Species interactions are some of the major drivers of ecological communities, yet few studies and models have incorporated such biotic interactions (Gilman et al. 2010). Climate change will have far-reaching effects on such interactions (Traill et al. 2010; Wernberg et al 2012), but because species respond differently to climate stressors, it will be a huge challenge to predict what future communities might look like (Davis et al. 1998). The structure of ecological communities (abundances, species diversity, species identity) lies at the basis of how ecosystems function, how productive they are, and the degree to which they recover from disturbances (Dossena et al. 2012). Therefore, there is an urgent need to improve our understanding of the ways in which global change might alter interspecific interactions, how this could directly affect food webs or other community members, and how this will ultimately affect the species diversity and functioning of ecosystems.
The study of Milazzo et al. (2013) is unique because it combines the results from field surveys, fish abundance manipulations in mesocosm experiments, and observations on fish behaviour. The authors first studied the present-day distribution of two species of co-occurring fish species (wrasses) in the Mediterranean Sea along a latitudinal gradient of almost 9°. Both species selected algal habitat along this gradient, but the warm-tolerant, range-expanding species was more common at lower latitudes, while the opposite was true for the cool-water species. They also observed that only the cool-water species was found in sub-optimal seagrass habitat, and that this trend intensified at lower latitudes. This pattern suggests that the cool-water species is displaced from its optimal algal habitat by the more tolerant and northward-moving sympatric species. This observation formed the basis for manipulative experiments to elucidate the underlying mechanisms. Unlike many fine-scale studies, large mesocosm tanks (50 m2 surface area) containing algal and seagrass habitats were used, making the set-up much more realistic. Choice tests for both species separately confirmed the field observation that algal habitat was preferred over seagrass habitat. Testing both species together and manipulating the density of the warm-tolerant species alone, it became evident that the cool-water species occupied both habitats (instead of only algal habitat) at roughly similar densities and for similar periods. However, at elevated water temperature, as projected for the end of this century, the cool-water species was displaced completely to inferior seagrass habitat, but only beyond a threshold of a three times higher density of the warm-water species than the cool-water species. In addition, the cool-water species altered its behaviour in seagrass by showing more resting activity, perhaps due to metabolic costs of higher temperatures and a reduced metabolic scope.
The results of the Milazzo et al. (2013) study build to provide a mechanism that explains the pattern first quantified by underwater visual census with experiments that study various underlying causes. The incorporation of density-dependent processes into this climate change-related experiment is not only realistic (as it mimics the increasing density of a range-extending species) but also key to the conclusions, because no effects from climate stress were observed when the warm-adapted species was below a certain density. One potential caveat is that no control experiment for density dependence was done for the cool-water species alone, so it is possible that habitat selection seen at the highest densities was due partly to an increased fish density overall as well as addition of the competing warm-water species. Nevertheless, no displacement was observed at elevated competitor densities under present-day conditions, raising an important question about studies that have found a lack of an effect from warming: is the interpretation of a lack of effect real, or is the lack of an effect due to the study operating below density-dependent thresholds at which species interactions become evident? This issue complicates any advancement in our understanding of potential future species displacement, as we still know little about which species will dominate at which densities as a result of climate stress and range extensions. Clearly, the relative densities of animals in future species communities will determine how ecosystem function and services will be affected (Harborne & Mumby 2011; Simpson et al. 2011).
One aspect that did not receive detailed attention in this study is the mechanism of habitat displacement. Competition for space can occur during early life stages through higher recruitment or survival of one species over the other (Svensson et al 2006), but also at later life stages through behavioural processes such as aggression or territoriality (Nilsson et al. 2012). It is important to understand how such displacement affects life-history traits of the species involved. Although the authors argue that feeding is more optimal in algal than seagrass habitats, it is unclear to what degree fitness is affected in seagrass habitat through alterations in net food intake, body condition, tissue growth and reproductive success, and which potential trade-offs exist by occupying one habitat over the other (Grol et al. 2011). Likewise, it is important to consider that the species’ responses to climate stressors are not static; some species will be better at adapting or acclimatizing to rapidly changing seawater conditions than others (Donelson et al. 2012), leading to alterations in interspecific interactions (Grigaltchik et al. 2012) that in turn affect the degree of climatic forcing of community composition (Ohlberger et al. 2011).
While the Milazzo et al. (2013) study provides good evidence of how two species might interact under future climate conditions resulting in a readjustment of their habitat occupancy, we are still far from understanding the composition of future communities. The matter is complicated because communities usually consist of many species. Aside from direct interspecific interactions between two species, intraspecific interactions, predator–prey interactions and indirect multispecies interactions (e.g. through mutual predators) have a strong effect on the outcome of community structure (Davis et al. 1998; Harley 2011). Depending on the ecological role (e.g. top predator, keystone species) that climate-affected species play in local food webs, habitat displacement could have cascading effects on entire communities (Kratina et al. 2012). To complicate matters, community structure of the system or locality of interest might not be stable through time due to natural disturbances, while fluctuations in larval settlement, survival rates and food abundance could affect their persistence in time (Lande 1993). Finally, the species themselves also form a dynamic component, changing as a function of invasive and range-extending species that create novel interactions in recipient systems (Urban et al 2012). Currently, there is a large gap in studies that have added these complex interactions in their design, but an understanding of such processes is needed to make realistic predictions of potential shifts in community structure and food-web interactions, both of which have implications for biodiversity, habitat productivity and ecosystem resilience.
Of course, environmental stressors often act in concert (Bellard et al. 2012). Due to increasing climatic and anthropogenic effects on marine ecosystems, few systems remain that are unaffected to some degree of eutrophication, habitat destruction or fragmentation, pollution, anthropogenic noise and overfishing (Jackson 2008), and most (or all) will be affected by global warming and ocean acidification (Hooper et al. 2012). Thus, it is critical to elucidate the independent as well as interactive effects of multiple stressors. Simple outcomes will probably not be the case as stressors might act in an additive, synergistic, antagonistic or cumulative manner (Tylianakis et al. 2008).
As Milazzo et al. (2013) briefly discuss, the habitats within which multispecies interactions play out are themselves also likely to be affected (Jackson 2008; Connell & Russell 2010). The interplay of changing communities within habitats of changing quantity and quality complicate matters and will make predictions of future community structure extremely difficult, especially as different species show different habitat dependencies (Preston et al. 2008). Due to strong animal–habitat interactions (Eklöf et al. 2012), any climate-related changes in habitat area or quality will have a feedback effect on its occupants (Wernberg et al. 2013). Clearly, mathematical models need to be developed or adjusted to incorporate such complex species-species and species–habitat interactions, while capturing natural variability in environmental and biotic factors. Nevertheless, by taking a two-species approach, Milazzo et al. (2013) provide an important contribution to our understanding of how interspecific interactions might affect animal communities under future climatic conditions, and specifically how increased competition from range-extending species could affect species persistence in habitats at higher latitudes.