The Functioning of Marine Ecosystems A fisheries perspective Philippe Cury Lynne Shannon Yunne-Jai Shin Good Morning Ladies and Gentlemen I am going to develop here several theoretical aspects of the functioning of marine ecosystems using a fisheries perspective This is a paper that I did with Lynne Shannon from MCM - South- Africa and Yunne Shin from IRD - France

Definition of Marine Ecosystems The term “Ecosystem” is recent (Tansley 1935) An ecosystem is defined as “a spatially explicit unit of earth that includes all of the organisms, along with all the components of the abiotic environment within its boundaries” (Likens 1992) A marine ecosystem contains water, detritus, hundreds of kinds of organisms including bacteria, phytoplankton, zooplankton, fishes, mammals, birds … and fishers! The term “Ecosystem” is recent and dates back to the thirties An ecosystem is defined quite vaguely as “a spatially explicit unit of earth OR OCEAN that includes all of the organisms, along with all the components of the abiotic environment within its boundaries” Consequently a marine ecosystem contains water, detritus, hundreds of kinds of organisms including bacteria, phytoplankton, zooplankton, fishes, mammals, birds … and fishers! And All these components are connected within a complex food web through dynamic interactions which is coupled with the physical environment

Ecosystem as an ‘Uncomfortable’ large scale Unit for Ecological studies but an Integrative level for Fisheries Management Ecosystems have no apparent boundaries and lack the sort of clear objective or purpose that can be ascribed to other, more tractable, biological or ecological entities (e.g. cell, individual or population): there is no clear objective function to maximize However the ecosystem is now viewed as an integrative level, and its overall complexity is perceived as critical to its sustainability Ecosystems have no apparent boundaries and lack the sort of clear objective or purpose that can be ascribed to other, more tractable, biological or ecological entities (e.g. cell, individual or population) ): No clear objective function to maximize … except perhaps the ‘future’ that we would like to ascribe to the ecosystem However the ecosystem is now viewed as an integrative level, and its overall complexity is perceived as critical to its sustainability Ecosystem is Uncomfortable large scale Unit for Ecological studies but an Integrative level for Fisheries Management

Questions Regarding the Exploitation of Marine Ecosystems : Which species are most critical, and which ecological processes are most sensitive to exploitation? Does the removal of top predators have a strong impact on lower trophic levels? Does heavy exploitation of forage species, such as anchovies and sardines, cause changes in the functioning of upwelling ecosystems? And Important questions need to be addressed when exploiting marine ecosystems such as: Which species are most critical, and which ecological processes are most sensitive to exploitation? Does the removal of top predators have a strong impact on lower trophic levels? Does heavy exploitation of forage species, such as anchovies and sardines, cause changes in the functioning of upwelling ecosystems?

The key to answering these questions and exploring whether general principles apply lies in understanding the energy flow in the ecosystem The key to answering these questions and exploring whether general principles apply lies in understanding the energy flows and how it is controlled in the ecosystem

Which Energy Flows in Marine Ecosystems? Who is controlling Whom? Different types of control have been identified in marine ecosystems: in 1887 Hensen Used an analogy with agriculture where crop yields can be predicted from the control of the input, then he made the assumption that food supply regulates adult fish stocks, In other words, in a Bottom-up control the regulation of food-web components is made by primary producers. In this case the energy flow is controlled from the bottom up to the top Species mostly interact through predation . In a top-down control, which means the regulation of lower food-web components by one or several upper-level predators, is considered to be critical in the functioning of marine ecosystems. In this case the energy flow is controlled from the top down to the bottom. in several marine systems there is a mid-trophic level, occupied by a limited number small pelagic fish species, those are dominant populations which vary radically in abundance. They can exert a major control on energy flows, and this is called wasp–waist control. In this case the energy flow is controlled up and down from the middle. Bottom-Up Top- Down Wasp-Waist

Bottom-up Control Now I would like to illustrate these different types of control and and we start with the bottom up control

The Very Small drive the Very Large Primary Productivity, strongly coupled with the physical environment, is the driving force under a bottom-up approach, in this case the very small drive the very large the primary production, here the control factor is the red line and the responses are the blue line. In the present case the physical environment is for example less favourable, it then controls the decrease in abundance of the phytoplankton, which in turn has a negative impact on the abundance of the zooplankton. The diminution of the zooplankton controls the decrease in abundance of the prey fish, which itself leads to a decrease in the abundance of the predators . Parallel long term changes can be observed at different trophic levels

westerly weather phytoplankton zooplankton Parallel long-term trends across four marine trophic levels and weather in the North Sea (from Aebischer et al, Nature 1990) herring Kittiwake laydate Parallel long-term trends were found across four marine trophic levels and weather in the North Sea suggesting a bottom up control Even though the mechanisms behind the parallelism on trends remain unclear, the effect of the environment was identified as the driving force for structuring several components of the ecosystem. Kittiwake clutch Kittiwake chicks

Five ecosystems in the Pacific were affected by the mid-1970s climate change event (from McGowan et al. 1998) Five ecosystems in the Pacific were affected by the mid-1970s climate change event Ecosystems are connected and respond to drastic environmental changes However the mechanisms by which climate exerts its influence vary as components of the ecosystem are constrained by different limiting environmental factors. Thus similar species at the same trophic level may respond quite differently to climate change Findings from one system cannot necessarily be extrapolated to others, and predicting the effects of global-scale environmental change on ecosystems does not appear to be simple.

