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The basis for boundaries in pelagic biogeography
Prog. Oceanog. Vol. 34, pp. 121-133, 1994 Copyright © 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0079 - 6611/94 $26.00
Pergamon 0079-6611(94)00014-X
The basis for boundaries in pelagic biogeography S. VAN DER SPOEL
Institute of Taxonomic Zoology, PO Box 94766, 1090 GT Amsterdam, The Netherlands
CONTENTS 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
Introduction The ecosystem The community The biotope and habitat The niche The population The species and biodiversity The range and boundary The shoals and patchiness The geographic ranges in the ocean and the approach to their study Climateversus water-mass Conclusions Acknowledgements References
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"The limits of the habitat are decided arbitrarily by the student as the first step toward his study of the community. Of course 'habitat" has been used loosely and in diverse contexts (such is the fate of a l l ecological terms) "' A~rOP,EW~a~TO_Aand Bmc-a(1974)
1. INTRODUCTION Most ecological terms like 'niche', 'community', 'habitat', and 'ecological system' are frequently used, especially in oceanography, without maintaining the original meaning. Range, population and species are concepts fi'equentlyusedinconsequentlyin taxonomy studies. Taxonomy, biogeography and ecology are studies based on these concepts, which involve the species, their environments and their interrelations. Characters of the species, specimens and environment are studied to provide the data on which conclusions and predictions can then be based. In this short review, the following concepts will be discussed: ecosystem, community, biotope and habitat, niche, population, species and biodiversity, range and boundary, patchiness, shoals and patterns, geographic ranges in the ocean and the approach to their study, climate versus water-mass. 2. THE ECOSYSTEM In marine ecology there are periodic and predictable phenomena like production-maxima, production levels, particle size distribution and diurnal migration, so as in terrestrial ecology, one may expect there to be a system specifically related to these phenomena - the marine ecosystem. Since at different geographic localities the dominant processes vary, different ecosystems may 121
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to be present. Congruency in sometimes disjunct distributions of many species implies (proves) that homologous ecosystems are found in different oceans (BEKLEMISHEV,1981). An ecological system functions and maintains itselfby internal recycling in addition to the import and export of energy and material, which must remain in balance if the system is not to change. Hence in my opinion it is clear that when inputs (normal solar energy excluded) and losses dominate quantitatively over the recycling processes in the area, the identity of the ecosystem is lost. In this case the mechanism controlling the succession of phenomena in that area becomes dominated by external influences. Take any ecological process in the open ocean; at any given place and time it is evident that this process is more dependent on influences from outside the area than on local ones. Thus, locallyisolated ecosystems are not expected to occur in the pelagic ocean. Vertically, all systems are dependent on the autotrophic biota inhabiting the surface layers as solar energy is only supplied through the surface. The nutrients are either recycled, lost through sedimentation or supplied from the deep layers. Aeolian inputs are small but still significant in oligotrophic regions. Horizontally there is always transport of water, particles and biota (thus energy and material) with the currents and turbulent mixing. Thus, superimposed on incidental horizontal fluxes there is the obligate vertical flux. The permanently-stratified tropical waters are essentially different in their ecology from temperate waters where there is deep winter mixing. Similarly, the ecology of the mesopelagic realm is very different from that of the epipelagic. It seems necessary to subdivide the oceanic ecosystem, not into sharply separated systems with clearly defined boundaries, but into ecotones: horizontally into geographical ecotones and bathymetrically into vertical ecotones. It is clear that one ecotone may be more dependent on the surrounding system than another, and M(:GOWAN(1974) distinguished clearly identifiable, and hence isolated, ecosystems and ecotones in the Pacific Ocean. The first objection to be made about McGowan's subdivision is that they are limited to the epipelagic zone, so that their lower bathymetric limits are undefined. The second objection is that all these ecotones are strongly influenced by their adjacent systems by major exchanges of populations (thus energy and material). McGowan's ecotones are so strongly dependent on adjacent ecosystems for the composition of their biota and the exchange fluxes is so extensive that even this well-patterned ecosystem appears to be a network of interdependent geographical ecotones. The gyral current systems in the Pacific were described by VORONINA(1978) as ecosystems each composed of four dependent subecotones. In the centre of each gyral ecosystem Voronina distinguished a region unaffected by its surrounding systems. These more independent areas, however, are not congruent with the ecosystems describedby McGowan. The systems distinguished by both MCGOWAN (1974) and VORONINA (1978) are, like most ecosystems described for the pelagic realm, based on species distributions rather than ecological processes and so their boundaries are blurred by advective processes. For this reason, these divisions should not be taken as a starting point for biogeography. The following theoretical model may give better understanding of the reality. Ecotones are horizontally linked to each otherby lateral and vertical fluxes of material. As the production within each ecotone is largely exported to other systems, and so the sources of energy and material within each ecotone are largely external, one should always consider if a system is predominantly consuming or producing, and in which direction are the fluxes. One should also consider to what degree the water movements influence these fluxes. In general, the upper ecotones are 'producing' and the deeper ones are 'consuming'. Likewise, on average upwelling and divergence-systems are 'producing', i.e. exporting, while convergence-systems are 'consuming', i.e. are predominantly
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importing, but there are times (and seasons) when export-based systems are importing and vice versa.
