Ocean Of Pdf.org

[Brian Scarano]

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A primary response of many marine ectotherms to warming is a reduction in body size, to lower the metabolic costs associated with higher temperatures. The impact of such changes on ecosystem dynamics and stability will depend on the resulting changes to community size-structure, but few studies have investigated how temperature affects the relative size of predators and their prey in natural systems. We utilise >3700 prey size measurements from ten Southern Ocean lanternfish species sampled across >10 of latitude to investigate how temperature influences predator-prey size relationships and size-selective feeding. As temperature increased, we show that predators became closer in size to their prey, which was primarily associated with a decline in predator size and an increase in the relative abundance of intermediate-sized prey. The potential implications of these changes include reduced top-down control of prey populations and a reduction in the diversity of predator-prey interactions. Both of these factors could reduce the stability of community dynamics and ecosystem resistance to perturbations under ocean warming.

Global warming represents a major threat to the structure and functioning of ecosystems. One possible consequence of rising temperatures is a decrease in body size across many species and communities1. At the individual level, warming alters the physiology of organisms and is likely to reduce body sizes within populations as organisms attempt to maintain metabolic functioning1,2. At the community level, warming may alter assembly processes through environmental filtering, competition, or trophic interactions, which may result in communities dominated by smaller-bodied species1,3. The subsequent impacts on population abundances and species interactions can drive changes to structure and function at the ecosystem scale4. Aquatic ectotherms such as fish are particularly susceptible to temperature-induced reductions in body size, due to the lower rates of oxygen diffusion in water and the energetic costs associated with maintaining water flow over surfaces5. Additionally, gape-limited feeding means that many fish species display ontogenetic changes in prey selection, with larger predators consuming larger, more energetically valuable prey6,7. Declines in prey size with warming may therefore reduce the rates of energy acquisition by larger predators, resulting in reduced fish growth and smaller overall body sizes within populations8. Furthermore, such altered prey size distributions may favour smaller-sized predator species, providing them with a competitive advantage and thereby shifting the fish community composition towards smaller body sizes9. Evidence from the last interglacial period suggests that fish communities experienced declining body size in response to warmer conditions10,11, and the average size of contemporary fish is expected to show a similar pattern under the current rate of global warming12. However, there is currently little understanding of how these changes will impact the structure and stability of marine ecosystems.

Body mass is a key life-history trait that determines factors such as consumption rates, handling times and gape size13,14. As such, body mass provides an important link between individual physiology and food web structure and is therefore often used to parameterise models of population dynamics and energy flow within ecosystems15,16. In the marine environment, predators are generally larger than their prey, and the predator-prey mass ratio (PPMR) is a good predictor of trophic interactions. For example, allometric diet breadth models accurately predict who eats who in aquatic ecosystems13, whilst declines in PPMR typically result in lower per capita interaction strengths as predators are able to gain the same amount of energy by consuming fewer large prey17. At the community level, larger ectotherms may decline in size more rapidly than smaller ectotherms with warming as a result of their reduced surface area to body mass ratio and the associated challenge of maintaining a higher metabolic rate5,18. This is particularly true for the marine environment, where larger fish and invertebrates display the strongest temperature-size responses19. If warming causes a greater decline in the size of ectotherm predators relative to that of their smaller prey (i.e. changes in community size structure), the average PPMR might decrease, with consequences for interaction strengths and thus energy flow through marine ecosystems.

The physiological basis for temperature effects on PPMR at the community level may be complicated by behavioural responses to environmental change. For example, predators may select for more nutritious (larger) prey in an effort to increase per capita energy intake under energetically stressful conditions, thus reducing their PPMR20,21. Alternatively, predators might feed in a more density-dependent manner, consuming a greater proportion of abundant but relatively smaller prey and thereby increasing PPMR. Importantly, behavioural responses are unlikely to be uniform across predator body sizes, given the different dietary niches of small and large organisms and their differential susceptibility to warming. Previous research has identified variable size-dependent relationships between PPMR and temperature, such that both systematic increases22 and decreases23 to per capita interaction strength are possible.

It is clear we still have limited understanding of how temperature-driven changes in body size may alter community-level feeding relationships, and it is vital to address this knowledge gap if we are to predict ecosystem responses to warming. This is particularly true for the Southern Ocean, which is experiencing widespread environmental changes including rapid regional warming in areas such as the western Antarctic Peninsula24 and northern Scotia Sea25. The Southern Ocean supports a diverse array of higher predator populations including seabirds, seals, penguins and whales, with a food web largely centred around krill (particularly Euphausia superba)26. However, it is expected that krill will shift their distribution southward in response to ocean warming27, with potentially drastic consequences for many regional predator populations unless other suitable prey are available28. Previous research has identified mesopelagic lanternfish (Family Myctophidae, hereafter myctophids) as one such potential alternative resource, due to their extremely high biomass and their role in supporting energy flow to higher predators including seals and penguins during periods of low krill availability29. Additionally, myctophids themselves are major generalist consumers of prey including krill, amphipods and copepods, and therefore exert significant influence over food web dynamics30. Myctophids are strongly size distributed in the Southern Ocean, with smaller species and individuals found at lower (warmer) latitudes31, and they display clear size-selectivity in their feeding32,33. Warming may therefore alter the size distribution of myctophids and the size relationships between these predators and their prey, and it is important that we understand what these likely changes will be in order to model ecosystem responses.

In this study, we assessed the relationship between temperature and the relative sizes of myctophids and their prey using a dataset of 1576 stomachs and 3707 prey size measurements from 10 myctophid species sampled across >10 of latitude in the Southern Ocean (Fig. 1). We hypothesised that myctophids would exhibit a decline in PPMR with increasing temperature, due to (1) a greater decrease in the size of these predators versus their prey, and/or (2) predators selecting for larger prey as temperature increases.

a partial residual plot from a linear mixed model of the effect of sea-surface temperature (SST) on prey-averaged predator-prey mass ratio (PPMR); (b) partial residual plot from a linear mixed model of the effect of SST on predator body mass; (c) scatterplot of the relationship between SST and abundance-weighted average prey mass in predator stomachs. Y-axis values are in log10 g. Lines represent predicted values at each SST. Shading represents 95% confidence intervals. Source data are provided as a Source Data file.

The effect of declining PPMR on interaction strengths will depend on the interactive effects of temperature and body mass on metabolism and consumption34, making it difficult to predict the consequences for ecosystem stability. It has previously been found that temperature alters the directionality and shape of the relationship between PPMR and predator attack rate and prey handling time, with low PPMR destabilising community dynamics under warming due to elevated predation rates at low prey density34. Additionally, when declines in body mass under warming are restricted to isolated trophic levels, community stability is expected to be reduced35, possibly due to lower top-down control of prey populations36. However, while the reduced ingestion efficiencies and higher metabolic costs associated with higher temperatures are expected to make predator populations increasingly vulnerable to starvation, this effect is exacerbated under high PPMRs37, therefore the observed decline in predator size with warming may in fact provide a buffer against population crashes. Ultimately, the effects of warming and PPMR on the strength of interactions will depend on factors including predator and prey identity, predator body size and thermal tolerance. Further investigations of the combined effects of temperature and PPMR on interaction strengths will be important for determining the possible consequences of altered size-structuring of predator-prey interactions for the stability of ecological communities. This could be facilitated through the application of ecosystem flux or dynamical population models38,39.

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