From an Antagonistic to a Synergistic Predator Prey Perspective

Bifurcations in Marine Ecosystem

Tore Johannessen

• Publisher: Academic Press
• Year: 2014
• Print ISBN: 9780124170162
• eBook ISBN: 9780124201118
• Topic: Biological Sciences
• Subtopic: Ecology
• Index: Biological Sciences

From an Antagonistic to a Synergistic Predator Prey Perspective: Bifurcations in Marine Ecosystems is a groundbreaking reference that challenges the widespread perception that predators generally have a negative impact on the abundance of their prey, and it proposes a novel paradigm — Predator-prey Synergism — in which both predator and prey enhance abundance by their co-existence. Using this model, the text explains a number of issues that appear paradoxical in the case of a negative predator-prey relationship, including observed ecosystem bifurcations (regime shifts), ecosystem resilience, red tides in apparently nutrient depleted water, and the dominance of grazed phytoplankton over non-grazed species under high grazing pressure. This novel paradigm can also be used to predict the potential impact of global warming on marine ecosystems, identify how marine ecosystem may respond to gradual environmental changes, and develop possible measures to mitigate the negative impact of increasing temperature in marine ecosystems. This book approaches the long-standing question of what generates recruitment variability in marine fishes and invertebrates in an engaging and unique way that students and researchers in marine ecosystems will understand. - Introduces a new paradigm, Predator-prey Synergism, as a building block on which to construct new ecological theories. It suggests that Predator-prey Synergism is important in some terrestrial ecosystems and is in agreement with the punctuated equilibria theory of evolution (i.e., stepwise evolution). - Suggests a general solution to the recruitment puzzle in marine organisms - Proposes a holistic hypothesis for marine spring blooming ecosystems by considering variability enhancing and variability dampening processes - Asserts that fisheries will induce variability in marine ecosystems and alter the energy flow patterns in predictable ways

Chapter 1

Introduction

This book presents predator-prey synergism as a novel perspective in ecology, in which predator-prey relationships are defined as enhancing abundances of both the predator and the prey. The idea emerged during analyses of near–century-long-term time series of observations of marine coastal ecosystems, but it is suggested that synergism may be important in some terrestrial systems too. Predator-prey synergism has wide-ranging implications for management of marine ecosystems and for theories in ecology and evolution. Resilience in marine ecosystems may be explained mechanistically by synergism, as may repeated incidents of bifurcations observed in the long-term time series. Bifurcations are sudden and persistent regime shifts as a result of gradually changing environmental conditions. It is suggested that global warming may induce bifurcations, which in turn may result in recruitment failures in fishes and substantially reduced fish abundances.

Keywords

Predator-prey synergism; bifurcation; fish recruitment; global warming

If at first the idea is not absurd, then there will be no hope for it.

Albert Einstein

1.1 About this book

This book’s title, From an Antagonistic to a Synergistic Predator-Prey Perspective: Bifurcations in Marine Ecosystems, includes two concepts that indicate the book’s main focus, namely synergism in relation to predator-prey interactions and ecosystem bifurcations. In addition, recruitment variability in fish is dealt with in detail. Throughout the book, the terms predator and prey are used in the broadest sense of the words, including grazers as predators on primary producers. Predator-prey synergism, introduced as a new concept, is defined as predator-prey relationships enhancing abundances of both predator and prey. Hence, synergistic predators have a positive impact on the abundance of their prey, whereas antagonistic predators have negative impact on their prey. The idea of predator-prey synergism (hereafter “synergism”) emerged as an alternative predator-prey model to account for phenomena observed in long-term time series (since 1919) from the south coast of Norway that appeared paradoxical under an antagonistic predator-prey model, for example, dominance of edible phytoplankton under high grazing pressure, red tides occurring in apparently nutrient depleted water, and repeated observation of bifurcations.

Ecosystem bifurcation is defined as an abrupt and persistent regime shift that affects several trophic levels and results from gradual environmental changes. The concepts and theoretical background for bifurcations are reviewed in this introduction. The empirical basis for suggesting that marine ecosystems are vulnerable to bifurcations is the previously mentioned long time series from the south coast of Norway, obtained during increasing anthropogenic eutrophication, and also increasing temperatures over the past 25 years.

This book consists of seven chapters plus this introduction. A full appreciation of the novel perspectives and theory will only be gained by reading the entire book. Each chapter was written to also satisfy readers wishing to read only selected chapters, however, and hence some repetition was unavoidable.

