Populations, metapopulations, and the open‐closed dilemma: the conflict between operational and natural population concepts

When we sent Alan Berryman a first draft of this essay for review, he sent us back an unpublished manuscript that discussed similar questions and possible solutions (Berryman 1999, 2002). Consequently, we decided to submit these two essays together in the hope of stimulating ecologists to think about how they define and use the population concept. The population concept is central to ecology and evolution. The definition of a population represents a fundamental problem for understanding ecological dynamics, and it has wide implications for applied issues such as management and conservation. Further, the population concept merges evolution and ecology, because interactions between nonspecific individuals, as well as between species (enemies, mutualists, etc.) and the environment are reflected in survival and reproduction rates. These rates determine population dynamics and thus represent the basic elements of natural selection and microevolutionary forces (Futuyma 1986). Therefore, populations are faced with evolutionary and ecological forces, both operating through demographic processes (Caswell 1989, Futuyma 1986). Consequently, the way ecologists define populations may change drastically the theoretical framework used to understand nature, leading to divergent views on the dynamics of ecological systems, such as the non-equilibrium versus equilibrium paradigms (Berryman 1987). A review of current ecological textbooks reveals that the population concept is usually defined very broadly or from the observer's perspective (Berryman 1981, Dodson et al. 1998), where the ultimate criterion refers not to biological variables but rather to undefined or dimensionless spatial aspects such as "area", "place", or so. Despite its plasticity to account for different research objectives this type of definition may not be useful to represent natural populations, and to develop theoretical and empirical tools for understanding these biological entities. In particular, a common problem with the population concept is how to distinguish the area and spatial structure of a population (Yablokov 1986), which is in close relation with the problem of what is an appropriate scale for studying natural populations. The difficulty in defining a population has been augmented due to the widespread use of the "metapopulation" term (Hanski 1997, Hanski and Gilpin 1999, but see Hastings and Harrison 1994 for criticisms). As also noted by Berryman (see companion paper), in most metapopulation studies there is no clear definition of a "local population" or "metapopulation" because the concept of "population" is not explicitly defined. Even in the first formal proposition by Levins (1969), the metapopulation was conceived as a suite of dimensionless units, thus emphasizing operational rather than natural criteria. While the heuristic and practical value of the metapopulation frame can hardly be disputed when applied to patch dynamics, its terms and definitions do not necessarily convey more biological reality than that implicitly assumed by the researcher. On the other hand, an increasingly popular notion is leading to additional difficulties. Many studies on marine intertidal systems emphasize the "openness" of such populations as a specific property that renders them different from other (especially terrestrial) populations, and consider the latter as a paradigmatic case of closed systems (Roughgarden and Iwasa 1986, Roughgarden et al. 1994, Caley et al. 1996). In fact, some authors (e.g. Roughgarden et al. 1985) propose that because most sessile marine species release their larvae to the ocean, open models that incorporate the arrival of larvae from other adult populations should describe their populations. Such a framework is considered more realistic than the stock-recruitment approach (Roughgarden et al. 1985, 1988, Caley et al. 1996). In this context, "openness" is seen as the primary condition of marine benthic populations when observed at local scales (Gaines and Roughgarden 1985) and, as a conse-