Schimbarile Climatice Si Circuitele Biogeochimice- Ecosystem Response to Climate Changes

TRENDS in Ecology & Evolution Vol.16 No.9 September 2001

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Roberto Danovaro*Antonio DellAnnoAntonio PuscedduInstitute of MarineScience, University ofAncona, Via BrecceBianche, 60131 Ancona,Italy.*e-mail: [email protected]

Mauro FabianoDIPTERIS, University ofGenoa, Corso Europa 26,16100 Genoa, Italy.

Anastasios TselepidesInstitute of MarineBiology of Crete, PO Box2214, 71003 Heraklion,Crete, Greece.

There is an increasing awareness that theenvironment of the Earth is changing, but it isunknown whether these changes occur cyclically,stochastically, episodically or are long-term trends1.Although our knowledge of some short-lived events[e.g. the El Nio Southern Oscillation (ENSO) event]that have been proven to induce significantmodifications in the structure and functioning ofecosystems is improving, the role of climaticvariations in regulating marine populations andcommunities is not well understood2.

There are indications that marine systemsrespond to climate change: temperature variations,for example, do not only affect metabolic rates ofmarine organisms, but also influence other importantenvironmental variables, such as local currents,water column stratification, nutrient cycling andprimary production3. These variables strongly affectpopulation and community dynamics and, over time,community structure and function.

Major studies of the effects of climate change onmarine ecosystems have taken place in the PacificOcean and many of them have focused on theconsequences of ENSO events. ENSO is the result of acyclic warming and cooling of the surface ocean of thecentral and eastern Pacific. During El Nio years, theinfluence of upwelling cold waters decreases, causingthe surface waters of the central and eastern Pacificto warm up. By contrast, when the upwelling of colddeep waters is more intense than usual, the so-calledLa Nia event takes place. ENSO events have beenproven to modify the structure and productivity of thepelagic ecosystem at extremely large spatial scales46.During El Nio events, the increased water column

stratification inhibits nutrient upwelling, causes adecrease of primary production, zooplanktonabundance and larval fish productivity and modifiesthe planktonic food-web structure711. El Nio-relatedclimatic events also affect coastal benthic communityproduction and structure12,13, and the opposite effectsprobably occur as a result of La Nia-relatedevents14,15.

Climatically driven ecosystem disturbance hasalso been recently reported in coastal areas of thewestern Mediterranean, where the anomalousincrease of summer temperatures (of 23C) and the deepening of the thermocline have resulted in a massive mortality of the benthic fauna (e.g. sponges and gorgonians) inhabiting hard substrates. Mortality was attributed not only to the surface water warming per se, but also to thestability of high sea temperatures over long periods (i.e. several months)16. A similar climate-induced disturbance was observed in theIndian Ocean and along the Caribbean coastline,where the increase in water temperature over anextended period resulted in extensive coral bleaching and mortality17,18.

Compared with terrestrial ecosystems, in whichthe response to climate change is increasinglyapparent19, evidence of ecosystem response in theoceans is difficult to obtain. This applies particularlyto the deep sea, where the need for expensive high-tech sampling devices limits the acquisition oflong-term data. Therefore, only a few studies haveexamined the effects of current climate changes onthe deep sea20.

Recently, large changes in the physicochemicalcharacteristics of the eastern Mediterranean deepwater, known as the Transient event, have beenreported21. Long-term investigations of deep-seabiology have been carried out in the easternMediterranean, providing a unique opportunity tostudy the response of a deep-sea ecosystem to climatevariability on a decadal scale. Because theMediterranean Sea behaves as a miniature ocean22,changes that occur in the eastern Mediterranean canbe used as a model of the potential instability of theoceanic circulation. Such a model would help ourunderstanding and our predictions of the impact ofclimate change in deep seas worldwide23.

Climate change is significantly modifying ecosystem functioning on a global scale, but little is known about the response of deep-sea ecosystems to such change. In the past decade, extensive climate changehas modified the physicochemical characteristics of deep waters in theeastern Mediterranean. Climate change has caused an immediateaccumulation of organic matter on the deep-sea floor, altered the carbon andnitrogen cycles and has had negative effects on deep-sea bacteria andbenthic fauna. Evidence from a miniature ocean model provides new ways ofinterpreting signals from the deep sea and indicates that, contrary to whatmight have been expected, deep-sea ecosystems do respond quickly toclimate change.