The influence of currents on fluxes means that there is a gradual decline in flux strength from the major exporting ecotones; e.g. as found in the Gulf Stream, to the more or less independent ecotone found in the centre ofgyres and in semi-enclosed basins. The delimitation of such ecotones is arbitrary and prone to errors resulting from either inadequate sample coverage or the variability of the community structure, which was already clear from the maps ofecotones given by McGowan and Voronina. The smaller the system considered the less valuable it is for research, the larger it is, however, the more arbitrary its boundaries become. Systems which are well definedby local periodic and predictable processes include the Sargasso Sea area and the NW African upwelling area. The former is typifiedby small export fluxes, the latter by large export fluxes. But how should these systems be delimited?'Upwelling can be understood only in the frame of models covering a large space, perhaps all the ocean, where the upwelling centres appear as nodal points-of-stress' (MARGALEF,1978). The NW African and the Sargasso system can probably be best described as being bounded by nodal-points-of-stress (sensu Margalef). VINOGRADOV,GITELZONand SOROKIN(1973) studied the systems of tropical divergence and convergence and illustrated the vertical and lateral fluxes in the upper 100m by means of vertical distribution ofphytoplankton. This showed that the spatial structure of the system varies and that the type of flux is related to this spatial structure. Recent investigations in upwelling regions have shown that not only is the type of flux related to the spatial structure of the system, but also to the behaviour of the community (SCHALK, 1988). A community changes in composition as the upwelling conditions vary, and is dependent on the physiology and migratory behaviour of the organisms advected into the upwelling region. Another problem arises when we consider a latitudinal ecotone with similar characters and fluxes through out. In spring, and to a lesser extent in autumn, the production maximum represented by the phytoplankton bloom develops initially at low latitude and propagates polewards as a result of seasonal heating. However, superimposed on and sometimes obscuring the seasonal trends is a mesoscale pattern of cold-core and warm-core eddies (e.g. SAVIDGE, TIIRNER, BIIRKILL, WATSON,ANGEL,PINGREE,LEACHand R/CHARDS,1992). Consequently no single system has a uniformity of seasonal cycle or fluxes because of the con stant change in the physical environment. Seasonally the nodal-point-of-stress shifts polewards across the system. Thus any boundaries described for ecosystems are always arbitrary, and only ecotones (with arbitrary limits) and nodal-points-of-stress can be recognized. The centres ofecotones forming the opposite of nodal-point-of-stress can be distinguished as nodal-points-of-flux. 3. THE COMMUNITY The community or biocoenosis is the total assemblage of individuals ofdi fferent species living in a certain limited space variously defined as: a biotope (RINGELBERG,1976); a water-mass (PETtPA, 1979); a gyral system (McGOWAN, 1971 ); or an ecosystem (VrNOGRADOV et al, 1973; THIRIOT, 1987). The different interpretations of'space' make the community concept already very vague. Still, the term is frequently used in studies on pelagic organisms and among others McGOWAN (1971) advocated the interrelation of species as fundamental for the community concept. A community is then the total mixed population of species that are related ecologically to each other. This concept of community is comparable to that of an ecosystem but with the fundamental difference thatit isbiotic rather than abiotic factors which are the primary con sideration.
