53402

What Structures Marine Biodiversity and why does it vary?

C. Heip

Centre for Estuarine and Coastal Ecology, Netherlands Institute of Ecology, NL-4400 AC Yerseke, The Netherlands corresponding author (e-mail):[email protected]

Abstract: Marine ecological biodiversity research is a scientific field with few observational data to support a weak theory largely borrowed from terrestrial ecology and lacking in experimental verification. The relative lack of scientific interest and effort until recently was a consequence of the general feeling that marine biodiversity is far less threatened than terrestrial biodiversity. This view is not sustainable. There is now ample evidence of widespread changes in most coastal habitats in populated areas around the world (coral reefs, mangroves, seagrass fields, intertidal rocky shores and subtidal sediments on the continental shelf and margin) due to exploitation of marine resources, introduction of exotic species and the increased pressure from mariculture and fisheries. The sustainable exploitation of the seas requires development of a sound theoretical framework for marine biodiversity, including genetic, species and habitat diversity and especially the relationships between them. At the present state of knowledge such a general theory is still far from being reality. In this paper an overview is given of the main elements that an ecological theory of species diversity should include and what aspects of human pressure on the biodiversity of marine ecosystems should be given priority attention.

Introduction

The very rapid and widespread changes due to a far and perhaps an elusive goal. Even the basic human activities in the abundance and distribution job of providing an adequate description of biodi- of biological species that have been documented versity is far from done. On the one hand there is over the last decade have raised the question still a major effort required in scientifically describ- whether these changes in biodiversity have impor- ing the species that inhabit the seas and much con- tant consequences for ecosystem functioning. Eco- cern has been expressed about the shear number of systems perform a series of vital functions for hu- undescribed species and the decline of taxonomic man society, many of which depend on a variety expertise. On the other hand we are at the dawn of of organisms present in a variable environment. unprecedented progress in charting and explaining The relationships between biodiversity and ecosys- genetic diversity in the oceans. For the first time the tem functioning are far from clear and before this prospect of a complete inventory of marine micro- issue can be properly rj::searched a number of more bial populations is no longer utopic. The research basic questions have still to be answered. that will be required to couple knowledge on genetic In current thinking biodiversity equals biologi- structure to the functioning of marine systems will cal variability, from genes to specie~ and habitats take many years and even decades to be accom- within ecosystems. The mech~nisms' that generate plished. The genomes of about 300 species will be and maintain variation at these different levels in characterized in the near future, but only very few the organisation of the biosphere are very differ- of them are relevant to marine ecology; so, although ent. A single coherent theory ofbiodiversity change the start has been taken, the work is only beginning. and maintenance will have as a major challenge the It is clear that many basic facts are missing and linking of these mechanisms over the spatial and that it will require many years of scientific effort to temporal scales at which they operate. This is still obtain them. This task can only be accomplished in

From WEFER G, LAMY F, MANTOURA F (eds), 2003, Marine Science Frontiers for Europe. Springer- Verlag Berlin Heidelberg New York Tokyo, pp 251-264

Publication 2891 Netherlands Institute of Ecology (NIOO-KNA W)

------~

252 Heip

a fruitful way if a coherent and testable theory on which organisms have to adapt without being able marine biodiversity will be constructed over the next to modify them. To include habitats in the biodi- few years. Whether a unified theory on biodiversity versity concept is therefore a far from simple task, should be based on characteristics of individual or- although the debate is part of the marine ecologi- ganisms, including their genetic composition, or on cal literature at least since Sanders (1968) in the species or communities in landscapes remains an frame of the stability-time hypothesis discussed open question. The most easily recognized opera- the difference between biologically and physically tional building block in the biodiversity hierarchy is dominated communities. the individual organism, which is often ignored in Although it would be fascinating to summarize marine ecology. All individual organisms are differ- the processes that structure and change genetic, ent to some extent, even in clonal species. The po- species and habitat variability, and to try and link tential genetic diversity present in populations is them, the task would be far outside the scope of this much large~than the number of individuals in which paper. Even restriction to the classical use of the it is expressed and each generation in a sexually term biodiversity - species diversity - requires reproducing population is a new and unpredictable addressing nearly the whole field of ecology. This sample from a very large gene pool. In a recent paper, is clearly impossible and I will restrict myself to a Pachepsky et al. (2001) present a framework for series of headings indicating what we should con- studying the dynamics of communities which sider to know in order to describe and explain ma- generalises the prevailing species-based approach to rine biodiversity and a short summary of what is one based on individuals that are characterised by known under that heading. I have heavily borrowed their physiological traits. from a number of review papers that appeared At the habitat or ecosystem level as well, there during recent years and that show the explosive is an important random element due to the unique growth of interest in the subject. I also refer to the and unpredictable geological setting in which eco- book ofOrmond et al. (1997) for an important col- logical processes take place. When one discusses lection of papers that cover many aspects of ma- characteristics and changes in habitats, a review rine biodiversity that are ignored here, e.g. phylo- would have to address the. complex physical, genetics and evolution. biogeo-chemical and geological processes and es- pecially their interactions that structure landscapes Is marine biodiversity special? in the sea, including the pelagic environment, and that can operate at very different time and space The theoretical foundations as well as the experi- scales. The newly coined term 'biogeomorphology' mental approach required to understand marine probably comes closest to what kind of questions biodiversity are very poorly developed, in general we have to formulate, at least for the sea floor. The and also when compared to terrestrial ecology. In interactions within biofilms and microbial mats, the fact, the whole literature is so much dominated by biological impact on sediment characteristics such theory developed for terrestrial ecosystems that one as bottom roughness, the structure of the benthic can scarcely speak of a field of marine biodiversity. boundary layer and benthic-pelagic coupling are ex- An important part of this theory has been devel- amples of research areas where a close link between oped by plant ecologists (e.g. Loreau 2000 for an biology and geology exists. Coral reefs in the trop- example) and its application to the oceanic envi- ics are the most prominent case of an environment ronments is of course problematic. One basic ques- nearly completely created by biotic processes, and tion is whether terrestrial and marine systems are several less spectacularreefforming organisms are similar enough to allow theory from one domain active in temperate waters, including maerl forming to be used for the other. Most probably this is not red algae, molluscs and polychaetes, deep water the case. Marine systems have a series of charac- corals and others. At the other extreme we have teristics which distinguish them from terrestrial environments such as sandy beaches which are systems, as explained in the following box (from nearly completely built by physical forces and to Heip et al. 1999). What Structures Marine Biodiversity and why does it vary? 253

