Stress
2. Organism responses to stress
Having considered the types of stresses which can operate in intertidal environments, we now look at how organisms respond to these in more detail.
Read the abstract of an early study by Oglesby 1969 on intertidal worms: http://icb.oxfordjournals.org/cgi/content/abstract/9/2/319. Note: When this paper was published research into these issues was, relatively speaking, in its infancy. One of the landmark papers in intertidal ecology, Connell (1961), was only published a few years earlier. Part of the abstract says: "In response to rapid lowering of salinity, worms gain water and lose salts, these processes combining in diluting the internal fluids. ... Mechanisms involved in hyperosmotic regulation include active transport of salts (demonstrated in Nereis diversicolor), reduction of the permeability of the body surface to salts and perhaps to water, and perhaps production of hypo-osmotic urine. Sipunculids can tolerate considerable loss of water from dehydration and concomitant increases in osmotic concentration of the body fluids. It is suggested that worms exposed to significant tidal variations in salinity may seldom be in osmotic equilibrium with their external medium." Thus, there is evidence of physiological mechanisms to deal with the stresses created by varying salinity, along with an increased ability to cope with changes.
Read the abstract for the study by Stephen Garrity on the behaviour of ten species of gastropod in Panama.
Note: "Newell (1976) discussed several ways marine organisms may deal with physical stress in the intertidal zone. They include microhabitat selection, and structural and physiological adaptations. This paper supports Newell's ideas. ... The present study demonstrates the importance of an additional 'strategy' involving well-defined, limited activity periods and specific behaviours." Garrity's ingenious observations and experiments reveal the complex ways in which these, relatively simple, animals coped with the harsh physical stresses occurring in the tropical intertidal environment. It is also interesting to note that, perhaps in contrast to popular opinion (at least at the time), it is the tropics which were shown to be physically harsh, compared to the more "benign" temperate regions. Finally, note that Garrity offers his results as a example of the importance of physical (abiotic) processes: intertidal ecology was, at the time, to some extent dominated by the idea that biological (biotic) processes – such as predation and competition – were the major organising forces.
Predation and competition are examples of "negative interactions": one organism benefits at the expense of another. Some ten years ago, Bertness, and colleagues, started to draw attention to the importance of "positive interactions" in intertidal communities: interactions in which "neighbouring organisms benefit on another by buffering potentially limiting physical stresses". Further, they noted that these might be more common, and important, in physically stressful environments.
Bertness and colleagues in 1999 studied ‘Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place’. The abstract reads: "To explore how climate may affect the structure of natural communities, we quantified the role of thermal stress in setting the high intertidal borders of the acorn barnacle, Semibalanus balanoides. At sites north and south of Cape Cod, a major faunal and thermal boundary on the east coast of North America, we examined the interacting effects of thermal stress and recruit density on individual survivorship. At hotter southern sites, particularly in bays, high intertidal barnacle survivorship was enhanced by experimental shading or by neighbors which ameliorate heat and desiccation stresses. In contrast, at cooler northern bay and coastal sites, neither shading nor group benefits increased barnacle survival, and mortality patterns were driven primarily by predators with largely boreal distributions. Our field results, like recent laboratory microcosm studies, suggest that predicting even simple community responses to climate change may be more complex than is currently appreciated."
Note: The authors conclude by making the point that "predicting even simple community responses to climate change may be more complex than is currently appreciated". This is because changing stress may change the very nature of interactions among organisms.
Further examples of positive interactions from soft-bottom environments such as salt marshes, are described in the paper by Bertness and Leonard (1997) The Role Of Positive Interactions In Communities: Lessons From Intertidal Habitats. The abstract reads: Positive interactions that result from neighbors buffering one another from stressful conditions are predictably important community forces in physically stressful habitats. Here, we examine the generality of this hypothesis in marine intertidal communities. Intertidal communities have historically played a large role in the development of community ecology since they occur across pronounced physical gradients and are easily manipulated. Positive interactions, however, have not been emphasized in studies of intertidal communities.
We first review studies of intertidal marsh plant communities that suggest that positive interactions play a dominant role in the structure and dynamics of these common assemblages. We then present the results of an experimental manipulation on New England rocky shores that suggests that group benefits are as important in maintaining the upper intertidal limits of dominant spaceholders on rocky shores as the negative forces of competition and predation are in maintaining lower distributional limits.