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Ifa community is nothing more than the specimens and species inhabiting an ecosystem, or in the pelagic realm of an ecotone, it seems logical to expect there to be dependent or relatedcommunities in the ocean. There will be strong interactions between members of relatedcommunities but still more so within a related-community. For pelagic communities there is little or no information on the actual interactions between specimens and species. The communities described are, until now, based on presence and absence of species in a certain area (MCGOWAN, 1971). Thus biogeographicai data and not ecological data have been used to distinguish communities, and for this reason operationally the community concept is not an ecological concept. The same objection can be made with regard to ecosystems, so that at the moment both (relatedcommunities and eco(tones) systems are only useful as refinements of the biogeography of the pelagic biota. The only promising, and really ecological, research on communities at the moment are the studies of food-chains, symbiotic relations and behaviour. Space limitation in the pelagic realm is a contradictio interminis, so that a related-community can never be based on the space in which it is located. When related-communities are considered as the biological basis for the ecosystem, one should realise that these are considered to comprise both nodal-points-of-stress, and ecotones of the oceans. BEKLEMISHEV(1961, 1971) described the ecotones as being found in secondary (mixing) water-masses with secondary (mixed primary) communities, and the ecosystems as found in primary (cyclical) water-masses with primary communities. A clear distinction between ecotones and ecosystems is notpossible. All areas of the ocean show characteristics of ecotones. For this reason, I consider most 'communities' or better relatedcommunities as secondary and thus dependent, with the restriction that related-communities in gyral systems are less dependent than others outside. The related communities in nodal-points-ofstress are the best described as primary related-communities. The nodal-point-of-stress applied to an upwelling system gives problems as it does not correspond to the primary community proposed by BEKLEMISHEV(1961, 1971). We know that in the upwelling area offNW Africa local races, forms and subspecies of several species are found (BADCOCK, 1981; HILGERSONand VAN DER SPOEL, 1987). These still apparently form a primary related community inhabiting the nodal-point-of-stress of the upwelling. Another, more promising, approach is to consider the communities ofecotones to be composed o ftwo parts: the biota linked with a stable-biotope component and the biota linked with a substratebi otope part of the ecotone. The biota linked with the stable-biotope component form a community of geographically stable nature, a primary related-community. The biota linked with the floating substrate-biotope form a community of 'pelagic nature' the secondary related community. The more a system has the nature of an ecotone, the more dominant will be the secondary relatedcommunity. How are we to discriminate between species comprising the secondary community and the primary community? We can use basic principles: the more planktonic (i.e. passively drifting) a species is, the more it belongs to the secondary community, the more nektonic, the more it belongs to the primary community. Diatoms, thus, are more likely to belong to the secondary community, whereas myctophid fish form part of the primary community. Species distributed over latitudinal climatic belts belong to the primary, whereas those species distributed according to the watermasses in general belong to the secondary communities. Summarising: in the ocean the associations of organisms are thus represented by related- or dependent communities, composed of primary and secondary elements.
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4. THE BIOTOPE AND HABITAT The area in which a community is living is usually named a biotope and that inhabitedby a single species (ofa community) is named a habitat. The biotope is thus, in principle, the total of abiotic components of an ecosystem, the community being the biotic part. It is an academic question to look for boundaries and limited areas for ecotones and related-communities. The biotope is, however, strongly linked with the concept of'area', with the conditions linked to a locality in the ocean. There are two types of abiotic component in each pelagic biotope. Firstly those that are geographically bound, including solar energy flux, day length, ice cover, bottom topography and current direction, and secondly those that are geographically independent and shift with the watermass and eddy-structure, including salinity, temperature, 0 2 content, associated organisms and nutrients. When discussing the habitat we encounter the same problem. There are geographically-fixed components, which are stable and predictable, forming the stable niche- orbiotope component, and geographically independent components which tend to be determined by the hydrodynamics of the system which are linked to the 'real substratum' forming the substrate habitat or biotope components. In a completely stable area the substrate-biotope part and stable-biotope component are identical. When, however, a current flows through the area it gives rise to instability such that the sustrate-biotope component advects through the stable-biotope component, sometimes with varying speed and direction which results in differential mixing of elements ofsubstrate-biotope component. The responses of organisms is largely determined by whether their species is linked either to the substrate-biotope part (members of the secondary community part) or to the stable-biotope component (members of the primary community part). Logically it can be assumed that those species distributed over latitudinal belts, i.e. with distributions determined by the latitudinally different factors of the climate, are linked to the stable-biotope component and those distributed according to specific water-masses or currents are more bound to the substrate-biotope component. In an ecotone the assemblage of species includes both those linked to the stable-biotope component and those linked with the substrate-biotope component. The latter are largely responsible