Individual variation and interactions explain food web responses to global warming

Abstract

Understanding food web responses to global warming, and their consequences for conservation and management, requires knowledge on how responses vary both among and within species. Warming can reduce both species richness and biomass production. However, warming responses observed at different levels of biological organization may seem contradictory. For example, higher temperatures commonly lead to faster individual body growth but can decrease biomass production of fishes. Here we show that the key to resolve this contradiction is intraspecific variation, because (i) community dynamics emerge from interactions among individuals, and (ii) ecological interactions, physiological processes and warming effects often vary over life history. By combining insights from temperature-dependent dynamic models of simple food webs, observations over large temperature gradients and findings from short-term mesocosm and multi-decadal whole-ecosystem warming experiments, we resolve mechanisms by which warming waters can affect food webs via individual-level responses and review their empirical support. We identify a need for warming experiments on food webs manipulating population size structures to test these mechanisms. We stress that within-species variation in both body size, temperature responses and ecological interactions are key for accurate predictions and appropriate conservation efforts for fish production and food web function under a warming climate. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.

Keywords: body growth; climate change; fish production; population size structure; predator–prey; trait variation.

Figure 1.

(a) Warming-induced responses of individuals, populations and food webs emerge from temperature-dependent rates of individual-level processes. Rates of food intake and metabolism depend on both individual body size and temperature, and size, in turn, on acquired net energy allocated to growth. Thus, warming-induced changes in these rates result in changes in the composition of populations and food webs, which feed back to affect individual growth, survival and reproduction. Such individual-level responses result from feedbacks from warming-induced shifts in population size structure (feedback indicated by 1 in (a)), intraspecific competition (2), interspecific competition (3) and predation (4). These feedbacks couple individual-level processes (yellow) to population (blue) and food web (red) dynamics, and thereby also impact how warming affects bottom-up (e.g. 3) and top-down (e.g. 4) regulation in food webs. (All species are size structured, but for clarity, we have illustrated this only for a focal species, and not for its predator, competitor and resource species.) (b) Examples of predicted, observed and experimentally tested responses to higher temperatures in aquatic systems at the levels of individuals, populations and food webs. Direction of responses is indicated by +, −, 0 or a bent arrow for hump-shaped responses. Numbers (in grey) correspond to citations listed below, where type of aquatic organism is indicated in brackets for observational and experimental studies; F = fish, Z = zooplankton, P = phytoplankton, I = insects, M = microbes, O = other: 1. [7] [F], 2. [4] [F], 3. [17], 4. [18], 5. [22] [F,Z,O], 6. [23] [M], 7. [24] [F,Z,O], 8. [25] [F], 9. [26], 10. [8] [F], 11. [27] [F,P,O], 12. [28] [F,Z,P,O], 13. [29] [M], 14. [30] [F], 15. [16], 16. [31] [ZP], 17. [32], 18. [33] [F], 19. [34] [F], 20. [35] [F], 21. [36] [F], 22. [15] [F], 23. [37] [O], 24. [38] [F], 25. [13] [I], 26. [39] [F], 27. [40] [F], 28. [41] [F], 29. [42] [F], 30. [43] [F], 31. [44] [F], 32. [45] [F], 33. [46] [I], 34. [3] [Z,P], 35. [47] [F], 36. [21], 37. [48], 38. [49], 39. [50] [I,O], 40. [51] [Z,P], 41. [52] [F], 42. [6], 43. [53], 44. [54] [P], 45. [55], 46, [56], 47. [57], 48. [58].

Figure 2.

Feedbacks between size-specific individual responses to warming and population size structure and biomass. Example of warming effects on European perch (Perca fluviatilis), where (a) size-specific effects of warming on individual energy acquisition (black lines and circles) and use (grey lines) in small (full lines and filled circles) and large individuals (hatched lines and open circles) influence (b) body growth responses to warming, being different for small (full lines, circles) and large (hatched lines, triangles) perch individuals in the whole-ecosystem heating experiment (i) and in the lake temperature gradient study ((ii) and (iii)), and subsequently their (c) mean size-at-age ((i): the heating experiment, (ii) and (iii): the lake gradient). This affects (d) population size structure; (i,ii) show catch in numbers per unit effort per length class in the heating experiment (ii) and control area (i) and mean body size (in mm) for year 1984 and 2003 is inserted as text, in (iii, iv) black dots indicate perch in the lake temperature gradient, and coloured dots the whole-ecosystem experiment in heated (red) and control (blue) areas 4 (open circles) or 23 years (filled circles) after the onset of heating. Changes in (e) population biomass production over temperature result from responses in individual body growth at size (b) and numbers of individuals at size in the population (d), and lead to variation in (f) population biomass with temperature. The total biomass (f) and size composition (d) of individuals in the population impact their (g) prey at lower trophic levels (in addition to the direct influence by temperature on prey individuals). The amount of prey and its variation across temperature (g), in turn, influence the food intake rate of individual consumers (a). (i) in (b,c) are redrawn from Huss et al. [7], while (ii) and (iii) in (b,c), (iii) and (iv) in (d), and (e,f) are redrawn from Van Dorst et al. [4].

Figure 3.

Warming impacts on predator–prey food chains depend on within-species variation (here individual variation in predation risk). Food chain models that (a) ignore within-species variation predict that warming will lead to gradual declines in top-predators and intermediate consumers (as well as resources, when these are also directly impacted by temperature), whereas a model that (b) accounts for within-species variation in size and corresponding vulnerability to predation in intermediate consumers, demonstrates that warming can lead to alternative stable states in the food chain and sudden predator collapses. In both cases, warming weakens top-down control owing to bottom-up effects of declining resources and a stronger warming-induced decrease in net energy gain of top-predators than of their prey, the intermediate consumer. However, when predation is size-dependent (b), weakened top-down control with warming can instead lead to a decrease in the prey that is vulnerable to predation (in b: small life-stage of the intermediate consumer), and collapse of top-predator populations owing to a lack of prey (right-most food web illustration in b). (Online version in colour.)