Deep-sea ecosystem response toclimate changes: the easternMediterranean case studyRoberto Danovaro, Antonio DellAnno, Mauro Fabiano, Antonio Pusceddu andAnastasios Tselepides

Climate-induced physicochemical changes in the deep seaDeep-sea ecosystems (excluding hydrothermal vents)are thought to be extremely stable compared withcoastal environments. With the exception ofhydrostatic pressure and hydrodynamic forcing(current energy and benthic storms), the main featureof deep seas is a very narrow range of temperatureand salinity, which, at any given depth, remainsalmost constant with time24.

Climate forcing causes surface waters to becomedenser and to sink as a result. Thus, thecharacteristics of deep waters are originallydetermined by the prevailing surface climaticconditions, although these are modified bysubsequent mixing. Consequently, any major changein surface climate can be expected to influence deep-water characteristics25. Climate-induced changes indeep seas can occur in two ways: (1) by deep-waterwarming, linked to surface temperature increasesand to intermediate layer warming; and (2) by theformation of new deep waters, which occurs whensurface waters, preconditioned by high salinity,become sufficiently dense by cooling to cause them to sink.

Both kinds of climate-induced change have beenrecorded in the Mediterranean. A general warmingtrend has been observed in the deep waters of thewestern Mediterranean, where water temperatureshave increased by 0.12C in the past 30 years as a

possible result of greenhouse gas-induced globalwarming26. The opposite effect occurred in the pastdecade in the eastern Mediterranean as a response toregional variability in atmospheric forcing23. Changesin the deep waters in this area occurred in twophases21,27: the first, between 1987 and 1992, wascharacterized by a massive formation of dense,relatively warm water in the south Aegean (theCretan Deep Water), mainly as a result of increasedsalinity; the second phase, from 1992 to 1994, wascharacterized by a drop in deep-water temperature of 0.4C, which resulted in even denser deep waterbeing formed21,27,28. Consequently, the old easternMediterranean Deep and Bottom Waters wereuplifted by several hundred metres21,27 and formed adistinct nutrient-rich intermediate-water layer (theTransitional Mediterranean Water)27,29, which, underthe influence of cyclonic circulation, reachedshallower depths (100150 m; i.e. close to theeuphotic zone2830).

Pelagicbenthic coupling and deep-sea biogeochemical changesLife in the deep sea depends on the constant rain ofsettling particles produced in the photic zone and/orexported from the continental shelf24. The easternMediterranean is considered to be one of the mostoligotrophic areas of the world and is characterized byextremely low primary productivity [2025 g carbon(C) m2 y1]31 and, as a result, extremely small amountsof primary organic matter reach the sea floor32.However, the Transient event and the consequentuplift of nutrient-rich deep waters in the easternMediterranean resulted in increased biologicalproduction. From the early 1980s to the 19941995season31,33 (i.e. after cooling), primary productivityover the continental shelf and upper slope increasedthreefold, reaching values comparable with those inmesotrophic environments (i.e. 6080 g C m2 y1)33.Such changes in primary productivity were alsocoupled with changes in phytoplankton assemblagecomposition (measured as the diatom:dinoflagellateratio), species dominance and average phytoplanktoncell size (which increased by between two and fivetimes)33,34. Increased primary production andphytoplankton cell size are known to enhance verticalfluxes of phytodetritus and organic C to deep-seasediments35. This was observed in the easternMediterranean, where phytodetritus input to thedeep-sea floor increased by up to two orders ofmagnitude36 (Fig. 1a). This flux determined anaccumulation of organic C and N on the sea floor36

(Fig. 1b) and enhanced the quality of sedimentaryorganic matter, evident in terms of proteinaccumulation (Fig. 1b), increased the totalprotein:carbohydrate content ratio and decreased theC:nitrogen (N) ratio (Fig. 1c, Box 1). Such phenomenaare opposite to those described during El Nio events,in which a reduced export production from theeuphotic zone has been reported7,10,37,38.


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Fig. 1. Changes in factorsaffecting the quality ofsedimentary organicmatter from 19891998measured in deep-seasediments [at depths of950 m (squares) and1540 m (circles)] of theCretan Sea43,45,46. (a)Trends in chlorophyll aconcentrations fromJanuary 1989 toSeptember 1997;(b) trends in organic C(yellow) and protein(green) concentrationsfrom January 1989 toSeptember 1997;(c) trends in thecarbon:nitrogen (C:N)(yellow) andprotein:carbohydrate(green) ratios fromJanuary 1989 toSeptember 1997. Barsindicate standarddeviations.