Box 1. The distinctive features of marine biodiversity

1. Life has originated in the sea and is much older in the sea than on land. As a consequence, the diversity at higher taxonomic levels is much greater in the sea where there are 14 endemic (unique) animal phyla whereas only 1 phylum is endemic to land. There is also a remarkablediversity of life-history strategies in marine organisms. The sum total of genetic resources in the sea is therefore expected to be much more diverse than on land. 2. The physical environment in the oceans and on land is totally different. Marine organisms live in water, terrestrial organismslive in air. Environmental change in the sea has a much lower frequency than on land, both in time and in space. 3. Marine systems are more openthan terrestrial and dispersal of species may occur over much broader ranges than on land. Although most species in the ocean are benthic and live attached to or buried in a substratum, in coastal seas a very large proportion of them has larvae that remain floating in the water for days to months. These high dispersal capacities are often associated with very high fecundities and this has important consequences for their genetic structure and their evolution. 4. The main marine primary producers are very small and often mobile, whereas on land primary producers are large and static. The standing stock of grazers is higher than that of primary producers in the sea, the opposite to the situation on land. Ocean productivity is on average far lowerthan land productivity. In the largest part of the ocean, beneath the shallow surfacelayers, no photosynthesis occurs at all. 5. High level carnivores often play key roles in structuring marine biodiversity and yet are exploited heavily with unquantified but cascading effects on biodiversity and on ecosystem functions. This does not occur on land, where the ecosystems are dominated by large herbivores and, of course, increasingly by humans which monopolise about 40 % of the total world primary production. 6. A greater variety of species at a higher trophic level is exploited in the sea than on land: man exploits over 400 species as food resources from the marine environment; whereas on land only tens of species are harvestedfor commercial use. Exploitation of marine biodiversity is also far less managed than on land and amounts to the hunter-gatherers stage that humans abandoned on land over 10,000 years ago, yet exploitation technology is becoming so advancedthat many marine species are threatened to extinction. Insufficient considerationhas been given to the unexpected and unpredictable long-term effects that such primitive foodgathering practices engender., ' 7. All pollution (air, land and freshwater)ultimately enters the sea. Marine biodiversity is thus most exposed to and criticallyinfluences the fate of pollutants in the world. Yet marine species are probably least resistant to toxicants. The spread of pollutants in marine food chains and therefore the quality of marine food is uncontrollable by man.

-- 254 Heip

There is (probably) less species diversity and smallest animals described by May (1975). Again, more genetic diversity in the marine environment it is unclear whether this pattern holds for the ma- than on land. If one looks at the arthropods, the rine environment where two groups of small to very insects and chelicerates on land and the crustaceans small marine animals exist that are claimed to be in the oceans, the difference is striking. A single the most numerous animals on earth, the copepods tree in the tropical forest may harbour over a in the plankton and the nematodes in the benthos. thousand species of insects. The entire planet Especially in the ne~atodes and other groups of the harbours eighty species of euphausiids. This indi- meiofauna, the tendency to mineraturisation allows cates that the mechanisms of speciation are very the exploitation of niches within finely grained en- different in the sea and that resource competition vironments and consequently an increase in local does not constitute a dominant selective pressure, biodiversity. although in fine-grained environments such as ma- A striking characteristic of marine species diver- rine sediments there are - as expected -more spe- sity is that, whatever the number of species, at the cies than in the water column. The upper water higher taxon level the marine environment is column has a very dominant vertical gradient in certainly much richer than the land. Of the 33 ani- light availability and nutrient concentration and, at mal phyla, only five do not occur in the seas and 13 least in some groups mostly from the micro- and are endemic to it (Grassle et a1. 1991). This implies picoplankton, more species may exist in the plank- that genetic, biochemical and physiological diver- ton than one may expect. This was called the para- sity is also much higher in the oceans than on land dox of the plankton by limnologist GE. Hutchinson (Lasserre 1992). The recent discoveries by using (1959) and was later applied to the marine envi- molecular markers of many new archaea and bac- ronment by Margalef(1968). However, no studies teria, and three new entire classes of marine algae have attempted to define resources in the sea at the prove that the same probably holds for microbiota same level of detail as is customary in the terres- and plants. What the consequences of this high trial environment. The distinction between differ- genetic diversity are for ecosystem functioning and ent food species during different phases of the life whether this larger genetic pool provides a better cycle, or the view that different parts of food buffering capacity for change is not known. species may offer different resources allowing for Coastal environments at the largest spatial specialization and speciation has not been tested. scales are discrete units separated from similar Overall, the smaller number of marine species, units by other types of environment. Even the when confirmed, make it reasonable to assume that pelagic environment can be termed discrete on the the mechanisms of diversity generation and main- global scale. At the other side of the spectrum are tenance are (very?) different. coastal lagoons and salt marshes that are very small One area where this generalization was not and sometimes very far away from each other but confirmed by reality was the deep-sea, where un- often contain very similar faunas and floras. Small til 1968 the general consensus was that species islands and estuaries fall somewhere in between. numbers were low. In that year Sanders (1968) It is clear that fragmentation has to be considered showed that, on the contrary, the deep-sea is very as a function of the genetic and ecological disper- species rich when compared to shallower waters sal capacity of species. Marine plant and animal and estuaries. This' he attributed to the constant and species have developed efficient strategies to be very old deep-sea environment which would allow able to colonize such habitats. Knowledge on dis- for large diversification and specialization and con- persal and life-history in general of many marine sequently narrow niches, a concept he called the plants and animals remains vert scarce. Even stability-time hypothesis. knowledge on distribution of almost all marine Another generalisation that was derived from species is fragmented and has not received much terrestrial studies is the lower diversity among the attention in the last decades. What Structures Marine Biodiversity and why doc:s it vary? 255