Regime Shifts within the Peruvian Ecosystem (from Pauly and Tsukayama 1987) If we focus now on the Peruvian Ecosystem Primary production seems to have affected the anchoveta as well as the overall fish productivity in the Peruvian ecosystem. But to interpret the responses of other fish populations like sardine, horse mackerel or hake is not simple

Bottom-up Control Under bottom-up control, the physical environment drastically affects the overall productivity (i.e. the carrying capacity) of ecosystems, but more importantly the dynamics of fish assemblages in a more or less predictable way… Decadal-scale regime shifts suggest the existence of multiple stable states in fish communities, resulting in sustained or un-sustained fisheries and induced ecosystem changes A Bottom-up control offers a comprehensive framework for understanding how different components would react to environmental changes or to changes at the bottom of the food chain Under bottom-up control, the physical environment drastically affects the overall productivity (i.e. the carrying capacity) of ecosystems, but more importantly the dynamics of fish assemblages in a more or less predictable way… Decadal-scale regime shifts suggest the existence of multiple stable states in fish communities, resulting in sustained or un-sustained fisheries and induced ecosystem changes A Bottom-up control offers a comprehensive framework for understanding how different components would react to environmental changes or to changes at the bottom of the food chain

Top-Down Control Lets explore now the effect of predation on ecosystem dynamics

The Very Large drive the Very Small Most species interact through predation, and in the case of the top-down control the very large drive the very small the predators, I.e. the control factor is in red line and the responses are in blue lines. The decreasing size of the top predator populations lead to a reduced predation on the prey that leads to an increase in the abundance of the prey fish. The increase predation of the fish prey on the zooplankton lead to a decrease in the population size. The diminution of the zooplankton abundance reduces the grazing pressure on the phytoplankton which consequently becomes more abundant.

Bigger Fish Eat Smaller Fish Predation is recognized as a key structuring process in aquatic ecosystems And due to their streamlined body shape without any prehensile appendices, this conducts to the admitted rule in the marine environment that bigger fish eat smaller fish (in the terrestrial environment you will see a lion eating a bigger animal, you will never see a fish eating a bigger fish)

Who is eating whom? Cannibalism, Omnivory Predators are constrained by the size of their jaw and prey fish that are less than 1/3 their own size Who is eating whom? Cannibalism, Omnivory The relative stability of the total fish biomass compared to that of individual species Predators are constrained by the size of their jaw and prey fish that are less than 1/3 their own size Who is eating whom? :we have here three different fish species in yellow, red and blue, due to their feeding strategy cannibalism is frequent, omnivory as well, as one species will feed on smaller sizes of other species, but it also a fact that a herring for example can prey on eggs or larvae of a cod Altogether this gives a complex dynamics of interaction that can help to explain two different patterns: Size-based predation provides an explanation for observed size spectra in marine ecosystems The relative stability of the total fish biomass compared to that of individual species Size-based predation provides an explanation for observed size spectra in marine ecosystems

Trophic Cascade in Alaska resulting in inverse patterns in abundance or biomass across trophic links in a food web (from Science, Estes et al. 1998) Not all species are equal some species are particular important for the functioning of the ecosystem, they are called keystone species Otters are keystone species When they are abundant they feed on sea urchin and by limiting the sea urchin population the kelp density becomes high When the killer whales prey on them, the abundance of otters diminish, the biomass of sea urchin then increases and the kelp forest become scarce. This process is called a Trophic Cascade resulting in inverse patterns in abundance across trophic links in a food web

Top-Down Control A top-down control can help to understand several observed ecological patterns at an ecosystem level when removing top predators Not all cascades propagate to lower trophic levels or have significant impacts on ecosystem processes as numerous compensatory mechanisms dampen or eliminate them Fishing usually greatly reduces the abundance of top predators, and it stands to reason that the abundance of prey populations and their effects on marine communities will increase after release from predator control A top-down control can help to understand several observed ecological patterns at an ecosystem level when removing top predators Not all cascades propagate to lower trophic levels or have significant impacts on ecosystem processes as numerous compensatory mechanisms dampen or eliminate them Fishing usually greatly reduces the abundance of top predators, and it stands to reason that the abundance of prey populations and their effects on marine communities will increase after release from predator control

Let s explore now the role of dominant forage fish species within ecosystems Wasp-Waist Control

Small pelagic fishes drive both the very large and the very small Small pelagic fish may exert a major control on energy flows in upwelling ecosystems, and this has been called wasp–waist control. Then Small pelagic fishes drive both the very large and the very small The abundance of the forage fish (sardine and anchovy) which is under the dependence of the environment, controls both the abundance of the predators and of the primary production.