Climatically driven deep-sea biological disturbancePrevious studies have shown that the input of organicmaterial to the marine sediment rapidly enhancesbenthic metabolism and secondary production39 anddetermines an increased density of deep-sea benthicorganisms40. These effects should be even moreevident in food-limited environments, such as highlyoligotrophic deep seas32. However, exactly the opposite

has been observed in the eastern Mediterranean. From1989 to 1997, benthic bacteria, which in the easternMediterranean, account for most of the total benthicbiomass41, decreased by as much as 90% (Fig. 2a). Thisdecrease was coupled with a large reduction in thetotal number of dividing bacteria and consequently areduced bacterial turnover (which decreased by 50%)36. Bacteria are known to be heavily dependentupon both fluxes in organic C (Ref. 42) and theavailability of labile organic compounds43. However,recent studies have also demonstrated that deep-seabacteria are stenotherms, and display a reduction ingrowth rate with decreasing temperature44.

Reduced bacterial density and activity, togetherwith the trend of decreasing oxygen levels in deepwaters29, have contributed to the reducedremineralization of organic matter and to itsaccumulation in marine sediments. Such significantaccumulation of nonconsumed and/or nonmineralizedorganic loads indicates a modification of the steady-state conditions of the C and N cycles in the deepsea36. After 1994, the physical characteristics of thedeep waters investigated tended to stabilize at newvalues23,27,28. This was reflected by patterns of organicC, the C:N ratio and bacterial density, which alsostabilized during this period45,46, providing moreevidence for a tight coupling between physical andbiological processes.

Climatically driven biological disturbance was alsoobserved for metazoans, and particularly formeiofauna. Meiofauna comprise 22 of the 40 animalphyla and are composed of the small organisms



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Fig. 2. Density of benthicbacteria and meiofaunafrom the sediments of theCretan Sea [at 950 m(squares) and 1540 m(circles)]41,43,46,49,50.(a) Interannual changes inbacterial density inSeptember 1989, 1994,1995, 1997 and March1998 (the exponentialcurve for 1540 m depth isshown); (b) interannualchanges in meiofaunadensity at 1540 m depth inSeptember 1989, 1994,1995, 1997 and March1998. Bars indicatestandard deviations.

With the exception of hydrothermal ventsand cold seeps, deep-sea benthicecosystems depend for their sustenanceon the rain of particulate organic matterproduced in the photic layera. During theirdescent through the water column, sinkingparticles are subjected to a progressivedegradation, which reduces the quantity andquality of the organic material reaching thedeep-sea bed. Only 13%of the organiccarbon produced by photosynthesis in thephotic layer is exported to the deep seasb.These particles are mainly composed ofdead or senescent phytoplankton,zooplankton moults and other debris ofmarine and terrestrial origin. When organicmatter reaches the sediment surface it issubjected to complex biotic and abiotictransformations, which alter its chemicalcomposition, calorific content andnutritional value.

Organic matter is composed of labile(simple sugars, fatty acids and proteins)and refractory (humic and fulvic acids and

structural carbohydrates) compounds invariable proportions. Only labile moleculesare directly utilizable as a food source bybenthic consumers, whereas refractorymolecules require an ageing process andconversion into low molecular weightcompoundsc. This process is largelymediated by bacteria. Organic matter qualityand its potential availability (i.e. its foodvalue for consumers) has historically beendetermined using the carbon:nitrogen(C:N) ratio. As organic N (protein) is morereadily utilized than organic C, low values ofC:N (

(30500 m) that represent the dominant componentamong benthic metazoans in all aquatic ecosystems47.Nematodes account for 7090%of the total density ofdeep-sea meiofauna. Because of their sensitivity tostressful conditions, lack of larval dispersal and highturnover rates, nematodes are considered to be usefulbio-indicators in environmental monitoring48 andcould be used as a model for investigating metazoanresponses to climate change.

After deep-water cooling, the deep-sea meiofaunain the eastern Mediterranean displayed a significantdecrease in density ( 65%, Fig. 2b). The decrease inmeiofaunal biomass was even greater (by 80%)49,50.These data contrast with experimental andobservational research demonstrating an increase inbenthic organisms induced by phytodetritalaccumulation on the sea bed39,40. Despite theincreased organic nutrient availability, changes in thephysical characteristics of the water masses had anegative effect on the metazoan density and biomass.