What is marine biodiversity? vaste geographical distributions. There are distinct oceanic spatial patterns of species diversity and these As the study of genetic and habitat diversity in the are large and few in number. These patterns are sea is only just starting, I will restrict this discus- correlated with the size and shape of the great sion to species diversity. Species diversity can be oceanic gyres and the equatorial currents and studied globally (i.e. the total number of existing counter currents. Smallerscale circulation patters, species), region ally or locally (the number ofspe- such as mesoscaleeddies,rings and the circulation cies occurring in a region, habitat, patch etc.). Glo- in small basins, do not seem to have.providedthe bally, at our present state of knowledge, marine same degree of persistence of habitat features species diversity appears to be low. There are prob- required for the coevolution of the diversity of ably about 7-8 million eukaryote species on Earth, species that is required for the establishment of although some authors claim higher numbers ono functional ecosystems (McGowan and Walker and even 100 million species. Most of those spe- 1993). cies (85 %) are terrestrial and most of them are As a consequence, species diversity in the oce- animals. About two thirds of all species occur in anic pelagic environment is extremely low. The the tropics, largely in humid forests. Out of these number of speciesin the upper 200mof the pelagic 7-8 million species, about 2 million have been sci- oceanicenvironmentiswellknown for fourgroups entifically described. of animals, the Euphausicacea, Chaetognatha, It is not well known how many marine species Pteropoda and Copepoda, which dominate the have been described. In the literature figures vary biomasseverywhere. There are only 80 species of between 200,000 and 500,000 marine animal spe- euphausiids, 50 of chaetognaths, about 40 of cies. Described species of marine viruses and mi- pteropods and less than 2,000 for the most diverse cro-organisms (bacteria, fungi, protozoans, micro- group,the calanoidcopepods.These dataare based algae) number in the thousands and perhaps 20,000 on more than 20,000 net tows and, although new marine plant species are described; the marine specieswill certainly continue to be discovered, it plant inventory must be more complete than that is obvious that pelagic biodiversity is of another of the animals, since there are no deep-sea plants. order than both terrestrial and marine benthic di- One of the most striking characteristics of ma- versity (McGowan and Walker 1993). rine biodiversity is the difference between the This lownumber of (animal)species isin strik- benthic and the pelagic environment. The pelagic ing contrast with the diversity of animals in oceanic environment is the largest habitat on earth; sediments. About 200,000 species are currently it is immense. It has very strong vertical gradients, known from benthic environments, most of them in light and temperature, in nutrients and in food, have been described from coral reefs, and only typically in scales of tens to hundreds of meters, but about 60,000 are known from soft bottom habitats sometimes much less. It has also important that cover most of the earth's surface. Benthic horizontal gradients existing over very large scales, species from the temperate shallow waters of hundreds to thousands of kilometres. The pelagic Europe are reasonable well known, especially in environment has been called coarse grained and the larger macro- and megafauna. The smaller uniform, but this has been contested by phyto-plank- meiofauna (mm sized animals) is less well de- ton and microbiid ecologists, who at the one hand scribed and a survey of the benthos in the North have described the paradox of the (phyto) plankton Seain 1986yieldedabout40 % ofbenthic copepod already mentioned and on the other have recently species new to science (Huys et al. 1992). discovered and discussed the very fine scaled Forthe continentalmarginandthe deep-sea,the gradients around bacterial and phytoplankton cells state of knowledge is poor. As an example, in the (Azam et al. 1994). Still, pelagic animal species are very extensive EU-OMEX programme on the grouped in clearly evident assemblages and all show Goban Spur continental margin it was often not

------

256 Heip

possible to name even dominant species of the In view of all these uncertainties, it is still pre- macrofauna (Flach et al. in press). Consequently, mature to give reliable estimates of the species there has been much debate recently on the number number in the marine benthos, but there may be of marine benthic species that is to be expected. severalmillions.Marinesedimentsare finegrained Numbers such as 108nematodes species globally environments with gradients in the order of have been published in the literature, although millimetersand centimetersin the verticalandcen- without proper justification. The main argument timetres to metres in the horizontal. It is to be ex- for a high number of undescribed species in the pected that the mechanisms of speciation are very macro-benthos comes trom a survey of Grassle and different in marine sediments than in the pelagic Maciolek (1992). The survey covered ten stations environment. This is well illustrated for instance sampled with a grab along 176 km of the 21OOm by marinenematodes,wheremany congenericspe- isobath (depth contour) off the east coast of the US cies may be found together in a single sediment and four additional stations at depths of 1500m and core, each living at a certain depth horizon only 2500m. In the ten stations a total of 798 species millimetres apart (Soetaert and Heip 1995; Heip representing 171 families and 14 phyla were iden- 1996). tified on a total sampled surface of21 m2.Of these species, 460 (58 %) were new to science. About Patterns of species diversity 20 % of the species were found at all ten 21OOm stations and 34 % occurred at only one station. Of Before we can answer the question why biodi- the total soft-sediment fauna 28 % of species oc- versity varies, we need to know the basic patterns curred only once and 11 % only twice. The number of its distributionin space andtime. The most fun- of species found increased continuously as more damental data of diversity are the numbers of spe- samples and individuals were collected. At a sin- cies in differentplaces.This is afundamentalprob- gle station species were added at a rate of about lem for marine biodiversity studies because this is 25 per 0.5 m2.When samples were added along the largelyunknown.There are someexceptions,such 176 km transect the rate of increase was about 100 as some animal groups from the zoop1anlcton,a species per 100 km. The rate of increase across number ofplant andanimal speciesfromintertidal depth contours is even greater. Since the deep-sea and shallow subtidal zones, and increasingly the at depths greater than 1000m occupies about 3.108 microbiota and fauna from hydrothermal vents. km2 of the earth's surface, if a linear addition of But we know next to nothing about the distribu- one species per km is extrapolated to 1 species per tion and the dynamics of the large majority of km2, the global deep-sea macrofauna would species living in the sediments covering millions contain on the order of 108species. Taking into of square kilometers of the deep-sea floor. account the fact that the deepest, oligotrophic areas Terrestrialecologistshaveused geographicdis- of the ocean floor have densities of macro-fauna tributions of species extensively andhave discov- of about one order of magnitude lower, this may eredrelationshipsbetween these dataand latitude, be reduced to 107 species. This estimate depends climate,biological productivity, habitat heteroge- on the hypothesis that rare species are different in neity,habitatcomplexity,disturbance,andthe sizes different areas and May (1992) pointed out that, and distances of islands. Several of these relation- since half of the species found in the Grassle and shipshavesuggestedmechanismsthat might regu- Macio1ek (1992) study were known to science, late diversity but in the terrestrial environment as the .implication that the total number of species well a general andcomprehensive theory of diver- is double the number of species described also sity accounting for most or all of these relation- provides some kind of (minimum) estimate, that ships does not exist. is two orders of magnitude lower. Again its accu- Spatial scale is the overriding variable that racy depends on whether the rare species are the needs to be considered when discussing the same ones in different localities on earth. changes in diversity and what are their causes. What Structures Marine Biodiversity and why does it vary? 257

