile predation rates (Ims 1990a). Four mechanisms can influence the reproductive timing of a community under threat of predation. The first is “predator satiation” (Rutberg 1987). In this scenario, predators are physiologically limited in the number of prey that they can process. Birthing synchrony ensures that enough young are produced to satiate predators, while some young remain to survive to the subsequent winter. Despite the sacrifice of a relatively low number of individuals, this adaptation can ultimately optimize reproductive success for a population or a community (Rutberg 1987).
Secondly, a phenomenon known as “predator swamping” may also lead to the development of reproductive synchrony. In this model, the sheer numbers of offspring produced can confuse or overwhelm predators. As a result, the predation rate may be decreased due to predator search images becoming confused by large mixed groups of adults and young (Hamilton 1971, cited by O’Donoghue and Boutin 1995).
These first two mechanisms can be difficult to tease apart empirically, but it is undeniable that predation can have a monumental impact on the timing of reproduction. A study by O’Donoghue and Boutin (1995) measured juvenile survival rates in snowshoe hares (Lepus americanus) as a function of degree of birth synchrony. Snowshoe hares produce three litters each year and demonstrate highly synchronous reproduction: all litters in the study population were born within seven days of the mean date of parturition, regardless of the season (O’Donoghue and Boutin 1995). Behavioral observations showed that the study population was subjected to high predation pressure, as evinced by the leverets’ precocial nature and unwillingness to aggregate outside of nursing bouts. This independence and propensity to hide–rather than congregate–allow them to escape detection by predators. The study demonstrated that the juveniles born closer to the peak dates of parturition had higher survival rates than those born further from the peak dates (O’Donoghue and Boutin 1995). Thus, the degree of reproductive coordination had a large impact on juvenile survival, and thus higher reproductive success can be achieved by synchronous breeding.
Another example of the effect of predation on reproductive timing is the well-documented case of the wildebeest (Connochaetes taurinus) of the Ngorongoro Crater in Tanzania, studied by Estes in 1976 (cited by Rutberg 1987). Spotted hyenas (Crocuta crocuta) are the primary cause of mortality among wildebeest juveniles. During calving, female wildebeest form large temporary aggregations to reduce the risk of predation to individuals. The study showed that these large aggregations also experience highly synchronous birthing as a defense mechanism. The researchers demonstrated that calves born at the peak dates of parturition have a higher probability of survival to the next month than those born earlier or later than these peak dates (Estes 1976, cited by Rutberg 1987). This system clearly demonstrates the advantages that reproductive synchrony confers to a population under threat of predation.
Thirdly, reproductive synchrony may be an adaptive response to predation in that large numbers of adults in breeding condition are available for group defense of offspring. This may take either the form of active cooperative defense, in which group members collectively and physically defend their offspring, or enhanced vigilance. In colonial species particularly, synchronized breeding may heighten the possibility of detecting danger (Ims 1990b).
In fact, group vigilance may constitute enough of an advantage to drive reproductive synchrony at the community level. In a study of rock hyraxes (Procavia capensis) and bush hyraxes (Heterohyrax brucei), Barry and Mundy (2002) demonstrated that synchronized birthing allowed for heightened vigilance in these associated species. Both rock and bush hyraxes must venture above ground to bask, which elevates the risk of predation by raptors. This in turn selects for the formation of heterospecific groups to enhance vigilant behavior. The close association of these two species extends to reproductive behavior; the hyraxes show a high degree of synchronous birthing, and the two species commonly share nurseries where adults care for the young of both species (Barry and Mundy 2002). The study concluded that in the presence of offspring, the two species exhibited a higher degree of association, thus enhancing vigilance. In addition, heterospecific groups contained more juveniles than did homospecific groups, suggesting that overall reproductive fitness is higher in heterospecific groups that synchronize births. Juvenile mortality is low in the first five months after birth and highest just after weaning, when these heterospecific associations disintegrate and the young become more independent (Barry and Mundy 2002). These observations demonstrate the critical importance of heterospecific association, enhanced vigilance, and reproductive synchrony in juvenile survival.