The observed disturbance of meiofauna in the deepsea has two possible explanations. The first is a directnegative effect of water cooling on benthic metazoans.This explanation is supported by the long-termadaptation of deep-sea organisms to constant

temperature conditions51 the abrupt decrease ofeven a few tenths of a degree centigrade might haveaffected their reproductive potential. The longduration of the deep-water cooling (over two years)enhanced the negative effects of the lowertemperatures, especially on organisms with highturnover rates (nematodes have a short generationtime, ranging from 463 days52: during the coldperiod, there would potentially have been at least 12and possibly over 200 generations).

The effect of temperature changes on deep-seabenthic fauna has been documented in the westernMediterranean, where macrofauna consist partly ofreproductively sterile pseudopopulations that aremaintained by a continuous larval inflow from motherpopulations inhabiting the colder deep AtlanticOcean53. The high temperature and high salinity of theMediterranean bottom waters is thought to hamperthe successful establishment of species arriving fromthe colder oceans. The same phenomenon has recentlybeen observed in other areas of the Mediterranean (inthe Ligurian and Tyrrhenian Seas), where theestablishment of macrobenthic pseudopopulationsand the mortality and/or introduction of certainspecies was attributed to temperature changesinduced by climate forcing54.

An alternative explanation for the observed climatechange-induced impact on nematodes is the reductionof the microbial biomass and activity48. Becausenematodes, particularly in the deep sea, are eitherspecific bacterial feeders or general microbial feeders,it is possible that the strong reduction of microbialbiomass resulted in a reduction of suitable organicfood sources.

From the overall deep-sea response to climatechange in the eastern Mediterranean (Fig. 3), it isevident that the climate change taking place therehas had direct (biological disturbance) and indirect(altered biogeochemical cycles) effects on the deep-seaecosystem. These effects are expected to be differentfrom those of deep-sea ecosystems that are subjected toclimate-induced warming. El Nio events in the easternPacific, with rising sea surface temperatures, cause adeepening of the mixed layer, decreased nutrientconcentrations in the surface waters, and reducedprimary production and export of organic materialtowards the sea bed7,9. During these warming events,therefore, deep-sea benthic ecosystems are likely to besubjected to more oligotrophic conditions as a result ofaltered plankton food-web structure. In this regard,recent studies carried out in the North Pacific haveshown that, since the late 1970s, the increased seasurface temperature (1.53C) has altered the surfaceproductivity, reducing the supply of organic matter tosediments. These studies conclude that climatechange has had a greater effect on benthic oxygenlevels than changes in ocean circulation patterns55.

Another potential source of change in deep seas,which can bias the interpretation of the relationshipbetween climate change and ecosystem response, is the



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Fig. 3. Conceptual modelof direct and indirecteffects of climate-inducedchange on the deep-seaecosystem of the easternMediterranean.

presence of anthropogenic disturbance, either fromconstruction activities on the shore, from resourceexploitation or from other sources56. None of thesecauses were evident in the deep eastern Mediterraneanduring the decade of observation. However, the growingdirect human impact on oceanic systems has to be takeninto account in future studies as a potentially importantsource of change in deep-sea ecosystem function57.

When studying causeeffect relationships betweenvariables, as in the case of the ecosystem response toclimate change, high-quality data are essential. Inparticular, investigations of the benthic compartment(owing to the bidimensional characteristics of thesubstrate) require that seasonal and spatialvariability are taken into account as anotherpotential source of bias (Box 2).

ProspectsThe effects of climate change on the oceans should beseen from both top-down and bottom-up perspectives.The increasing frequency of many deep-seaorganisms recorded in shallow waters during the pastthree decades, possibly induced by climate change25,confirms the existence of bidirectional interactionsbetween the surface and deeper waters. However,because of the lack of information, it is not clearwhether the deep sea responds rapidly to climatechange or if there is a lag period. As residence times ofdeep waters are of the order of several decades, recentstudies have suggested that there should be a lag and

that deep-sea organisms respond to climate changesthat occurred several decades ago25. However, theresponse from a miniature ocean model indicates thatclimatic change could have a more rapid effect ondeep-sea ecosystem functioning.