tbr passive (in and out) fluxes, the former largely determine the inner cycles and active vertical fluxes between ecotones through their vertical migration. In a region which is a nodal-pointof-stress, the dominant species are bound to the stable-biotope component either actively (e.g. through vertical migration as in the NW African upwelling system) or passively if the area is stable (e.g. the Sargasso Sea). In systems that are usually considered ecotones in literature, the species linked to the substrate-biotope component are dominant. BEKLEMISrtEV( 1961 ) is of the opinion that all species which are characteristic ofecotones and so are assembled into secondary communities (i.e. are linked to the substrate-biotope component) are of tropical origin. Most tropical waters are strongly stratified with small orno vertical mixing. The more vertically mixed the water column is, the less stable is the substratum, and so the more likely the species become adapted to factors associated with the local stable-biotope component. Thus systems with communities originating largely from ecotones contain more species typical of stratified warmer waters, whereas systems with community input from nodal-point-of-stress contain more species typical o funstratified cool waters. This difference is generated by the species which are related to the substrate-biotope component being more tolerant of dispersion, and so are readily advected systems, than species bound to stable-biotope components. dPO 34:2/3-C
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The conclusion is that the biotope is composed of two components, viz: one which is stable and determined by the geographic locality, the other which is substrate dependent and so is determined by the dynamics of the water mass. 5. THE NICHE A species can tolerate specific ranges of environmental conditions but outside these ranges it cannot survive in the long term. For each condition, biotic or abiotic, a maximum and a minimum value exists between which a species survives, contained within each range but not necessarily coincident. In pelagic biota, the factors are partly linked with the substrate-biotope, and partly with the stable-biotope component. Dependent upon the nature of each species the prevailing factors which are predominant in limiting distributions may either be related to the sub strate-bio tope component or the stable-biotope component. In tropical, stratified waters, in species which undertake pronounced diurnal vertical migrations and in distributions tightly linked to the water-masses, predominantly factors related to the substrate-biotope component are found; whereas cold-water species inhabiting waters of mixed origin, species distributed in latitudinal belts and species with ontogenetic vertical migrations have distributions largely determined by factors related to the stable-biotope component. However, even in those species mainly determined by stable-biotope factors, the substratebiotope component will still have an impact especially if the advection of a water mass through the region results in the niche being decreased. The same holds good for species mainly determined by the substrate-biotope factors; since they, too, may find themselves approaching or exceeding one or more ranges of tolerance as they are carried through a region. The less tolerant a species is to variations in those factors related to the stable-biotope component, the more restricted it is to nodal-points-of-stress. Similarly, the less tolerant a species is to variations in those factors related to the substrate-biotope components, the more restricted it is to stratified waters. In a species showing vertical migration, there are in principle three sets of factors influencing the species' s distribution, viz: the stable-biotope component factors related to the ecotone in which the species lives, the substrate-biotope related factors of the water layer the species occupies during the shallow phase of its migration and the substrate-biotope related factors of the water layer it occupies during its deep phase. Thus en vironmental factors limiting the distributi on of specimens and species are related to both the stable-biotope and of the substrate-biotope throughout the total depth range the specimens live at all stages of their life cycle, the range that equals the tolerance limit of the species. 6. THE POPULATION Taxonomists and biogeographers tend to be vague about their concept of population. It is a concept which strictly speaking should be used only for groups belonging to one species (the mathematical use of population is not considered). Definitions of populations are seldom closelyreasoned. MAYR (1971) defines the population as: 'a population or local population is the community of potentially interbreeding individuals at a given locality'. A difference between 'population' and 'local population' is not made. The use of community in this context is confusing and even what is meant by locality is vague, especially in the ocean. A better definition seems: 'a population is the group of potentially interbreeding individuals in an area surrounded by a
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discontinuity in interbreeding andnot crossed by such discontinuities'. For the pelagic system we can 'translate' this into: A population is a group of individuals living in one water-mass of the dynamic circulation system which have the potential to interbreed. This statement is probably easily understood but is scientifically empty. The oceanic circulation system, though dynamic, occurs over a complex spectrum o fspatial variability such that the water mass distribution does not match any simple circulation pattern, nor is there a realistic potential to interbreed throughout the whole system determinedby a water mass, so 'populations' even when restricted to well-defined watermasses are not biological entities. The problem is that a water-mass is described on the basis of physico-chemical properties to make it an identifiable entity. The biologist needs a water-mass to be based on not only physicochemical properties but also its biological characteristics assuming that it can be described as a limited biologically homogeneous space. Although distinct boundaries in the ocean are scarce or absent there is no homogeneity. Conditions are always changing and rates at which the biological characteristics