Definition of scales is not straightforward, neither its size, the physical, geological and chemical in terrestrial nor in aquatic environments. Scales environment,otherspeciesoccurringin the area, its are often definedfromthe perception of the human distance to other areas etc. There is thus a large observer and less as a function of the species number of very different factors that determine or communities considered. It is customary to whether a species can exist andmaintainitself in a distinguish between local, regional and global certain habitat. Because theory has often concen- spatial scales. Locally, species diversity in any trated on only one or a few of those factors, it is very locality is seen asa balancebetween two opposing difficultto presenta comprehensivepictureof what forces. On the one hand local abiotic processes, generatesand maintainsmarinebiodiver-sity. interactions between species and chance tend to Most of the ideas on this topic again have their reduce diversity; on the other hand immigration originin empiricallyobservedpattems.Speciesrich- from outsidethe localitytendsto increasediversity. ness appears to be related generally to climate Each local population is seen as a sample from a (Terborgh1973).Inparticular,conditionsthat favor larger speciespool. Theories on larger,mesoscale biological production - warm temperatures and patterns take migration and dispersion explicitly abundantprecipitationinterrestrialecosystems-are into account. The metapopulation concept and often associated with high diversity. In aquatic connectivity of land (sea)scapes are central in systemsthis generalizationprobablydoesnot hold. this approach. Global patterns are for instance Highly productive ecosystems, such as occur in latitudinal gradients. Within most groups of upwelling areas or as a consequence of eutro- terrestrialorganisms,thenumber ofspeciesreaches phication, are not linked to temperature and they its maximum in tropical latitudes and decreases oftenhold a limited number of species. both northward and southward toward the poles. A striking pattern is the connection between In many cases,the latitudinal gradient in diversity diversity and habitat complexity.Salt marshes are is very steep. Tropical forests, for example, may extremely productive but harbor few species of support ten times as many species of trees as forests plants and animals; deserts occupy the other end with similar biomass in temperate regions (Latham of the productivity gradient but may support a di- and Ricklefs 1993). verse flora and fauna. Regional or landscapecom- Since many factors vary in parallel with latitude plexity has also been implicated in patterns of di- the causal mechanisms that explain such patterns versity. Ecologists have long been aware of the are difficult to distinguish and, moreover, nearly greaterdiversityofmountainousregionscompared all studies are from terrestrial environments. In ma- with flatlands (Simpson 1964),or of rocky versus rine communities, the existence of such patterns sandyshores.This pattern may arisebecauseof the over large geographical scales has only rarely been increased numbers of species distributed studied (Rex et al. 1993). Whether they are as wide- allopatrically on isolated mountains or in isolated spread as in the terrestrial environment is question- valleyson the land,or in sandypockets,tidal pools, able, but even in terrestrial environments the gen- crevices etc. of rocky shores. eral trend in diversity is sometimes reversed, as it The influence of geography on diversity has is for shorebirds, parasitoid wasps, and freshwater long been apparent in island settings, where the zooplankton, of which more species occur at high number ofspeciestendsto increasewith island size and moderate latitudes than in the tropics. These and to decrease with distance from sources of counterexamples may reflect the latitudinal colonists (Hamilton et al. 1963; Connor and distribution of particular habi~at types, the history McCor 1979; Abbott 1980). MacArthur and of the evolution of a taxon, or ecological circum- Wilson's(1963, 1967)theory portraying diversity stances peculiar to a particular group. on islands as a balance between colonization and extinction emphasized the influence of both What structures species diversity? local and regional processes on the diversity The number of species co-occurring in a certain area of local communities. The theory of island bio- depend on the characteristics of that area: its history, geography can readily be applied to coastal ------

