Phytoplankton and the balance of nature: An opinion

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    In two recent judgements (ECJ, 2004, 2009) the European Courtof Justice ruled on several parts of this denition. The ruling ofinterest here concerns the balance of organisms. In paragraph 21of ECJ (2004), the Court stated that:

    necessarily involves reductions in other species. We draw on thescientic literature in support of three main arguments. First, theruling reects only one point of view in a continuing debate on thenature of ecosystems. Second, marine ecosystems, especially thoseinvolving micro-algal or cyanobacteria primary producers, arenaturally highly dynamic. Third, the growth of undisturbed as wellas disturbed populations of phytoplankters is typically exponential(which might be called proliferation) and although the biomass

    * Corresponding author.

    Contents lists available at

    Estuarine, Coastal a

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    Estuarine, Coastal and Shelf Science 113 (2012) 317e323E-mail address: richard.gowen@afbini.gov.uk (R.J. Gowen).ecosystems, driven, in part, by an appreciation of the threat tonatural systems by human pressures on the biosphere. One suchpressure is nutrient enrichment of coastal waters. The EuropeanUrban Waste Water Treatment Directive (UWWTD; CouncilDirective 91/271/EEC, 1991) requires nutrient stripping fromdischarges into waters that are eutrophic or at risk of eutrophica-tion. The Directive dened eutrophication as: the enrichment ofwater by nutrients, especially compounds of nitrogen and/orphosphorus, causing an accelerated growth of algae and higherforms of plant life to produce an undesirable disturbance to thebalance of organisms present in the water and to the quality of thewater concerned.

    other plant therefore constitutes, as such, a disturbance of thebalance of the aquatic ecosystem and, accordingly, of the balance ofthe organisms present in the water, even when other speciesremain stable. Moreover, given the competition between plantspecies for nutrient salts and luminous energy, the proliferation ofone or several species, by monopolising the resources necessary tothe growth of other algae and aquatic plants, very often if notalways entails reductions in other species.

    We identify two points for discussion, that proliferation of anyprimary producer constitutes a disturbance of the balance oforganisms and that the proliferation of one or more species1. Introduction

    There is currently much interest in0272-7714/$ e see front matter 2012 Elsevier Ltd.http://dx.doi.org/10.1016/j.ecss.2012.08.009organisms tend towards a stable climax composition, and (b) communities as dynamic systems that maybe governed by basins of attraction in state space. We use data from the Irish Sea and Narragansett Bay,together with a review of the literature, to show that: the dynamics of temperate marine phytoplankton,with seasonal successions, corresponds more to (b) than to (a); the temporary dominance of any onespecies of micro-alga or cyanobacterium is part of the natural dynamics of phytoplankton communitiesand does not permanently impact on other species. Understanding the phytoplankton as a dynamicsystem suggests its status should not be assessed against a climax model and that eutrophication shouldbe diagnosed from fundamental (nutrient-induced) perturbations of ecosystem state and function ratherthan from changes in xed assemblages of species and thresholds of abundance.

    2012 Elsevier Ltd. All rights reserved.

    ability and resilience of

    . the equilibrium of an aquatic ecosystem is the result of complexinteractions among the different species present and with theenvironment. Any proliferation of a particular species of algae orKeywords:

    Opposing views in this debate are those of (a) the balance of nature paradigm, in which communities ofAvailable online 11 August 2012more species as a cause of a reduction in other species. We discuss the scientic basis for this opinion inrelation to the growth of marine primary producers and current debates about ecosystem stability.Short communication

    Phytoplankton and the balance of natur

    Richard J. Gowen a,*, Paul Tett b, Theodore J. Smayda Fisheries and Aquatic Ecosystems Branch, Agriculture Food and Environmental ScienceBelfast BT9 5PX, UKb Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1cGraduate School of Oceanography, University of Rhode Island, Kingston, RI 02881, USA

    a r t i c l e i n f o

    Article history:Received 2 March 2012

    a b s t r a c t

    Recent European Court ruspecies of algae as a distu

    journal homepage: wwwAll rights reserved.An opinion

    ision, Agri-Food and Biosciences Institute, Newforge Lane,

    UK

    s in the context of eutrophication viewed proliferation of a particularnce to the balance of aquatic ecosystems and the proliferation of one or

    SciVerse ScienceDirect

    nd Shelf Science

    lsevier .com/locate/ecss

  • l anddeveloped as a result of such growth can sequester nutrients andabsorb photons, such dominance is typically short-lived andwithout long-term consequences for other phytoplankters. Wesupport the second and third claims with illustrations of patterns ofphytoplankton growth and succession in two temperate coastalwaters that we have studied.