Whether or not a species experiences reproductive synchrony is determined in part by its natural history. A combination of the prey species’ behavior and the vegetative structure of its habitat can actually drive a population under predation pressure towards highly asynchronous breeding. Ungulate species can be characterized as either “hiders” or “followers,” depending on the behavior of their neonates (Sinclair et al. 2000). “Follower” juveniles are highly precocial and are capable of trailing after their mothers within a few hours of birth. These gregarious species tend to form large aggregations as an anti-predator strategy. Follower species benefit from reproductive synchrony because the juveniles are visible and therefore vulnerable to predators. Predator swamping has been shown to be an effective strategy in many of these follower species, including topi, buffalo, and warthogs (Sinclair et al. 2000). In contrast, “hider” species tend to be territorial and solitary, and the juveniles are relatively altricial. These species tend to be widely dispersed, so temporal and spatial clustering of births is not adaptive. Their densities are too low to sufficiently satiate predators, so reproductive synchrony would cause a hider species to suffer higher predation rates (Sinclair et al. 2000). By the fourth mechanism of “predator avoidance,” these “hider” species would be expected to demonstrate asynchronous breeding as an anti-predator adaptation (Ims 1990b). For example, the distribution of births in Kirk’s dikdik (Madoqua kirkii), a hider species, does not correspond with the seasonal patterns of resource abundance; instead, births are distributed evenly throughout the year (Sinclair et al. 2000).
Mathematical models have also demonstrated that the impact of predation on the degree of synchrony is determined in part by the life history of the predator. The success of reproductive synchrony as a mechanism to reduce predation rates depends on the functional response of the predator. The functional response refers to the consumption rate of a predator in response to the density of the prey population. Prey species may benefit from synchronized breeding if the threat is from a typical specialist (type II) predator (Ims 1990b). If the pressure of predation remains constant throughout the year, a high degree of synchrony should satiate the predator during the breeding season, allowing for increased juvenile survival. In contrast, asynchronous breeding would be a more effective response to a generalist (type III) predator (Ims 1990b). Prey-switching, delayed in generalists due to the time required to develop a search image for a new prey type, should occur when prey densities are high. At the high densities generated by reproductive synchrony, a generalist predator would be able to quickly switch prey, resulting in high juvenile mortality. Asynchronous breeding would ensure that the generalist predator does not have time to develop a search image, thus maintaining a consistently low rate of predation (Ims 1990b).
An additional factor can influence this dynamic: spatial structuring can have an impact on the predator’s functional response. If synchrony is high within a single population (i.e. within a patch), predation risk from a specialist predator can be greatly decreased. If synchrony is high throughout populations (i.e. between patches as well as within patches), predation risk can be even further depressed. Thereby, reproductive synchrony can prove to be a highly effective strategy against a specialist predator (Ims 1990b). On the other hand, increased synchrony both within and between patches can increase predation pressure from a generalist.
Seasonal Resource Availability and the Timing of Reproduction
An alternative population-level explanation for the development of reproductive synchrony proposes that seasonality and cyclic availability of resources drive this phenomenon. There is an obvious advantage to coordinating the birth of offspring with seasonal resource abundance: it both enhances maternal condition and increases the availability of food for the young. In temperate ungulate species, for example, birthing early in the season may enhance offspring survival because it increases the growth period, permitting the young to bulk up and improve physical condition for their first winter (Rutberg 1987). Similarly, in tropical and subtropical ruminants, peak birthing days coincide with peaks in rainfall and vegetation (Rutberg 1987).
This idea that seasonality drives reproductive synchrony is supported by a study of topi and warthogs in the Mara-Serengeti system. If predation is the main force behind reproductive synchrony, then populations should demonstrate synchrony regardless of shifts in weather conditions (unless predator activity is also influenced by these shifts). If seasonality is the cause of synchrony, then populations should shift the timing of births to account for local disturbances such as droughts and floods (Ogutu et al. 2010). The study demonstrated that topi and warthogs were able to vary the timing of parturition by three to four months. The shift in breeding chronology was a response to extreme climatic factors: droughts were found to delay births, while floods precipitated them (Ogutu et al. 2010). These results indicate that seasonality is a very real force behind synchronized reproduction.
Another study, conducted on impalas (Aepyceros melampus) throughout the African continent, confirms this conclusion. The study found that different populations exhibited differing degrees of synchrony that correlated with the degree of seasonality in their specific habitat. That is, all study populations coordinated reproduction with respect to seasonal abundance in their respective habitats, but the timing across all populations varied due to variations in climate. Higher latitudes correspond with increased climatic seasonality, whereas lower latitudes tend to remain more climatically stable. Impalas exhibited increasing birth synchrony with increasing latitude, and thus increasing climatic seasonality (Moe et al. 2007). This study concluded that seasonality is the principal driving force behind reproductive synchrony.