258 Heip

environments (estuaries, lagoons, beaches, rocky made an important contribution to explain observed shores) but as well to isolated deep-sea environ- distribution patterns of species, one of the main ments such as deep-sea mountains and hydrother- contributions 1T0mmarine sciences to general eco- mal vents. logical theory. The greatest effect of disturbance is Other processes implicated in the regulation of at intermediate levels because a high level of diversity have occurred to ecologists as a result of disturbance precludes many species and a low level more theoretical considerations. These include carmot prevent competitive exclusion by the supe- density-dependent predation (Paine 1966; Janzen rior competitor. The theory is based on work in 1970), and temperal and spatial stochasticity (Levins rocky intertidal communities by Gonnell (1975) 1979; Chesson and Warner 1981; Thiery 1982; and Paine (1966), who showed that when these Clarke 1988). Theories based on these processes communities are left undisturbed they become obtain little empirical support from geographical eventually dominated by a single dominant patterns of diversity because ecologists lack a competitor. Disturbance, either by a physical event general understanding of the geographical distribu- such as a storm, or by the appearance of a predator, tion of these factors. That ecologists generally have allows more species to co-exist with the dominant a higher regard for empirically based hypotheses, competitor. The intermediate disturbance emphasizes our difficulty in distinguishing between hypothesis is closely linked with the succession phenomena as inspirations for hypotheses and as theory of Clements (1935). Landscapes typically tests of the mechanisms proposed to explain them include a mosaic of patches of disturbance of (Schluter and Ricklefs 1993) different extent and intensity such that each patch Early in the previous century, species diversity exists in some stage of succession, out of was regarded primarily as reflecting the accumu- equilibrium with the prevailing climax in its species lation of species over time, and thus largely an evo- composition (Watt 1947). Thus, the entire mosaic, lutionary subject. By the early 1960s, diversity had which is part of a larger regional equilibrium, come to be perceived as the outcome of ecologi- contains more species than any individual patch. cal interactions, particularly competition, that were Such species may form metapopulations, inhab- resolved within small areas and habitats and over iting suitable patches in fragmented landscapes and short time scales (MacArthur 1972). This is re- linked by migration. Most of metapopulation theory flected in the niche theory. This theory predicts has been developed for the terrestrial environment. that stable coexistence between species depends The most basic aspects have been analysed with on each being a superior competitor in its own simple spatially implicit models such as the Levins niche. The more niches there are in a certain habi- model in which a fraction h of the habitat patches is tat, the more species can co-exist. Complex habi- suitable for occupancy, the equilibrium fraction of tats will provide more niches and therefore more patches occupied out of suitable patches is given by room for more species. Niches may also change p* = 1- 8/h, where 8 is the ratio of the extinction to temporally, allowing for seasonal succession of the colonization rate. A spatially realistic model for species. The problem is that many species depend a finite number of habitat patches of known areas on the same resources and acquire them in a lim- and spatial locations can be constructed by ited number of ways and niche overlap is conse- modelling the rate of change in the probability that quently high so that exclusion of all species except a patch is colonized. Extinction rates are considered the superior competitor should be the result (see to be inversely proportional to the area of the patch however Huisman and Weising 1999). To over- and colonization rates depend on the distance come this difficulty a series of hypotheses have between patches and the migration distance of a been advanced relying e.g. on niche separation in species (Hanski and Ovaskainen 2000). time and space with consequent smaller overlap of Iflandscapes are mosaics and populations dis- species on relevant niche axes. perse over them in a random matter, habitat loss Such separation may be due to disturbance and will inevitably lead to species loss. To convert the so-called intermediate disturbance theory has habitat loss to species loss the principles of island What Structures Marine Biodiversity and why does it vary? 259 biogeography are applied. The relationship nature of spatial heterogeneity. A habitat may be between species and island area is nonlinear and more heterogeneous to a small organism than to a from this one can predict how many species should large one. May suggested that the quantitative re- become extinct as the size of the islands shrinks. lationship between organism size and habitat het- These doomed species do not disappear erogeneity, which may be represented by the fractal immediately however. The term extinction debt has dimension ofthe habitat, might help to explain the been coined to demonstrate the idea that many of large number of small-sized animal species. This the species present nowadays are doomed for idea was recently taken one step further by Ritchie immediate (in geological terms) extinction, even and 0Iff(1999) who discuss how many patterns of if conservation measures are taken. In this category biodiversity can arise from simple constraints on are 12 % of all plants and 11 % of all bird species how organisms acquire resources in space. These on earth (Hanski and Ovaskainen 2000). patterns include well-known responses ofbiologi- In terrestrial environments such calculations cal diversity to different factors such as the number show that on the order of thousand species per of available niches in space, productivity, area, decade per million species go extinct. However, body size and habitat fragmentation. Ritchie and this process is not spread evenly over the globe. 0Iff(1999) use spatial scaling laws to describe how Myers et al. (2000) have shown recently that species of different sizes find food in patches of roughly 30-50 % of plant, amphibian, reptile, bird varying size and resource concentration. From this and mammal species occur in 25 biodiversity they derive a mathematical rule for the minimum hotspots that occupy no more than 2 % of the ice- similarity in size of species that share these re- free land surface. The oceans are not included in sources. This packing rule yields a theory of spe- this analysis, but species dependent on coral reefs cies diversity that predicts relations between diver- are similarly concentrated. It is clearly one of the sity and productivity. The theory also predicts re- urgent tasks for marine biologists to come up with lations between diversity and area and between reliable estimates of the danger of species diversity and habitat fragmentation. Thus, spatial extinctions in the marine environment scaling laws provide potentially unifying first prin- One factor that clearly influences extinction ciples that may explain many important patterns of rate is body size. The vast majority of the earth's species diversity. animals have relatively small body sizes; there are far fewer species with large body sizes. The reason The influence of humans: is marine for the smaller number of large-bodied animals biodiversity threatened? may be the higher extinction rates oflarger species associated with their lower population density. Al- Loss of biodiversity is now occurring on a scale though smaller and more numerous organisms which is without precedent in the last 65 million should experience lower extinction rates, they also years. Most concern about elimination of genetic, may experience greater population fluctuations for species, and ecosystem diversity has focused on several reasons. First, on average, smaller organ- the terrestrial realm. It is now clear that marine isms have greater maximal population growth ecosystemsunder human pressure are also at risk, rates, which may give them a greater tendency to including estuaries, coral reefs, seagrass beds, oscillate (e.g. May 1975). Second, smaller mangrove forests, intertidal shores, and continen- organisms also have shorter lifespans and a lower tal shelves and slopes worldwide. ability to store resources, and thus live in a more At firstsight,it seemsreasonableto assumethat unpredictable environment than do larger the sea's extent makes it less vulnerable than for- organisms. Greater population fluctuations should ests. The world ocean, covering 361 x 106km2to increase the chance of extinction. an averagedepthofnearly4 kilometers,constitutes May (1986) offered several explanations for the more than 99% of the biosphere permanently in- larger number of smaller species, including the habited by animals and plants. In contrast, forests possibility that it might be caused by the fractal and woodlands cover 38 x 106km2,or 7.5% of the 260 Heip

