Elsevier

Progress in Oceanography

Volume 156, August 2017, Pages 91-103
Progress in Oceanography

Can schooling regulate marine populations and ecosystems?

https://doi.org/10.1016/j.pocean.2017.06.003Get rights and content

Highlights

  • Large schools, shoals or swarms are shown to appear at high population density.

  • They lead to a decrease of foraging success and an increase of predatory mortality.

  • At low population, small groups provide maximum foraging success and low predation.

  • This would lead to an emergent regulation of marine populations and ecosystems.

  • An evolutionary process is proposed, linking schooling to high fecundity.

Abstract

Schools, shoals and swarms are pervasive in the oceans. They have to provide very strong advantages to have been selected and generalized in the course of evolution. Auto-organized groups are usually assumed to provide facilitated encounters of reproduction partners, improved protection against predation, better foraging efficiency, and hydrodynamic gains. However, present theories regarding their evolutionary advantages do not provide an unambiguous explanation to their universality. In particular, the mechanisms commonly proposed to explain grouping provide little support to the formation of very large groups that are common in the sea (e.g. Rieucau et al., 2014). From literature review, data analysis and using a simple mathematical model, I show that large auto-organized groups appear at high population density while only small groups or dispersed individuals remain at low population density. Following, an analysis of tuna tagging data and simple theoretical developments show that large groups are likely to expose individuals to a dramatic decrease of individual foraging success and simultaneous increase of predatory and disease mortality, while small groups avoid those adverse feedbacks and provide maximum foraging success and protection against predation, as it is usually assumed. This would create an emergent density-dependent regulation of marine populations, preventing them from outbursts at high density, and protecting them at low density. This would be a major contribution to their resilience and a crucial process of ecosystems dynamics. A two-step evolutionary process acting at the individual level is proposed to explain how this apparently suicidal behaviour could have been selected and generalized. It explains how grouping would have permitted the emergence of extremely high fecundity life histories, despite their notorious propensity to destabilize populations. The potential implications of the “grouping feedback on population resilience, ecosystem stability and the persistence of marine biodiversity are discussed. The risk of harvesting marine species with fishing gears that enable catching dispersed individuals (such as longline, gillnet, trawl or using fishing aggregative devices for instance) is underlined. Finally, tropical tunas are used to exemplify the potential importance of schooling in shaping complex life histories and species interaction.

Introduction

Schooling, shoaling and swarming are pervasive in the oceans where the immense majority of pelagic species and 80% of all fish species aggregate and form dense and labile groups, at least during important periods of their life cycles (Fréon and Misund, 1999). Aggregative behaviour is so common in the aquatic realm that it has to provide very strong advantages to have been selected and generalized in the course of evolution. Auto-organized groups are usually assumed to provide facilitated encounters of reproduction partners, improved protection against predation, better foraging efficiency, and hydrodynamic gains (Brock and Riffenburgh, 1960, Fréon and Misund, 1999, Pitcher, 2010). However, present theories regarding their evolutionary advantages do not provide an unambiguous explanation to their universality. In particular, the mechanisms commonly proposed to explain grouping provide little support to the formation of very large groups (thousands to billions of individuals) that are common in the sea (Rieucau et al., 2014). From literature review, new data analysis and theoretical developments, I show that the emergence and the size of auto-organized groups are density-dependent, and that large groups and clusters of groups (Bertrand et al., 2008) expose individuals to enhanced predation and disease mortality and reduce individual foraging efficiency, while dispersed individuals, isolated or in small groups, largely escape those adverse feedbacks. This would prevent marine populations from outbursts and subsequent extinction due to resource exhaustion at high density, and protect them from predation while maintaining their reproductive capacity at low densities. This process would be a major ecological contribution to the stability and resilience of populations, communities and ecosystems. It would ensure the viability of extremely high fecundity life histories, despite their notorious propensity to destabilize populations (Mueller and Joshi, 2000). High fecundity is a major evolutionary asset. Its obligatory association with schooling would be the key to understand why schooling and swarming have been so universally generalized in aquatic ecosystems, despite the detrimental effects of large groups on individual fitness. A two-step evolutionary process acting at the individual level is proposed in this perspective, in agreement with standard evolutionary theory.