1.2 Unifying Principles in Ecology—Where are We?

At the dawn of the twentieth century, fishery biologists discovered that the year-class strength of many fishes varies substantially, and 100 years ago the Norwegian pioneer scientist Johan Hjort (1914) proposed the first recruitment hypothesis. This hypothesis suggests that recruitment variability results from different survival rates of fish larvae owing to the degree of match between the abundance of fish larvae and their prey. Hjort’s hypothesis (or modifications of his hypothesis) has up until now been the most generally accepted explanation for recruitment variability (Houde, 2008). However, despite its having been one of the main focuses of marine research for more than 100 years, the recruitment puzzle remains unresolved. Being one of the most important structuring mechanisms in marine ecosystems, the lack of insight into what causes recruitment to vary is indeed compromising our present level of ecosystem knowledge. Unfortunately, this dismal situation appears to be not unique for marine ecosystems, but seems to reflect the generally rather low level of ecosystem understanding. There are few aspects in ecology that are embraced with general consensus, and Ridley (2003, p. 5) is probably right in stating that “[evolution] is the only theory that can seriously claim to unify biology.”

One important approach of gaining insight into ecosystem mechanisms is by theoretical studies and mathematical modeling. Such studies show that it is theoretically possible that complex ecosystems are less stable than simple ecosystems (e.g., May, 1973). This was indeed an interesting perspective, as it turned the previous notion of ecosystem stability (Elton, 1958; MacArthur, 1955) upside down. However, the theoretical proposals of ecosystem mechanisms derived by mathematical models are per se, nothing but elegantly designed theoretical speculations from which to obtain new ideas that must be verified by studies of real ecosystems. Similarly, experimental ecosystem studies are inevitably too limited in terms of the number of species and spatial and temporal scales to be realistic (Pimm, 1991). Hence, both mathematical models and most experimental ecological studies can only provide ideas that will have to be tested by studies of real ecosystems on realistic temporal and spatial scales.

The problem faced in studying real ecosystems seems to be similar to that of studying evolutionary processes, which was so simply and convincingly formulated by Maynard Smith (1977, p. 236): “For example, consider selection. Suppose that there are two types of individuals in a population, say red and blue, which differ by 0.1 per cent, or 1 part in 1000 in their chances of surviving to breed. If the population is reasonably large (in fact, greater than 1000), this difference in chance will determine the direction of evolution, towards red or blue as the case may be. But if we wished to demonstrate a difference in the probability of survival during one generation—that is, wished to demonstrate natural selection—we would have to follow the fate of one million individuals, usually an impossible task.”

Nevertheless, evolution is a solidly grounded theory for several reasons (Ridley, 2003), two of which may provide guidelines for the advancement of ecosystem theory: (1) Evidence of evolution in the fossil record (the temporal problem) and (2) a mechanistic explanation for evolution in terms of mutations and natural selection. One way to overcome the temporal problem in studies of natural ecosystems is to collect long and systematic time series and then, based on patterns in such time series, develop mechanistic models for the processes underlying the observed patterns. These models should then be tested, preferably in real ecosystems. Through observations from real ecosystems, we can be relatively certain that the studied phenomena are genuine ecosystem responses.

This approach was adopted in this book, which starts off by presenting results from systematically collected annual abundance data of young-of-the-year gadoid fishes along the south coast of Norway (since 1919). This time series revealed repeated incidents of sudden and persistent recruitment failures in the gadoids. Comprehensive testing in the field of the mechanism underlying these recruitment failures, and direct and indirect evidence of concurrent shifts in the plankton community, provided substantial evidence suggesting that marine ecosystems are vulnerable to bifurcations.

1.3 Recruitment Variability

In order to disentangle the mechanisms underlying the recruitment failures in the gadoids, a recruitment hypothesis was suggested and tested in the field. Atlantic cod (Gadus morhua) was used as a model species in these studies. The generally accepted perception is that most of the recruitment variability in fish occurs during early life stages. In agreement with this, cod recruitment was mainly determined within the first six months after spawning but well after the larval stage. The results suggested that young-of-the-year cod depend on energy-rich planktonic prey until they are quite large (up to approximately 8 cm), and early shifts to less energy-rich prey (e.g., fish and prawns) result in low condition and poor survival. It was proposed that variability in the plankton community generates variable energy flow patterns to higher trophic levels and thereby induces recruitment fluctuations in cod, other fishes, and benthic invertebrates that depend on pelagic prey during early life stages. After this period of food-limited survival, abundant organisms will attract opportunistic predators, which will then act to reduce differences between year-classes at older stages. It is suggested that, as general phenomena, physical and chemical bottom-up processes generate variability in marine pelagic food webs, whereas predation, parasitism, and diseases act to dampen variability. Fisheries targeting larger fishes will thus induce variability in marine ecosystems.