Earth's surface (Carlton et al. 1999). However, the disease to occur and the microbizationof the most productive marine ecosystems, the world's coastal ocean as well as the consequences of cli- continental shelves, cover 28 x 106km2, less than mate change should not ignore the disappearance the area covered by forests. The most charismatic of the larger species. marine ecosystems, including coral reefs, kelp for- A large proportion of the world's fish catch ests, seagrass beds, and mangrove forests, consti- comes from continental shelves. Many fishing tute a very small portion of the sea. Coral reefs, methods are harmful because, in addition to killing which are considered the marine equivalents of target species and those incidentally brought on tropical forests, occupy only 0.6 x 106km2, or 0.1 deck (by catch), they severely disturb the seabed %, of the Earth's surface, a small fraction of the and organisms that provide food and hiding places. 12 x 106km2 of closed tropical forests (Carlton et Trawling and dredging have been used for a long al. 1999). time on smooth, shallow bottoms near industrial- That the sea is not immune to extinctions is ized nations. With the hugely increased engine clear from the geological past. At several times in power of modem fishing vessels, trawling can now the history of the planet more than 80 % of the be practiced on nearly any bottom type, with the marine biota got extinct in a relatively short time. exception of stony areas and around obstacles such Marine organisms are often thought to be less as ship wrecks, not only in shallow water on the prone to extinction because of having widespread continental shelf but increasingly in deeper waters, popu-lations and wide dispersal by ocean currents, including the upper continental slope, and sea- or because they live in refugia from human preda- mounts from subpolar to tropical waters (Carlton tion. Only a few marine extinctions are docu- et al. 1999). mented, but this is hardly surprising. Few scien- The effects of mobile gear on seabed biota re- tists work on marine extinction issues. As with the semble those of clearcutting in forests, removing once abundant and widespread eelgrass limpet, the the complex structures that are hiding and feeding extinction of which went unremarked for more places for many species (Carlton et al. 1999). than five decades, the fact that these extinctions Bottom trawling affects a greater area than any have not been documented is not evidence that they other benthic disturbance: Watling and Norse are not occurring. "One should not be surprised that (1998) estimated that an area equivalent to 14.8 x the marine equivalent of the passenger pigeon will 106km2 is trawled annually. Worldwide, an area soon be found as being one of the larger and/or equalling the world's continental shelf is trawled slow growing elasmobranch or bony deep-sea fish every two years. The North Sea floor on average species that are being exploited just in the recent is trawled twice a year (Lindeboom and De Groot past (Carlton et al. 1999)". 1998), but some areas (the best ones for fishing) are trawled much more frequently. Small spatial scale studies in the North Sea have shown that Trawling of the Sea Floor fishermen can very selectively look for target Ecological extinction caused by overfishing pre- species (Rijnsdorp et al. 1998). cedes all other pervasive human disturbance to For longer-lived species, repeated removal and coastal ecosystems.(Jackson et al. 2001). Over- physical disturbance on so large a scale can make fishing of large vertebrates and shellfish was the extinction all but inevitable. In Europe one of the first major human disturbance to all coastal eco- oldest documented local extinctions is that of the systems that were recently examined. The magni- flat oyster Ostrea edu/is in the Wadden Sea, more tude oflosses was enormous and large animalsare than a century ago, due to bottom trawling (Reise now absent from most coastal ecosystems in the 1982; Wolff2000b). The long-lived, large (1.5 m world. All other changes to coastal ecosystems long) bamdoor skate (Raja laevis), a Northwest At- came much later. Jackson et al. (2001) even con- lantic shelf -dwell ing fish that was once common clude that overfishing may be a necessaryprecon- in trawl bycatch, is now nearing extinction (Carlton ditionfor eutrophication,speciesintroductionsand et al. 1999). The same happened to all skate spe- What Structures Marine Biodiversity and why does it vary? 261 des in the southern North Sea (Wolff 2000a). with local stocks. Movement of feed and stocks Concern in Europeis rapidly growing on the wide- also increases the risk of spreading pathogens. spread destruction of banks of the deep-sea cold Global production offarmed fish and shellfish water coral Lophelia with its associated fauna, has more than doubled in the past 15 years. Many occurring in a narrow band along the continental people believe that such growth relieves pressure slope. As in tropical forests, the disappearance of on ocean fisheries, but the opposite is true for some the most observable species is likely a strong in- types of aqua culture. Farming carnivorous species dication of greater extinction. reguires large inputs of wild fish for feed. Some aquaculture systems also reduce wild fish supplies Mariculture through habitat modification and wild seedstock collection. Fry of wanted species are often obtained The impact of aquaculture on aquatic ecosystems from the wild at the expense of fry of non-wanted has been recently reviewed by Naylor et al. (2000). species (Naylor et al. 2000). More than 220 species of freshwater and marine fmfish and shellfish are farmed; the range includes marine species such as giant clams, mussels and Habitat modification salmon. These activities impact on marine biodi- versity in different ways. They share or compete The coastal environment in Europe has undergone for many coastal ecosystem services, including the profound modifications in many areas. Subtidal provision of habitat and nursery areas, feed and sediments, sandy beaches and dune systems have seed supplies, and assimilation of waste products. been transformed through the construction ofhar- Production practices and their impacts on marine bours, dykes and breakwaters; coastal inlets and ecosystems vary widely. Molluscs are generally rivers have been dammed with decreased export of farmed along coastlines where wild or hatchery- sediments to the coastal zone as a consequence; reared seed are grown on the seabed or in sus- sand and gravel are exploitated for the building in- pended nets, ropes or other structures. The animals dustry, sand is suppleted to beaches to prevent ero- rely entirely on ambient supplies of plankton and sion etc. The many forms of individual human use organic particles for food. Several systems - (tourism, collection, food gathering etc.) change the ponds, tanks or cages - are used in farming fmfish. physical environment as well, e.g. by turning stones Most marine and diadromous finfish are reared in on the beach, cutting algae that provide shelter etc. floating net cages nearshore, and all their nutrition In the tropics the situation .is perhaps even is supplied by formulated feeds. In such intense worse. Hundreds ofthousands of hectares of man- cultivitation the density ofindividuals is increased, groves and coastal wetlands have been transformed which requires greater use and management of into milkfish and shrimp ponds. This transforma- inputs, greater generation of waste products and tion results in loss of essential ecosystem services increased potential for the spread of pathogens. generated by mangroves, including the provision Shrimps dominate crustacean farming and are of nursery habitat, coastal protection, flood control, grown in coastal ponds which are often constructed sediment trapping and water treatment. Mangrove in former mangrove areas. forests serve as nurseries that provide food and Cultured species imported from elsewhere can shelter to many juvenile finfish and shellfish escape and establish in the wild. A spectacular caught as adults in coastal and offshore fisheries. example of this is the dramat~c increase of the Japa- In southeast Asia, mangrove-dependent species nese oyster Crassostrea gigas in the Ooster-schelde account for roughly one-third of yearly wild fish area in the Netherlands, where this species now landings excluding trash fish. A positive outcompetes the native cockles and oysters for relationship between finfish and shrimp landings space and food. Also well documented is the es- and mangrove area has been documented in cape fromnet pens of over255,000Atlanticsalmon Indonesia, Malaysia and the Philippines. Man- in the Pacific Ocean, where they now interbreed groves are also linked closely to habitat conditions