Birds and Sardine in South Africa and Namibia (from Crawford 1999) In nature this is difficult to be a predator And the abundance of two marine birds (Penguin and Gannets) closely follows the abundance of their favourite prey , the sardine In South Africa when sardine came back so did the penguins In Namibia the collapse of the sardine stock in the seventies was followed by a collapse of the gannets The abundance of sardine in those two ecosystems control the abundance of marine birds

Pelagic fish abundance & zooplankton Black-Sea Pelagic fish abundance & zooplankton 300 Zooplankton abundance 200 100 200 400 600 800 Ghana Pelagic fish abundance 200 South-Africa 100 7 More surprisingly it appears that the abundance of pelagic fish species can alter the abundance of their prey, the zooplankton Higher abundances of fish are then associated with low abundance of zooplankton , this appears to be the case in the Black sea, Ghana, South Africa and Japan 100 200 300 5 Japan 60 3 100 300 500 700 40 20 2000 4000 6000

Wasp-Waist Control Under wasp-waist control the collapse of a dominant prey species can generate drastic changes at higher, but most surprisingly at lower trophic levels As fisheries remove substantial amounts of small pelagic fish one must carefully consider the implications for the other species in the ecosystem Under wasp-waist control the collapse of a dominant prey species can generate drastic changes at higher, but most surprisingly at lower trophic levels As fisheries remove substantial amounts of small pelagic fish one must carefully consider the implications for the other species in the ecosystem

Bottom-Up Top- Down Wasp-Waist Considering top-down, bottom-up or wasp-waist type of controls produces different ecosystem dynamics, and consequently different possible ecosystem responses to fisheries activity and management Let’s take an example: in all three examples top predators decrease in abundance as a result of only fishing if we consider a top down control, as a result of both fishing and the environment if we consider bottom-up control or as a result of a combined effect of fishing and less forage fish considering the wasp waist control

Who is controlling whom in Marine Food-Webs ? Most ecosystems are not purely top-down or bottom up or wasp waist but a mixture of these controls Who is controlling whom in Marine Food-Webs is a key question that has only received a few preliminary answers until now How such ecosystems in the Benguela will react to changes top fish predators abundance or to an increase in prey species abundance is still an open question.

the ability to predict ecosystem behavior is limited No General Theory can be ascribed to the Functioning of Marine Ecosystems the ability to predict ecosystem behavior is limited This is no General Theory can be ascribed to the Functioning of Marine Ecosystems (and there will not be) And our ability to predict ecosystem behavior is most of the time limited, like for any complex dynamical system

However ecosystems are neither totally predictable nor totally unpredictable : tentative generalisations can be proposed Control by the environment (bottom-up control) predominates Control by predators (top-down control) plays a role in dampening ecosystem-level fluctuations Trophic cascades are seldom found, except in lakes, or in marine hard substrata ecosystems and mainly for less complex food-webs Wasp-waist control is most probable in upwelling systems. However ecosystems are neither totally predictable nor totally unpredictable : tentative generalisations can be proposed Control by the environment (bottom-up control) predominates Control by predators (top-down control) plays a role in dampening ecosystem-level fluctuations Trophic cascades are seldom found, except in lakes, or in marine hard substrata ecosystems and mainly for less complex food-webs Wasp-waist control is most probable in upwelling systems.

From ‘common sense’ and ‘pet concept’ toward an operational framework for dealing with responsible fisheries in marine ecosystems? These difficulties do not mean that an ecosystem approach to fisheries management should be abandoned or that we should just wait for more additional results on the functioning of ecosystems Major steps are urgently needed, that will define an operational framework for dealing with responsible fisheries in marine ecosystems, for example by using ecosystem-based indicators and reference points This is a complex issue that needs to integrate our simplistic and disparate views of nature and to reach major steps towards incorporating our recent and incomplete, but consequential, theoretical background on the functioning of marine ecosystems These difficulties do not mean that an ecosystem approach to fisheries management should be abandoned or that we should just wait for more additional results on the functioning of ecosystems Major steps are urgently needed, that will define an ecological framework for dealing with responsible fisheries in marine ecosystems, for example by using ecosystem indicators and reference points This is a complex issue that needs to integrate our simplistic and disparate views of nature and to reach major steps towards incorporating our recent and incomplete, but consequential, theoretical background on the functioning of marine ecosystems

‘Not only is the science incomplete, but the [eco]system itself is a moving target, evolving because of the impact of management and the progressive expansion of the scale of human influences on the planet’ Holling C.S. (1995) Thank you for your attention