Adaptive Significance of Mast Fruiting
The anti-predator explanation has also been proposed to produce the same phenomenon in plants. Also known as mast fruiting or seeding (Gochfeld 1982), reproductive synchrony in plants would occur in alternate years, thus cyclically starving and satiating predators (Kon et al. 2005). In non-mast years, plants amass enough energy to fuel a massive subsequent crop season (Gochfeld 1982). Predator populations subsequently decline as a result of diminished prey numbers during intermittent periods between population peaks. In mast years, this low predator population is easily satiated by the large seed masses produced, so a greater proportion of seedlings can survive (Kon et al. 2005). Moreover, a functional response may be operating as predators require time to develop a search image. The products of asynchronous breeding outside of mast years draw the attention of predators, inducing massive seed mortality (Silvertown 1980, cited by H. Kon et al. 2005). On the other hand, mast seeding increases seedling survival by affecting the predators’ numerical and functional responses.
If this explanation is accurate for mast seeding, then this phenomenon should occur in long-lived perennial plants that can afford to miss reproductive opportunities (Kon et al. 2005). In the Japanese beech (Fagus crenata), for example, when the total seed crop was 20 times greater than in the previous year, the rate of predation dropped significantly, by 30% (Kon et al. 2005). Another example is provided by a study of Dicymbe corymbosa, showing that this tropical monodominant experienced low rates of predation by invertebrates and fungi in mast years (7–21%), resulting in a dense uniform seedling cohort (Henkel et al. 2005).
However, there are subtle nuances in the relationship between predation and synchrony in plants. One factor that complicates this relationship is seed dispersal and pollination by seed predators. The predator swamping mechanism has also been applied to this relationship (Ims 1990b). To be efficient, pollinators or dispersal agents cannot be swamped because this leads to low germination rates. Instead, dispersal agents select for asynchronous seeding (Ims 1990b). In addition, the difference between specialist and generalist seed dispersers may also play a role in determining the degree of reproductive synchrony in plants. Specialist dispersers are more likely to be swamped by this synchrony than are generalist predators because they process more of the seedlings of the masting species (Ims 1990b).
An additional complication is interspecific competition for pollinators and dispersers. Two disparate explanations have been advanced to explain how plants optimize their dispersal by the timing of their reproductive events. The first proposes that asynchronous fruiting, or segregated fruiting phenologies, results in reduced competition for dispersers (Snow 1965, cited by Poulin et al. 1999). For example, a study conducted in Panama showed that shrubs of the genus Miconia demonstrate asynchronous fruiting, which allows avian dispersers to feed year-round (Poulin et al. 1999). The second hypothesis proposes that synchronous fruiting draws the attention of more dispersers (Rathcke & Lacey 1985, cited by Poulin et al. 1999). Multiple factors play into this dynamic, one of the most significant being the temporal abundance of frugivores as dispersers. For example, the same study by Poulin et al. demonstrated that members of the Psychotria genus exhibit mast fruiting, taking advantage of the late wet season during which migrant thrushes pass through the region (1999).
The Evolution of Reproductive Synchrony
Despite its apparent benefits, it is unlikely that reproductive synchrony developed primarily as a result of predation pressure. A few individuals showing slightly more synchronized reproduction than the rest of the population would not constitute an adequate advantage to decrease predation rates, so there would be no reason for this behavior to evolve further. Instead, it has been proposed that populations exhibiting seasonal reproduction in response to climatic patterns would subsequently gain from the anti-predator benefits conferred by reproductive synchrony (Rutberg 1987). Thus, climatic seasonality might have been responsible for the initial synchronization of reproduction, but the anti-predator advantages served to reinforce the schedule and tighten synchrony to a point that could not have been achieved by seasonal breeding alone. In effect, predation pressure accelerated the evolution of reproductive synchrony.
However, it is equally unlikely that fluctuating climate conditions were the only pressure selecting for reproductive synchrony, since many studies show a higher degree of synchrony in species than would be predicted from seasonality alone. Several ecologists have proposed that timing and synchrony of reproduction are two separate processes influenced by disparate pressures (Ogutu et al. 2010). Sinclair et al. (2000) made a distinction between “phenology” and “synchrony” that could help to clarify this problem. The first term refers to the time of year during which reproduction occurs and is most likely correlated with seasonal resource availability. The latter refers to the degree of coordination between reproductive events in a population, and is likely an anti-predator adaptation (Sinclair et al. 2000). Thus, seasonality may be the primary factor selecting for reproductive timing, while predation may serve to further modify this schedule. Timing and synchrony are two different processes that can experience selection simultaneously; thus, predation and seasonality are not mutually exclusive hypotheses.