respond to these changes is highly variable, so watermass will probably always have to be defined according to its non-biological properties. Populations are also strongly dependent on water circulation and as there is no match between circulation patterns and water mass distributions a second problem arises. This can be tackled only by omitting either water-mass or circulation from the definition of population. The concept of water-mass is simplest to omit, the definition of population then becomes: 'A population is a group of potentially interbreeding specimens in a closed (oceanic) circulation system'. This statement is equally valid for awater body which is at rest. The full implication of the phrase 'a group of potentially interbreeding specimens' is that the population is the smallest category above the level of the individual specimen that has biological meaning, and into which a species can be split. However, within a species there will be intermittent interbreeding between populations (i.e. gene flow) otherwise in time genetic drift will result in their divergence. We can only recognise populations when some degree of divergence has occurred, usually in some characteristic of reproduction. Thus in these smaller groups the possibility of interbreeding is equally represented, interbreeding is of the same nature, or interbreeding is occurring in the same time period. The possibility for specimens meeting, mating andreproducing in the pelagic realm is dependent on the number of specimens per volume of water, the movement and structure (stratification) of the water, the mobility of the specimens, and themode offertilisation (internal or external). Mobility of specimens (mainly by vertical migration) frequently results in the active or passive formation of aggregations. Water movements which result in aggregations can be small (e.g. Langmuir cells) or larger (e.g. eddy structure), and once formed behavioural responses by the individual may maintain the aggregation long beyond the lifetime of the physical process which formed them. Consequently local swarms, shoals or patches may function as population in the pelagic (see also Section 9). However, patches and shoals or swarms are of short duration relative to the process of interbreeding and speciation. For example many fish species are known to congregate into shoals mainly at dusk and dawn, and tend to disperse at other times. Eddies with diameters of 200m persist for about a day and even mesoscale features like rings have durations of months, far too brief to allow the formation of populations. Consequently only within the large oceanic circulation systems like the West Wind Drift or the Sargasso Sea gyre which time characteristics of a decade or more, can identifiable population develop. However, at such large scales other mechanisms ofspeciation are theoretically possible (PALl/MBI, 1992). This supports also the definition given above.
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There are two consequences of the given population concept. Firstly most species with limited distribution in the ocean are composed of only one population. For example some circum-Antarctic species which are restricted to the West Wind Drift may be composed of a single population. In the absence of separate populations, there is a concomitant absence of geographical differentiation and so no geographical speciation. Secondly, species with wide distribution have populations which are limited by climatic belts of water-masses, and they show geographic variations across their range. 7. THE SPECIESAND BIODIVERSITY Before attempting to define what a species is, or what diversity is, one should consider their manifestations in the different realms of the world. The concepts of species and diversity are rather different for an ocean or a freshwater system because the geological history of the two types of system are of such different time-scales. The oceans are all interconnected but with the degree ofinterconnection varying, for example the Panama Isthmus was open about 5 million years ago and the ocean basins themselves are quite ancient - the Atlantic for example is some 200 million years old. The freshwater systems (and certainly also the brackish water systems) are all isolated from each other and only a few have a geological history of more than a few million years, and at high latitudes glacial periods cause major changes to the freshwater systems. The continental terrestrial environments have a long history with many vicariant events. The non-continental terrestrial biota are isolated and of very limited geological age. These differences result in different development of variation in the species; the rates of evolution and extinction in each realm are very different and so are their patterns of biodiversity. The oceanic realm probably shows the most biological influences, say: 'natural evolution', or the most species-dependent evolution; while terrestrial environments give the most environmentaldependent evolution. In the ocean the continuity of the environment provides very limited scope for isolation to assist in creating differences in, and between, species, so that many related species merge into each other gradually. In many cases the (morphological) differences between individual pelagic species are no greater than is seen between populations of a single terrestrial species. In taxonomy, 'taxonomic difference' describes the unique differences between taxa, and in this sense variation between populations is not representative of'taxonomic difference'. Hence 'clear taxonomic differences' are not found between many related species in the ocean. The words 'difference', 'taxonomic difference', (bio)diversity', 'variation' and the opposites 'monotypic', 'equality' need to be used carefully in the oceanic context, and can not be translated directly from terrestrial to oceanic conditions. Differences and variation cover the same phenomena, but diversity may result from variation as well as from taxonomic difference, while differences and monotypy are in some cases hard to separate. A more detailed approach and calculations of pelagic biodiversity are given by VAN DER S~'OEL(1994a). Thus, in the ocean, taxonomic differences between species tend to be small, within species variation or infraspecific variation and intraspecific differences are important but often merge almost seamlessly.