From the information available, it is emerging thatdeep-sea ecosystems are fragile and that deep-seacommunities are extremely sensitive to a wide rangeof disturbances24. Even relatively small changes inthe physical characteristics of deep waters mightalter the steady state of important biogeochemicaland functional variables. There is still littleinformation about the long-term (i.e. decades tocenturies) variability of several deep-sea parameters(e.g. temperature, salinity, bottom currents, organicand inorganic nutrients) and, without knowing aboutlong-term trends, the effect of climate change on deep-sea ecosystem functioning cannot be predicted.Recent studies of deep-sea coral banks indicate thatthese colonies, which have lifespans of severalcenturies, can provide deep-sea records of climatechange58. This promising new information shouldsatisfy the need for long-term data on changingclimatic conditions, but the deep-sea ecosystemresponse to such changes is still largely unknown.

As deep seas cover over 50%of the surface of theEarth and drive biogeochemical cycles on a globalscale, investigating climate-induced changes in thedeep sea is crucial to our understanding and ability topredict the consequences of climate change.



509Review

Spatial heterogeneity is an importantsource of variability of benthic parameters.In deep-sea sediments, chemical elementsand living organisms can display a patchydistribution. The distribution of chemicalelements is largely driven by physicalprocesses (e.g. bottom currents andbenthic storms), whereas the distributionof the living biota is also controlled bybiologically mediated disturbances(e.g. predation), which createenvironmental heterogeneity favouringthe aggregation of organisms. Theseprocesses occur at different spatial scales.At a large scale, physical processes are themain factors that regulate the distributionof benthic parameters, whereas at the localscale, the complex biological interactionswithin the food web dominatea.

Investigations carried out in the easternMediterranean have revealed an extremelylow micro- (i.e. at the cm scale betweensediment cores taken from the same area)and mesoscale (i.e. 1100 m scale in corestaken from different areas) spatial variabilityof the sediment parametersb. In addition,

no statistically significant differences havebeen observed on a larger spatial scale(i.e. at the km scale, between samplingsites at similar depths)c.

The temporal variability of chemicalelements and living biota in deep seas arelinked to the organic matter produced inthe euphotic zone. The fraction of thisproduction that escapes the euphotic zoneas particulate organic matter sinking intothe deep sea also exhibits temporalvariability, reflecting the changes insurface water production. Long time seriesmeasurements of particulate fluxes andbenthic variables (e.g. phytodetritusdeposition, faunal density and biomass andcommunity structure) in the deep sea haverevealed the presence of seasonal andinterannual changesd. Interannualvariability of biological processes generallybecomes larger than seasonal variabilitywhen relevant interannual changes inenvironmental conditions occur as a resultof episodic or stochastic events, or long-term climate change. Temporal analysisand comparisons between seasonal and

interannual changes clearly indicate thatthe deep-sea ecosystem of the easternMediterranean exhibits limited variabilityamong seasons that is almost negligiblecompared with changes observed onlonger timescales (i.e. over a decade)e.

Referencesa Schaff, T.R. and Levin, L.A. (1994) Spatial

heterogeneity of benthos associated withbiogenic structures on the North Carolinacontinental slope. Deep Sea Res. II 41, 901918

b Danovaro, R. et al. (1998) Heterotrophicnanoflagellates, bacteria and labile organiccompounds in continental shelf and deep-seasediments of the eastern Mediterranean.Microb. Ecol. 35, 244255

c Danovaro, R. et al. (1995) Meiofauna of the deepEastern Mediterranean Sea: distribution andabundance in relation to bacterial biomass, organicmatter composition and other environmentalfactors. Progr. Oceanogr. 36, 329341

d Smith, K.L. and Druffel, E.R.M. (1998) Long time-series monitoring of an abyssal site in the NEPacific: an introduction. Deep Sea Res. II 45,573586

e Danovaro, R. et al. (1998) Long-term changes indeep-sea benthic ecosystems: the easternMediterranean case. In Variability of theMediterranean Sea (Lykoussis, V. andSakellariou, D., eds), pp. 202203, NCMR Press

Box 2. Spatial heterogeneity and temporal variability in deep-sea sediments

AcknowledgementsWe thank A. Theocharis forproviding information onclimate-induced physicalchanges, F. Azam,G. Bavestrello, F. Boero,O. Carnevali, C. Cerrano,N. Della Croce,A. Eleftheriou, L. Ferrante,S. Fraschetti, C. Gambi,P. Giordani, E. Ignatiades,D. Marrale, E. Olmo,W. Roether, A. Russo,M. Serresi and twoanonymous reviewers fordiscussion andconstructive comments onthis article. This study wassupported by EuropeanUnion CINCS(pelagicbenthic couplingin the oligotrophic CretanSea) and MATER (masstransfer and ecosystemresponse) programmes.

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