The role of reproductive synchrony in the colonization potential of kelp

Ecology, Dec, 1997 by Daniel C. Reed, Todd W. Anderson, Alfred W. Ebeling, Michele Anghera

INTRODUCTION

Varying degrees of reproductive synchrony in propagule production and release are widespread among plants and animals in both terrestrial and marine habitats (reviewed in Ims 1990a, Santelices 1990, Robertson 1991, Silvertown and Doust 1993, Morgan 1995, Clifton 1997). The numerous hypotheses proposed to explain these phenomena fall into two broad categories: proximate causes, which explain the immediate factors that cause synchrony (e.g., climatic events and fluctuations in resources; Norton and Kelly 1988, Barry 1989, Sork et al. 1993), and ultimate causes, which explain the evolutionary advantages incurred by synchrony (e.g., reduced predation and enhanced fertilization; Janzen 1971, 1976, Babcock et al. 1986, Allen and Platt 1990, Ims 1990b, Smith et al. 1990, Koenig et al. 1994). In any particular case there may be multiple causes for reproductive synchrony, and the predicted advantage of a particular cause depends on the ecological setting in which populations reproduce (Ims 1990a).

Both limited and extended dispersal of propagules have been suggested as ultimate causes of reproductive synchrony in plants and animals (see Kelly 1994, Morgan 1995 for reviews). Such synchrony may increase dispersal distance by attracting animal vectors (Christensen and Whitham 1991) or by taking advantage of physical conditions that promote dispersal (Nygan and Price 1983, Salmon et al. 1986). By contrast, the synchronous release of propagules during conditions that promote retention results in limited dispersal (Naylor 1976, Berry 1982). Although dispersal may provide a release from competition associated with remaining near the parental site, it exacts a formidable cost in uncertainty of propagules reaching a favorable habitat. In general, limited dispersal is expected in harsh environments where localized disturbance is rare (e.g., dry deserts in the case of annual plants), and extended dispersal is expected in relatively favorable environments that are characterized by frequent localized disturbances (Levin et al. 1984).

Spatial and temporal heterogeneity in the environment favors the evolution of mechanisms such as propagule dispersal that allow sedentary species to escape locally unfavorable conditions (Levin 1976, Vance 1980). An alternative strategy to dispersal for dealing with adverse environmental conditions is propagule dormancy, which allows for escape in time from locally unfavorable conditions (Venable and Lawlor 1980, Levin et al. 1984). For example, some shrubs possess hard coated seeds that lie dormant in the soil until a fire passes. Rather than being consumed by fire, the seeds are scarified, which enables them to absorb water and germinate in a nutrient rich and competition free environment (Agee 1993). Thus, dispersal and/or dormancy are key elements that promote the recovery of local populations following a damaging disturbance. The evolved level of dispersal is expected to be inversely related to that of dormancy (Cohen and Levin 1987).

In nearshore coastal zones, disturbance from water motion, grazing, and disease is frequent and variable in extent ranging in area from a few square meters to hundreds of square kilometers (Paine and Levin 1981, Connell and Keough 1985, Sousa 1985, Jangoux 1987, Tegner and Dayton 1987, Dayton et al. 1992). Thus, it is not surprising that many nearshore marine organisms produce planktonic propagules capable of widespread dispersal (Strathmann 1974, Scheltema 1977, Doherty and Williams 1988, Keough 1988, Caley et al. 1996). Widespread dispersal affords local populations greater resilience to disturbance, because their recovery is not dependent on the local production of propagules (Roughgarden et al. 1985, Roughgarden et al. 1988, Gaines and Lafferty 1995). Interestingly, many species that seem to have rather limited dispersal (based on their production of relatively short-lived propagules) can rapidly colonize relatively distant areas that have been disturbed (Chapman 1981, Davis et al. 1982, Svane 1983, Keough 1984, Ebeling et al. 1985, Young 1989, Ambrose et al. 1993, Worcester 1994). Various hypotheses have been proposed to explain this phenomenon including the passive drifting of detached individuals or reproductive fragments (Dayton 1985, Paine 1988, Worcester 1994). The hypothesis evaluated in this paper is that synchrony in propagule release may allow organisms with otherwise limited dispersal to take advantage of periodic conditions that promote greater transport.

Some of the best documented examples of rapid recolonization of seemingly distant sites by organisms perceived to have limited dispersal can be found in large brown seaweeds known as kelps. Kelps are dominant features of subtidal temperate reefs worldwide, and their populations undergo relatively frequent and unpredictable local extinctions and recolonizations (Jones and Kain 1967, Mann 1977, Choat and Schiel 1982, Dean et al. 1984, Ebeling et al. 1985, Harrold and Reed 1985, Miller 1985, Dayton et al. 1992). Recovery following local extinction of kelp populations is often rapid and can occur over large areas of reef (Harris et al. 1984, Ebeling et al. 1985, Dayton and Tegner 1989). Such rapid colonization over large areas results either from the large-scale immigration of propagules via extended dispersal following the disturbance or widespread recruitment of dormant microscopic stages that survive the disturbance.