Intercontinental Comparison of Fish Life History Strategies along a Gradient of Hydrologic Variability

—The flow regime is considered the primary driver of physical processes in riverine ecosystems; thus we expect that the trait composition of fish assemblages might respond similarly to hydrologic variability, even at broad spatial scales. Here, we test the hypothesis that freshwater fish life history strategies on two continents (southern United States and eastern Australia) converge along gradients of hydrologic variability and primary productivity at the drainage scale. Our results show that the fishes of the United States and Australia conform to the three-dimensional adaptive space arising from the trade-offs among three basic demographic parameters of survival, fecundity, and onset and duration of reproductive life. Species from both continents represent the endpoints in adaptive space defining the periodic (19% versus 33% for the United States and Australia, respectively), opportunistic (69% versus 52%), and equilibrium life history strategies (12% versus 15%). We found evidence that fish life history composition of drainage basins in the two continents have converged across similar gradients of hydrologic variability and productivity despite phylogenetic and historical differences. Moreover, these relationships were largely consistent with predictions from life history theory. Increasing hydrologic variability has promoted the greater prevalence of opportunistic strategists (a strategy that should maximize fitness in environmental settings dominated by unpredictable environmental change) while concurrently minimizing the persistence of periodic-type species (a strategy typically inhabits seasonal, periodically suitable environments). Our study provides a conceptual framework of management options for species in regulated rivers because life history strategies are the underlying determinants for population responses to environmental change and therefore can be used to classify typical population responses to flow alteration or mitigation via environmental flow prescriptions. * Corresponding author: [email protected] Introduction The importance of hydrologic variability for shaping the biophysical attributes and functioning of riverine ecosystems is well recognized (Naiman et al. 2008). Flow has been suggested to be the “master variable” that determines pattern and process in rivers, thus limiting the distribution and abundance of species and regulating ecological integrity (Poff et al. 1997). Natural spatial variation in the hydro84 olden and kennard logic regime is influenced by variations in climate and basin geology, topography, and vegetation, which interact at multiple spatial and temporal scales to shape the physical template upon which ecological and evolutionary processes operate in river ecosystems (Poff and Ward 1990; Bunn and Arthington 2002; Lake 2008). The natural flow-regime paradigm postulates that the structure and function of riverine ecosystems, and the adaptations of their constituent riparian and aquatic species, are dictated by patterns of intraand interannual variation in river flows (Poff et al. 1997). A rich body of literature has demonstrated that the longterm physical characteristics of flow variability have strong consequences at local to regional scales and at time intervals ranging from days (ecological effects) to millennia (evolutionary effects). Flow variability, including flood and drought events, interacts with the underlying geology to shape the river’s physical and chemical templates and constrain assemblage structure for fish (e.g., Lamouroux et al. 2002; Hoeinghaus et al. 2007; Kennard et al. 2007), stream invertebrates (e.g., Poff and Ward 1989; Vieira et al. 2004; Dewson et al. 2007), riparian plants (e.g., Nilsson et al. 1993; Naiman and Décamps 1997; Pettit et al. 2001), and riparian invertebrates (e.g., Wenninger and Fagan 2000; Lambeets et al. 2008). Adaptations to natural flow regimes include behaviors that enable insects to avoid desiccation by droughts, fish life history strategies that are synchronized to take advantage of floodplain inundation, and plant morphologies that protect roots by jettisoning seasonal biomass during floods (reviewed in Lytle and Poff 2004). There has been considerable interest in the identification of major axes of ecological strategy variation in freshwater ecosystems based on trait correlations across large numbers of species (Winemiller 2005; Olden et al. 2006; Poff et al. 2006; Verberk et al. 2008; Frimpong and Angermeier 2010, this volume). Species traits may be intercorrelated through physiological constraints, trade-offs (i.e., investments in one trait leaving fewer resources available for investment in another), or spin-offs (i.e., investments in one trait reduce costs or increase the benefits of investment in another trait), resulting in the creation of life history strategies or tactics represented as sets of coevolved traits that enable a species to cope with a range of ecological problems (Stearns 1992). Comparative studies from a diverse array of fishes in marine and freshwater systems have independently identified three primary life history strategies that represent the endpoints of a triangular continuum arising from essential trade-offs among the basic demographic parameters of survival, fecundity, and onset and duration of reproduction (Winemiller 1989, 1992; Winemiller and Rose 1992; Vila-Gispert and Moreno-Amich 2002; Vila-Gispert et al. 2002; King and McFarlane 2003; see Figure 1). Winemiller and Rose (1992) synthesized these life history trade-offs and proposed the following characteristic biological and habitat environmental attributes associated with the three life history strategies. Periodic strategists are large-bodied fishes with late maturation, high fecundity per spawning event, and low juvenile survivorship (i.e., no parental care) and typically inhabit seasonal, periodically suitable environments with large-space spatial (patchiness) and temporal (seasonality) heterogeneity. Opportunistic strategists are small-bodied fishes with early maturation, low fecundity per spawning event, and low juvenile survivorship and typically inhabit habitats subjected to frequent and intense disturbances. Equilibrium strategists are small to medium-bodied fishes with moderate maturation age, low fecundity per spawning event, and high juvenile survivorship (i.e., provides parental care) and typically 85 intercontinental