The mechanism underlying the repeated incidents of sudden and persistent recruitment failure in the gadoid fishes was suggested to be abrupt shifts in the plankton community as a result of gradual environmental changes (eutrophication and increasing temperature).

1.4 Ecosystem Bifurcation

With the prospect of global warming, a significant topical question is how marine ecosystem will respond to gradual environmental changes. At present, the assessment and monitoring of dynamics of ecosystems are based on the assumption of simple dose-response relationships. Gradual environmental changes or perturbations are expected to cause corresponding changes in the abundance of affected species. However, it has long been recognized theoretically that ecosystems may shift between alternative stable states, each of which has its own basin of attraction (Holling, 1973; Lewontin, 1969; May, 1977).

More recently, evidence of shifts between contrasting states in large-scale ecosystems was provided (Scheffer et al., 2001). Most of these examples were ecosystem shifts attributed to abrupt environmental shifts or catastrophic events (e.g., storms, mass mortality due to pathogens). One example, however, was the gradually increasing eutrophication in shallow lakes, causing shifts from a clear water state with submerged vegetation to a turbid state in which phytoplankton dominated. Such shifts have been classified as bifurcations (Biggs et al., 2009; Scheffer et al., 2009). According to mathematical theory, a bifurcation occurs when a small, smooth change made to the parameter values of a system causes a sudden change in system behavior.

In the marine literature, the term “regime shift” has been frequently used to describe abrupt changes in time series. However, the application of different definitions of regime shifts (Jarre et al., 2006; Overland et al., 2008) has rendered the concept vague. To be more explicit, the concept of ecosystem bifurcations used in this book refers to abrupt and persistent ecosystem shifts that affect several trophic levels and result from gradual environmental changes. To define more precisely, the term “persistent” is not straightforward. A useful criterion, though, could be the one suggested by Connell and Sausa (1983, p. 808) to judge whether real ecosystems are stable: “the fate of all adults must…be followed for at least one complete overturn… .”

Resilience is a concept inseparably linked to ecosystem bifurcations. However, there are different definitions of the concept (Gunderson, 2000; Pimm, 1991). Here, resilience is used as proposed by Holling (1973), defined as the maximum perturbation a system can sustain without causing a shift to an alternative stable state.

Ecosystem bifurcations are not restricted to shifts triggered when tipping points in critical variables are reached. Bifurcations may also occur when shifts are triggered by environmental perturbations after the resilience of the system has been reduced as a result of gradual environmental changes, that is, the shift may occur before the tipping point is reached.

The theoretical relationships of bifurcations, resilience, and environmental perturbations is illustrated in Fig. 1.1 (modified from ideas by Lewontin, 1969; May, 1977; Scheffer et al., 2001). In nature, there are different dynamically stable ecosystem states—that is, the community structure varies within specific limits. A stable state can be considered as a trough in which a ball is being rocked back and forth by environmental and biological perturbations (e.g., temperature variability, diseases, and invasions). The depth of the trough represents resilience. Under a specific environmental regime the ecosystem state for which the conditions are optimal will have the highest resilience (Fig. 1.1a and c). When the resilience is high, large perturbations are needed to bring the ball out of the trough. If the environmental conditions change in favor of State 2 (Fig. 1.1b), the resilience o...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Dedication
• List of Contributors
• Preface
• Chapter 1. Introduction
• Chapter 2. Repeated Incidents of Abrupt and Persistent Recruitment Failures in Gadoids in Relation to Increasing Eutrophication, 1919–2001
• Chapter 3. Causes of Variation in Abundance, Growth, and Mortality in 0-Group Gadoids After Settlement and a Hypothesis Underlying Recruitment Variability in Atlantic Cod
• Chapter 4. Growth and Mortality in Settled Atlantic Cod in Relation to Diet—Evidence for a Recruitment Mechanism
• Chapter 5. Bifurcations in Marine Ecosystems: Concurrent Recruitment Collapses in Gadoid Fishes and Changes in the Plankton Community
• Chapter 6. Predator-Prey Synergism in Plankton
• Chapter 7. Ecological Implications of Predator-Prey Synergism in Marine Ecosystems
• Chapter 8. Variability Enhancing and Variability Dampening Mechanisms in Marine Ecosystems
• Index