--- 262 Heip of coral reefs and seagrass beds (Naylor et al. Conclusion 2000). It is clear that marine biodiversityis alreadyheav- Loss of mangrove forests results in increased ily changed by human exploitation, especially of sediment transport onto downstream coral reefs. the large mammals, reptiles, fish, crustaceans and Fisheries capturetromreefscontributesabout 10% mollusks that have been greatlyreduced in coastal of human fish consumption globally and much waters worldwide. Besides other local problems more in developing countries. The loss in wild fisheries stocks due to habitat conversion with eutrophication, pollution, invaders and dis- ease, one may expect changes in the distribution associated with shrimpfanning is large.Naylor et and abundance of marine plants and animals due al. (2000) estimate that a total of 400g of fish and to effects of global climate change, including sea shrimp are losttrom capturefisheriesper kilogram level rise and changes in temperature,and perhaps of shrimp fanned in Thai shrimp ponds developed more subtle effects such as changing pH or Fe of in mangroves.If the fullrange of ecologicaleffects the ocean surface waters. All these changes take associatedwith mangroveconversionis accounted place against a background that is hardly for, including reduced mollusc productivity in understood. It is not known how many marine mangroves and losses to seagrass beds and coral species exist, where they exist and why. The reefs, the net yield trom these shrimpfanns is low. evolutionary history and the scope for adaptation of most species is unknown. There is hardly any Invading species infonnation on microbes and only scattered The risk of the establishment of exotic species in the infonnation on almost all ot~erspecies, including seas is not yet widely acknowledged outside the large vertebrate species. It is not known what biological circles, but there are now many spectacu- the extinction of known and unknown marine lar, documented examples. Species are transported species would mean for ecosystem functioning, in high numbers and high densities over vaste dis- includingthe deliveryofa largerangeof ecosystem tances, mainly through the ballast water of ships. goods andservicesthat areessentialto humanwell- The sheer number of invasions is staggering and has being. An important research effort aimed at been calculated at one species of macrofauna and underpinning sustainable use of marine resources flora per week in areas with heavy shipping traffic. is therefore a first requirement in the near future. There is nearly no infonnation on microbes. Most invasions probably even do not take off, but a large Acknowledgments number does. This can lead to qualitative changes This is paper nr. 2891 of the Centre for Estuarine in ecosystem functioning when empty niches are and Coastal Ecology, Netherlands Institute ofEcol- filled or the global erosion ofbiodiversity with the ogy. I thank the organizers of the Hanse Meeting loss of valuable genetic material. There are many fodnviting me and Angelika Brandt and Gerd Graf case studies that report on invading species. There for constructive comments on an earlier draft of the are now many spectacular examples of animal (e.g. manuscript. Marenzelleria viridis) and plant (e.g. Caulerpa taxifalia) outbreaks, but not many of these cases have been followed up sufficiently long to be able References to say something about the long tenn success and Abbott J (1980) Theories dealing with the ecology of consequences of these invasions. An excellent landbirds on islands. Adv Ecol Res 11:329-371 summary, focusing on North American coastal AzamF,SmithDC, StewardGF,HagstromA(1994)Bac- communities, is provided by Ruiz (2000). This is an teria- organic-mattercouplinganditssignificancefor active and important area of research with many oceanic carbon cycling.MicroEco128:167-179 practical consequences, e.g. in mariculture, for Carlton JT, Geller JQ, Reaka-Kudla ML, Norse EA which codes of practice have been established (1999) Historical extinctions in the sea. Ann Rev (ICES). Ecol Syst 30:515-538 What Structures Marine Biodiversity and why does it vary? 263