comparison of fish life histories Figure 1. Triangular life history model depicting environmental gradients selecting for endpoint strategies defined by optimization of demographic parameters generation time, fecundity, and juvenile survivorship (modified from Winemiller 2005). Example species from the study regions and representative hydrologic regimes expected to favor each life history strategy are illustrated. Australian fish illustrations by B. J. Pusey; U.S. fish illustrations freely available on the Internet. inhabit environments with low variation in habitat quality and strong biotic interactions. The demographic parameters discussed above are direct reflections of the ways in which fish allocate energy to reproduction, and the three life history strategies of the continuum can be interpreted as being adaptive with respect to relative variability and predictability of temporal and spatial variation in abiotic environmental conditions, food availability, and predation pressure (Winemiller 2005). Hydrological variability plays a dominant role in shaping physical processes in riverine ecosystems, and a number of recent studies have supported the association between hydrology and fish life history strategies. Tedesco and Hugueny (2006) found that regional climate (presumably related to hydrologic variability) induced greater population synchrony of periodic fish species in rivers of the Cote d’Ivoire (Africa) compared to equilibrium species. By comparing trends in native and nonnative species distributions among fish life history strategies in the lower Colorado River basin (USA), Olden et al. (2006) found that century-long modifications in flow variability have likely promoted the spread of nonnative equilibrium strategies (favored in constant environments) while leading to greater distributional declines of native species located along the periodicopportunistic continuum (strategies favored in more unpredictable and variable environments). Tedesco et al. (2008) found higher proportions of periodic species in highly seasonal drainage basins of western Africa (e.g., rivers with short and predictably favorable seasons), whereas more hydrologically stable basins with a wet season of several months 86 olden and kennard were dominated by equilibrium strategists. Collectively, these studies (and others) suggest that the distributions of freshwater fishes are shaped, at least in part, by interactions between life history strategies and patterns of predictability and variability in hydrologic regimes. Enhancing our mechanistic understanding of the functional linkages between environmental drivers of fish species distributions will provide a foundation for predicting existing and future impacts of altered flow regimes, invasive species, and land-use change. Gaining this knowledge is predicated upon examining how fish assemblage structure varies in response to flow variability and testing the generality of these relationships across large spatial scales. By using the “habitat templet” concept proposed by Southwood (1977), and applied to riverine systems by Townsend and Hildrew (1994), we predict that because life history strategies are synchronized with long-term hydrologic dynamics, even geographically distant regions will presumably favor the persistence of species with similar traits if subjected to similar historical flow regimes. If the functional characteristics of organisms and communities are predictable from features of their environment, then convergence in these characteristics across regions implies the existence of key, repeated evolutionary mechanisms responsible for these relationships (Schluter 1986). Community convergence driven by similar environmental selective forces would be supported by observations of similar relationships between spatial variations in community life history composition along environmental gradients (Lytle and Poff 2004). In the present study, we explore this question by providing an intercontinental examination of patterns in fish functional composition across a gradient of hydrologic variability and productivity in the southern United States and eastern Australia, focusing on the opportunistic-periodic-equilibrium trichotomy. The freshwater fish faunas differ strikingly between the two regions, with the U.S. fauna being extremely diverse and with low endemism in comparison to the comparatively depauperate and highly endemic Australian fauna. Our primary objective was to test the hypothesis that the relationship between fish life history patterns, hydrologic variability and net primary productivity (NPP) in the United States and Australia is concordant with predictions from life history theory, as proposed by Winemiller (1995, 2005) and McCann (1998) (Figure 1). Specifically, by virtue of their small size and rapid turnover rates, we predict that opportunistic species should maximize fitness (and thus be more prevalent) in drainage basins characterized by productive and frequently disturbed habitats (i.e., high hydrologic variability and high NPP). By contrast, periodic and equilibrium strategists are predicted to be more common in drainage basins exhibiting low-flow variability and either more productive habitats for periodic strategists (i.e., low hydrologic variability and high NPP) or less productive habitats for equilibrium strategists (i.e., low hydrologic variability and low NPP). For periodic strategists this may be seen as a consequence of the storage effect (i.e., long life stage buffers times of low recruitment: Warner and Chesson 1985) and high annual fecundities, and for equilibrium strategies as a result of low adult mortality rates that enable them to survive on lower resource biomass (McCann 1998). By taking a functional approach, our study underscores the theoretical expectation that species traits promoting local persistence will change along environmental gradients, thus facilitating the comparison of regions separated by large geographic distances and aiding the development of broadly applicable generalizations regarding patterns of fish life history strategies. If fish species show similar 87 intercontinental comparison of fish life histories ecological responses to the same environmental challenges irrespective of their ancestry, we expect that hydrologic variability has selected for similar community patterns in fish life history strategies despite originating from completely different regional species pools at opposite sides of the world.