    2. The balance of nature

    As reviewed by Cuddington (2001), claims about the balance ofnature fell into three categories:

    1) natural populations have a more or less constant numbers orindividuals;

    2) natural systems have a more or less constant number ofspecies;

    3) communities of species maintain a delicate balance of rela-tionships, where the removal of one species could cause thecollapse of the whole (an associated claim is that communitiesform a single biological entity and have a characteristic speciescomposition).

    Point (1) relates to the Courts concern about proliferation. Point(2) does not seem central to the argument. Point (3) turns on tworelated matters; how biological communities function, and howthey have been conceived to function. Two contrasting views of thenatural world have inuenced modern ecological thought andenvironmental management. One view, originating with Heraclitusof Ephesus (c.535ec. 475 BCE: see Graham, 2005) holds thateverything is in a state of ux. In contrast, the more widely heldview was of the constancy and harmonious working of nature. Forexample, Herodotus of Halicarnassus (c.484ec.425 BCE) wrote, inbook 3 of The Histories that the natural world had been made sothat predators and prey were in an essentially static balance(Watereld and Dewald, 1998). According to Egerton (1973), andsee also Simberloff (1980), it is this view of natural harmony thathas inuenced scientic opinion throughout recent history,particularly the 19th century and into the early 20th century.Pickett and Ostfeld (1995) suggested that one consequence of thisview is that ecosystems have been considered to be: primarilyclosed, self eregulating, and subject to a single stable equilibrium.That is, one which does not change with time unless disturbed andif disturbed returns to the equilibrium state.

    A simple view of equilibrium in the biological community is thatit is a single state in which each species has a unique abundance.Thus, as developed by Frederic Clements (Clements, 1916),a (climatic) climax community is a biological community of plantsand animals which, through the process of ecological successionhas reached an equilibrium in response to climate, soil and otherenvironmental factors. In the absence of human interference, thisstate is self-maintaining. Tansley (1935) argued for a relativelystable dynamic equilibrium. Succession and development areinstances of the universal processes tending towards the creation ofsuch equilibrated systems. In parallel to such views, zoologistsdeveloped theories inwhich inter-species competition led to a stateof balance in animal populations (Nicholson, 1933).

    This balance of nature paradigm has had much inuence on themanagement of terrestrial ecosystems (Cuddington, 2001; Pickettet al., 2007; Spieles, 2010). In opposition, Gleason (1926) heldthat terrestrial oras were no more than contingent associations ofspecies, and Davis and Slobodkin (2004) argued that it wasamistake to try tomanage ecosystems as if theywere organic units.Nevertheless, many ecologists (see Winterhalder et al., 2004) thinkthat ecosystems do behave to some extent as integrated systems.

    R.J. Gowen et al. / Estuarine, Coasta318Therefore, the debate is better seen as about what sort of integratedsystem: one that tends towards an equilibrium or climax, or onethat is best described as oscillating within a basin of attraction(Holling, 1973). An attractor is the dynamic behaviour that thesystem tends towards (The Encyclopaedia of Science, 2012). Therst type is that of the balance of nature view, inwhich ecosystemsare seen as structured functional units in equilibrium inwhich eachspecies has a unique abundance. The second is a non-equilibriumview with an emphasis on: heterogeneity and instability (DenBoer and Reddingius, 1996); exchanges of energy and matter andshifts in dominance within communities (Pickett and Ostfeld,1995). Based on evidence, opinion is shifting towards the secondview. ONeill (2001) saw ecological systems as meta-stable adaptivesystems that may operate far from equilibrium. Botkin (1990) tookexamples from well-documented studies in North America, Africa,Australia and New Guinea, and concluded that there was over-whelming evidence to refute the balance of nature paradigm.