Section snippets

Marine populations exhibit density-dependent alternative states

Marine populations, from bacteria to fish, can be composed of up to billions of individuals. Large numbers of elementary interactions between them often lead to the emergence of macroscopic structures such as zooplanktonic swarms or fish shoals and schools (Parrish et al., 2002). Similar phenomena are observed for terrestrial populations with bird flocks, bee or locust swarms, and ungulate herds (Buhl et al., 2006). Field studies (e.g. Fréon et al., 1996) show that marine populations can exist

The number and size of aggregative structures increase with population density

Macroscopic processes acting at the group level drive the size-distribution of groups. Theoretical models based on the probability of group encounter, coalescence and splitting, as well as field observations, show that animal group-size distribution follows a universal power-law decay (Bonabeau and Dagorn, 1995, Niwa, 1998, Bonabeau et al., 1999) truncated at a cut-off size proportional to population density (Niwa, 1998, Niwa, 2003). The mean group size is therefore linearly related to

Is grouping always beneficial to individuals in the sea?

It is generally hypothesized that grouping provides individuals with important evolutionary advantages such as (1) increased probability to find sexual partners, (2) better foraging efficiency, (3) protection against predators (Brock and Riffenburgh, 1960, Pitcher and Parrish, 1993, Fréon and Misund, 1999) and (4) energy savings due to hydrodynamic advantages (Fish, 1999, Herskin and Steffensen, 1998, Parker, 1973, Weihs, 1973). The goal of this paper is not to provide a detailed review of the

Are large aggregative structures dissipating marine populations faster?

We have seen that large auto-organized groups (e.g. swarms/shoals/schools) are likely to enhance predation and disease mortality and reduce individual foraging efficiency. I propose to consider them as dissipative structures (Nicolis and Prigogine, 1977), emerging from individual interactions when population density increases. Dissipative structures are ordered self-organized macroscopic structures that can appear in dissipative systems (open systems that continuously exchange energy, matter

Could grouping provide populations with a stabilizing feedback?

Following my reasoning, dispersed populations would remain virtually undetectable for predators who would only find dispersed prey by chance, when they are so close that they can be seen. Prey would become massively available to predators only after condensation, when groups bigger than the detection threshold appear, just like gaseous water is invisible and becomes visible when it becomes liquid. Dispersed populations would furthermore experience minimal risk of infection and epidemic while

Evolutionary perspective and the importance of high fecundity

When a population’s biomass is low, aggregative behaviour leads to the formation of small groups that ensure better reproductive success and lower predation mortality to individuals than in the absence of aggregative behaviour. These constitute clear evolutionary advantages acting at the individual level in agreement with standard evolutionary theory (Pitcher, 2010). At high population biomass however, large groups appear, leading to low foraging efficiency and high predatory and disease

Effects of grouping at the community and ecosystem levels

Simple ecological models predict that predator-prey dynamics are intrinsically unstable (e.g. Volterra, 1926, May, 1976). However, unstable predator-prey oscillations are generally not observed in reality where strong density-dependent processes must be acting to explain the stability of populations and communities (e.g. Jennings, 2005). Amongst other factors such as partial niche overlap between predator and prey and the stabilizing role of spatial heterogeneity, the grouping feedback loop

Grouping, fishing, multi-species schools and complex life-histories

Fishing is a predatory activity. Some fishing gear like purse seines target fish schools and cannot efficiently harvest dispersed individuals. Corresponding fishing data only reflect the condensed fraction of the population and thus might dramatically amplify the actual population variability (Fréon, 1991) (Fig. 9). Those fisheries operate like other top predators in the sea and compete with them for the condensed fractions of their prey populations. Other fishing gear like longlines, gillnets

Conclusion

The present paper suggests that the ecological role and evolutionary advantage of aggregative behaviour in the sea might differ from previous views on the topic, which posit that swarming, shoaling and schooling are always beneficial to individuals by enhancing their foraging efficiency and protecting them from predation. It is proposed that aggregative behaviour simultaneously improves individual reproductive success and protects from predation at low population density while it leads to a

Acknowledgements

I would like to thank Janet Coetzee, DAFF, South Africa and Jessica Farley, CSIRO, Australia who kindly provided the data used in Fig. 3 as well as Alain Fonteneau, IRD, France who kindly provided the data used in Fig. 4. I would also like to express my gratitude to the colleagues who read an earlier version of this paper, for their encouragements and criticisms that helped to improve considerably my hypothesis. In alphabetic order: Olivier Aumont, Emlyn Ballarin, Arnaud Bertrand, Laurent Bopp,

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