It is also important to note a significant distinction between proximate and ultimate mechanisms. An ultimate mechanism is an adaptive force that selects for the evolution of the behavior in question. On the other hand, a proximate mechanism is a force that controls a behavior at an organismal level but may not necessarily be a driving force in its development. An example illustrates this distinction: in the greater spear-nosed bat (Phyllostomus hastatus), females live in groups attended by one male. The reproductive timing of the group is such that lactation coincides with peak food availability (Porter and Wilkinson 2000). The timing of births is not conserved across years, but the degree of synchrony is consistently high, with all births occurring within 19 days in every year of the study. The study suggests that seasonal environmental cues may dictate the timing, whereas the tight synchrony is due to social cues such as hormones. The close physical contact among females would facilitate the spread of chemical cues to synchronize reproduction (Porter and Wilkinson 2000). Thus, while seasonal resource abundance may be the ultimate mechanism selecting for synchronized reproduction, proximate social cues serve to reinforce this schedule and tighten synchrony. This same distinction may be important in differentiating between the seasonality and predation explanations.
Secondary selective factors driving the evolution of this reproductive synchrony include social elements. In the South American fur seal (Arctocephalus australis), predation may have first caused females to spatially and temporally cluster birthing (Boness and Iverson 1995). However, the behavior is also advantageous in that it can deter sexual harassment from males, which can damage maternal condition and thus reduce the probability of offspring survival. In this species, females congregate to give birth and subsequently mate. Synchronized reproduction is beneficial because the large number of available females sufficiently satiates the males, as they are occupied with their own harems. Females that are late to pup may suffer from harassment from the males since they are easier to single out (Boness and Iverson 1995). After having mated with all the females in their respective harems, multiple male fur seals will all pester this lone female. Male harassment effectively functions as a stressor that can decrease her maternal condition, thus decreasing her offspring’s probability of survival. Female lion-tailed macaques (Macaca silenus) demonstrate estrous as well as birthing synchrony, suggesting that socially mediated hormonal cues are the proximate mechanisms governing reproductive chronology (Clarke et al. 1992). Thus, while ecological factors may have been the primary forces driving this dynamic, social factors are the proximate mechanisms that reinforce it.
From these explanations regarding the origin of reproductive synchrony, it is possible to predict the proximate mechanisms on which natural selection operates to produce this behavior. If the phenomenon originated in response to seasonal climate patterns, mechanisms that likely control reproductive chronology are regular and correlated with season. These may include photoperiod, maternal nutritional status as a function of resource availability, food quality, and rainfall (Rutberg 1987). On the other hand, if reproductive synchrony evolved as a means of lowering predation rates, then the cues do not have to be linked with seasonal abundance. Cues may come from sources such as lunar cycles or social elements (Rutberg 1987). Female bison (Bison bison), for example, closely monitor the ano-genital regions of other females to time parturition in the herd (Berger 1992).
While seasonality may have been the initial driving force in the evolution of reproductive synchrony, it is likely reinforced by a host of complex, interacting factors, including social effects, local weather and topography, seasonality of resources, and predation pressure (Rutberg 1987). These mechanisms may be operating simultaneously or independently, working together to produce the phenomenon of coordinated reproduction. The degree of reproductive synchrony exhibited by any population and the adaptive advantage that it confers vary greatly but are ultimately determined by the local interplay of ecological and social forces.
Reproductive synchrony is widely regarded as an adaptive behavior due to its wide expression in a variety of organisms, including both vertebrates and seed plants. Ecologists agree that reproductive synchrony has value as an anti-predator strategy, by means of four separate mechanisms: predator satiation, predator swamping, group defense, and predator avoidance. In plants, the anti-predator theory must also take into consideration disperser and pollinator behavior. At any rate, predation pressure has been shown to drive the synchrony–or asynchrony–of reproductive events and ultimately, other community dynamics. However, predation is unlikely to be the sole factor determining reproductive coordination. Surveys of multiple taxa inhabiting differential environments indicate that reproductive synchrony is a product of multiple interplaying factors, both ecological and social.
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