ChessonPL, WarnerRR (1981)Envirorunentalvariabil- Ices J Mar Sci 49:23-44 ity promotes coexistencein lotterycompetitivesys- Hutchinson GE (1959) Homage to Santa Rosalia or tems. Amer Nat 117:923-943 Why are thereso many kinds of animals?Amer Nat Clarke RD (1988) Chance and order in determining 93:145-159 fish-species composition on small coral patches. J Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Exp Mar BioI Ecol 115:197-212 Botsford LW,Bourque BJ, Bradbury RH, CookeR, ClementsFE (1935)Nature and structure ofthe clima.x. ErlandsonJ, EstesJA, HughesTP,Kidwell S, Lange J Ecol 24:252-289 CB, Lenihan HS, Pandolfi JM, Peterson CH, Connell JH (1975) Somemechanisms producing struc- Steneck RS, Tegner MJ, Warner RR (2001) ture in natural communities:A model and evidence Historical overfishing and the recent collaps of form field experiments.In: Cody ML and Diamond coastal ecosystems. Science 293:629-638 J (eds) Ecology and Evolution of Communities. Janzen DH (1970) Herbivores and the number of tree HarvardUniversityPress,Cambridge,Mass 460-490 species in tropical forests. Amer Nat 104:501-528 Connell JH (1979) Intermediate-Disturbance Hypoth- Lasserre P (1992) The role of biodiversity in marine esis. Science 204:1345 ecosystems. In: Solbrig, van Emden and van Oordt ConnorEF,McCoy(1979)The statisticsand biologyof (eds) Biodiversity and Global Chang. IUBS Press, the species-arearelationship.AmerNat 113:791-833 Paris, France pp 105-130 Duarte CM (2000) Marine biodiversity and ecosystem Latham RE, Ricklefs RE (1993) Global patterns of tree services: An elusive link. species richness in moist forests. Energy-diversity Flach E, MuthumbiA and Heip C (in press) Meiofauna theory doesnot account forvariation in species rich- And Macrofauna Community StructureIn Relation ness. Oikos 67 To Sediment Composition At The Iberian Margin LevinsR (1979)Coexistencein a variable envirorunent. Compared To The Goban Spur (Ne Atlantic). Prog AmerNat 114:765-783 Oceanogr Lindeboom HJ, De Groot SJ (1998) The effects of dif- GrassleJF,LasserreP,McIntyreAD andRay GC (1991) ferent types of fisheries on the North Sea and Irish Marine biodiversity and ecosystem function. Biol- Sea benthic ecosystem. NIOZ Report nr. 1. ISSN ogy International Special Issue 23; 19p 0923-3210.404 p Grassle JF,MaciolekNJ (1992) Deep-sea speciesrich- Loreau M (2000) Biodiversity and ecosystemfunction- ness - regional and local diversity estimates from ing: Recent theoretical advances. Oikos 91:3-17 quantitativebottomsamples.AmerNat 139:313-341 MacArthurRH (1972) GeographicalEcology: Patterns Hamilton TH, Rubinoffl, Barth RH, Bush GL (1963) in the distributionof species.Harper and Row,New Species abundance: Natural regulation of insular York variation. Science 142:1575-1577 MacArthur RH, Wilson EO (1963) An equilibrium Hanski I (1999) Habitat connectivity, habitat continu- theory of insular zoogeography ity, and metapopulations in dynamic landscapes. MacArthurRH, Wilson EO (1967)The theory of island Oikos 87:209-219 biogeography. Princeton Univ Press, Princeton NJ Hanski I,Ovaskainen0 (2000)The metapopulationca- MargalefR (1968) Perspectives in Ecological theory. pacity of a fragmented landscape. Nature 404:755- Chicago Univ Press 758 May RM (1975) Biological Populations Obeying Dif- Heip C (1996) Biodiversity of Marine Sediments. In: ference Equations - Stable Points, Stable Cycles, di CastriF andYounesT (eds)Biodiversity,Science And Chaos. J Theor BioI 51:511-524 and Development.Towards a New Partnership. pp May RM (1986) Biological Diversity -How Many Spe- 139-148 cies Are There. Nature 324:514-515 Heip C,'warwickRM, d'OzouvilleL (1999)AEuropean May RM (1992) Biodiversity -Bottoms Up for the SciencePlan on MarineBiodiversity.EuropeanSci- Oceans. Nature 357:278-279 ence Foundation, Stasbourg. Mc Gowan JA, Walker PW (1993) Pelagic Diversity Huisman J,WeissingFJ(2000) Biodiversityof plankton Patterns. In: Ricklefs RE and Schluter D (eds) by species oscillations and chaos. Nature 402:407- SpeciesDiversity in EcologicalCommunities.Univ 410 of Chicago Press, Chicago pp 203-214 Huys R, Herman PMJ, Heip CHR, Soetaert K (1992) Myers N, Mittermeier RA, Mittermeier Ca, deFonseca The meiobenthosofthe north sea: Density,biomass GAB, Kent J (2000) Biodiversity hotspots for con- trends and distribution of copepod communities. servation priorities. Nature 403:853-858 264 Heip

Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, esses, and biases.Ann Rev Ecol Syst 3I:481-531 Beveridge MCM, Clay J, Folke C, Lubchenco J, Sanders HL (1968) Benthic marine diversity: A com- Mooney H, TroeIl M (2000) Effect of aquaculture parative study.AmerNat 102:243-282 on world fish supplies.Nature 405:1017-1024 Schluter D, Ricklefs RE (1993) Species diversity: an Ormond RFG, Gage JD, Angel MV (1997) Marine introduction to the problem. In: Ricklefs and Biodiversity: Patterns and Processes. Cambridge Schluter(eds)SpeciesDiversityin EcologicalCom- University Press munities.Historicaland GeographicalPerspectives. Pachepsky E, CrawfordJW,Bown JL, SquireG (200 I) The Univ of ChicagoPress pp 1-10 Towards a general theory of biodiversity. Nature Simpson GG (1964) Speciesdensities of NorthAmeri- 410:923-926 can mammals. Syst ZooI 13:361-389 Paine RT(1966)Food web complexity and and species Soetaert K, Heip C (1995) Nematode assemblages of diversity.Amer Nat 100:65-75 deep-sea and shelfbreak sites in the North Atlantic Reise K (1982)Long-termchanges in themacrobenthic and MediterraneanSea.Mar EcolProg Ser 125:171- invertebrate fauna of the wadden sea - are poly- 183 chaetes aboutto take over?NethJ SeaRes 16:29-36 Terborgh J (1973) On the notion offavorableness in RexMA, StuartCL,HesslerRR.AlIenJA, SandersHL, plant ecology.Amer Nat 107:481-501 WilsonGDF(1993)Global-scalelatitudinalpatterns Thiery RG (1982) Environmental instability and com- of species diversityin the deep-sea benthos. Nature munity diversity.Bioi Rev 57:671-710 365:636-639 WatlingL, Norse EA(1998) Disturbance of the seabed RijnsdorpAD, BuysAM, Storbeck F,Visser EG (1998) by mobile fishing gear: A comparison to forest Micro-scale distribution of beam trawl effort in the clearcutting. ConservBioi 12:1180-1197 southern North Sea between 1993and 1996in rela- WattAS (1947) Pattern and process in the plant com- tion to the trawlingfrequency of the sea bed and the munity. J Ecol 35:1-22 impact on benthic organisms. ICES J Mar Sci WolffWJ (2000a)Causesof extirpationsinthe Wadden 55:403-419 Sea, an estuarine area in the Netherlands. Conserv Ritchie ME, OlffH (1999) Spatial scaling laws yield a Bioi 14:876-885 synthetictheoryofbiodiversity.Nature400:557-560 WolffWJ (2000b)Thesouth-easternNorth Sea:Losses Ruiz G.M,FofonoffPW, Carlton JT, WonhamMJ and of vertebrate fauna during the past 2000 years. Hines AH (2000) Invasion of coastal marine com- Conserv Bioi 95:209-217 munities inNorthAmerica:Apparentpatterns,proc-