    3. Growth and proliferation of aquatic primary producers

    The adverse effects of coastal eutrophication result from anexcessive stimulation of algae and cyanobacteria (Ferreira et al.,2011). These effects can be found in the plankton or benthos andthe latter include macro-algae (seaweeds). The excess growth ofopportunistic seaweeds, exemplied by Enteromorpha spp., oftenappears as a proliferation of green thalli that can smother otherplants and cause sediment deoxygenation (Raffaelli et al., 1998). Inthe plankton, enrichment can sometimes result in harmful algalblooms that can have a negative impact on ecosystems and theservices they provide to humans (Gowen et al., 2012).

    In general, the vegetative growth of microalgae (and cyano-bacteria) typically involves the binary division of free-living cells(or similar division within chains of cells). This process results inexponential population growth, although the rate of such growth(m) depends on the interval between cell divisions and hence on theavailability of light and nutrients. In addition, populations ofphytoplankters are subject to grazing pressure (and to the inuenceof water movements). First order models of grazing parameterize itas the daily removal of a certain proportion (g) of the population,a process that on its own leads to exponential decrease (e.g. Landryand Hassett, 1983). Thus, as a rst approximation, the combinedrate m-g results in exponential change in the population, at a ratethat may be fast or slow, positive or negative. Physical watermovements may lead to additional exponential decrease throughdilution or dispersal, or to non-exponential increase throughconcentration of cells at convergences (Pitcher et al., 1998).

    Our argument is that all these processes occur naturally in thesea, although mmay remain higher for longer where nutrients havebeen enriched, or there may be greater population biomass to beconcentrated. Competition between species, in terms of nutrientuptake or storage abilities, avoidance of grazing, and ability toexploit water movements or stratication, can be seen as involvingdifferences in exponential rates of population change, with certainspecies beingmore successful under certain conditions, only to giveway to others as circumstances change. Concern about nutrientenrichment should therefore be focussed on sustained disturbanceof the community of phytoplankters rather than on the blooming(proliferation) or enhanced exponential growth of any particularalga. Roelke et al. (2003) make a similar point: managementapproaches should not focus on individual species but rathercommunity behaviour within a desired basin of attraction. Manystudies of phytoplankton composition and abundance undernatural conditions, including those illustrated below, show thatsuccessive growth of species populations need entail no permanentreduction in the abundance of species that have been temporarily

    Shelf Science 113 (2012) 317e323out-competed for resources.

  • 4. Balance and growth in the phytoplankton

    Most studies referenced in Section 2 have dealt with terrestrialecosystems. Pelagic marine systems may be different. Species ofzooplankton have life-spans ranging fromweeks to a few years, andspecies of phytoplankton and pelagic protozoans, like most micro-organisms, are short-lived but are capable of rapid growth.According to Harris (1980) the earliest view of the planktonicenvironment was of an: isotropic homogeneous environment atequilibrium over large scales. However, this has proven not to be thecase. Plankton experiences an inherently variable environment asa result of physical variability driven by meteorology and clima-tology, interacting with tidal and density-driven ows. As a conse-quence, phytoplankton exhibit variability on a range of spatial andtemporal scales (Harris, 1986). Nevertheless, although the mixture

    of species, and their abundance, changes even in samples taken inthe same water-body in successive weeks, there are higher-orderconstancies such as the recurrent annual cycle of phytoplanktongrowth in coastal waters (e.g. Tett and Wallis, 1978; Smayda, 1998;Gowen et al., 2008) and the succession of lifeforms in seasonallystratifying temperate shelf seas (Margalef, 1978). Such recurringbut varying cycles could be seen in terms of basins of attractionwithin ecosystem state space (Lewontin, 1969; Holling, 1973).

    Much has beenwritten on the underlying causes of variability inthe phytoplankton (Margalef, 1978; Kilham and Kilham, 1980;Gaedeke and Sommer, 1986; Harris, 1986; Padisk, 1993; Huismanand Weissing, 1999; Reynolds et al., 2002; Roelke et al., 2003;Smetacek and Cloern, 2008). However, our intention here is not toreview this literature but to illustrate the variability in the phyto-plankton with observations from two locations, the Irish Sea and

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