We conclude by discussing the generality and implications of our results. We argue that biogeographic biases have limited appreciation of the role played by positive interactions in intertidal communities. Most of the work that has formed the foundation of marine intertidal ecology was done in cool temperate habitats, whereas positive interactions driven by the amelioration of thermal or desiccation stresses are likely more important in warmer climates. We further argue that many important positive feedbacks operate at large spatial scales, not conducive to experimental study, and thus have escaped critical attention and general acceptance. We suggest that recognizing the role of positive interactions in communities may be key to understanding population and community processes in physically stressful habitats, many large-scale landscape processes, and uncovering long-suspected linkages between biodiversity and community stability.
The final example in this section is concerned with changes in variability, in contrast to changes in the mean, in stress. Read the abstract from the study by Benedetti-Cecchi and colleagues, done in the Mediterranean, on the effects of stress from aerial exposure. The abstract reads: Extreme climate events produce simultaneous changes to the mean and to the variance of climatic variables over ecological time scales. While several studies have investigated how ecological systems respond to changes in mean values of climate variables, the combined effects of mean and variance are poorly understood. We examined the response of low-shore assemblages of algae and invertebrates of rocky seashores in the northwest Mediterranean to factorial manipulations of mean intensity and temporal variance of aerial exposure, a type of disturbance whose intensity and temporal patterning of occurrence are predicted to change with changing climate conditions. Effects of variance were often in the opposite direction of those elicited by changes in the mean. Increasing aerial exposure at regular intervals had negative effects both on diversity of assemblages and on percent cover of filamentous and coarsely branched algae, but greater temporal variance drastically reduced these effects. The opposite was observed for the abundance of barnacles and encrusting coralline algae, where high temporal variance of aerial exposure either reversed a positive effect of mean intensity (barnacles) or caused a negative effect that did not occur under low temporal variance (encrusting algae). These results provide the first experimental evidence that changes in mean intensity and temporal variance of climatic variables affect natural assemblages of species interactively, suggesting that high temporal variance may mitigate the ecological impacts of ongoing and predicted climate changes.
Note: These results add an additional potential level of complexity: the effects of stress may change – reverse! – if the variability changes. They say: "It is reasonable to expect that temporally variable events that operate with high intensity on average, have much larger effects on natural populations than events that operate with the same level of temporal variance, but with lower mean intensity."
A thread developing in the second series of papers is that of going beyond understanding how organisms respond to stress to being able to predict how communities will change in response to the changing, potentially increasing, stress from climate change. The complexity of the organism's responses and interactions, even in relatively simple intertidal communities, reveals the challenging nature of this task.
Natural variability and forecasts
Early thinking about nature and ecosystems tended to focus on stability; along the lines of the ideas summed up in the phrase "the balance of nature". Wikipedia refers to this as a "pseudoscientific fallacy" but this is not really correct; rather, the idea is one which is simply not consistent with the natural world revealed by observations and experiments.
Read about natural variability in coastal ecosystems: Ducrotoy (2021) http://www.coastalwiki.org/wiki/Natural_variability_and_change_in_coastal_ecosystems
Climate change is frequently considered in terms of changing levels of stress and disturbance (considered for marine systems in the next topic in this module). Being able to predict the consequence of these changes, should enable us to better manage them. Read a review of the current reliability of predictions of the effect of climate change on biodiversity by Botkin et al. (2007).
Note: The authors refer to the "Quaternary conundrum" that "during recent ice ages surprisingly few species became extinct". Their discussion of this, and possible explanations for it, highlight some of the difficulties involved in thinking about future change.
Other stresses
The discussion here has focussed primarily on temperature stress in intertidal environments. This does not mean, of course, that this is the only kind of stress that is important in marine systems or that this is always the most important stress. Organisms may be stressed by changes in salinity, as in the second article mentioned above, changes in oxygen levels and changes in other physical variables. An issue receiving much attention in recent years is changes in the ocean's acidity due to increasing carbon dioxide in the atmosphere (briefly discussed in Wikipedia). I chose to focus the discussion here primarily on temperature because temperature, and changes in temperature, are key elements of both terrestrial and aquatic systems. And, partly for this reason, there is a history of work on temperature in intertidal systems.
Activity 9
Complete the activity to test your understanding of these issues.
References
- Bertness, M. D., G. H. Leonard, et al. (1999). Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place. Oecologia 120: 446-450. Available online.
- Botkin, D. B., H. Saxe, et al. (2007). Forecasting the Effects of Global Warming on Biodiversity. BioScience 57: 227-236. Available online.
- LARRY C. OGLESBY, Salinity—stress and Desiccation in Intertidal Worms, American Zoologist, Volume 9, Issue 2, May 1969, Pages 319–331, https://doi.org/10.1093/icb/9.2.319
- Töpke, Katrien (2021): Rocky shore habitat. http://www.coastalwiki.org/wiki/Rocky_shore_habitat