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8. THE RANGE AND BOUNDARY In the pelagic ocean the environment is continuous enough and dynamic enough for ranges to be determined by the species itself. Ranges are defined by: (a) environmental factors that are limiting and can only be met by the species with an absolute reaction of either being absent or present; (b) environmental factors with ranges that the species can tolerate for example by adaption; and (c) the genotypic variation which gives rise to characters which interact with the climate and with the water-mass factors. Biotic factors, i.e. mutual exclusivity between species, is not mentioned as in feeding and mobility pelagic species did not develop competitive adaptations. For (a) and (b) remember that the environment comprises the stable-biotope and substrate-biotope components. The transition s between (a) and (b) are gradual in that the extreme limits of tolerance may only be approached if at all, by a very few factors in any particular environment. In the latter situation we are dealing with the absolute reaction and in the former with the flexible reaction. There is a relation between (b) and (c) as a species' genotype cannot determine a range if the environment offers no possibility for a flexible response. Moreover, situations in which an absolute reaction has existed in the past may have changed, and a present day flexible reaction may have evolved in response to this past situation giving rise to races or subspecies within a species adapted to the extremes of the environment. In a previous attempt to describe ranges and evolution in plankton (VAN DER SPOEL, 1986) special attention was given to population dynamics. It was postulated that: 'In plankton it is not the influence of the environment but the characters of the organism that chiefly determine the ranges of the species. As population dynamics restrict the dispersal and distribution of species ... to an ... area smaller than the niche available... Evolution in the pelagic environment (in large populations) is too slow to reach optimal adaptation to the conditions of the large area available, resulting in a smaller range than possible ... Or environmental changes are still too quick which is the same as evolution is too slow.' To use 'population dynamics' in this postulate was probably an acceptable simplification. However, by replacing the concept o fpopulation dynamics by 'species specific genetic characters and adaptation developed in the species', the hypothesis better fits in the present theory. The statement 'evolution is too slow to reach optimal adaptation' seems incomplete. In reality, environmental changes in the ocean are, or were, too quick relative to the size of the habitats in the ocean. In this very large realm the changes prevent evolution from proceeding. Ranges thus are shaped by a multitude of influences in the present and past, among these are the genetic factors. All ranges have borders and though these are influenced by the same ecological factors so that with the obvious exception of the land/sea interface, the variations in responses to the various factors and the lack of sharp changes in the abiotic environment results in the borders for different species seldom coincide. The key to whether coincidence at present is important or not relies on the mechanism by which the borders are being maintained; this is an ecological question. For biogeography the question of coincidence of borders of different organisms in the open ocean is, though difficult, very relevant, since the geological history has influenced present day borders of ranges. A zone where borders of the distributions of many species are found close together, like near 42°N in the Atlantic is termed a boundary zone. It is evident that to the north and to the south of 42°N different faunas are found with cold- and warm-water representatives respectively, but exactly where is the transition between these fatmas? It is clear that all borders in a boundary zone show similar patterns, but no two are identical.
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9. THE SHOALSAND PATCHINESS Individuals of pelagic species are never distributed homogeneously over the total range of the species; there are areas of high abundance interspersed with areas of low abundance or even absence. The high abundance can be divided into two types: shoals and patches. Shoals are determined actively by the animals' behaviour and are usually structured groups of specimens with a certain orientation in space moving in the medium. Patches are more or less unstructured aggregations of specimens moving with the environment and sometimes are generated by passive response to the phytodynamics of the physical environment. Is the heterogeneous distribution within a species's range just a smaller scale repetition of the phenomena that determine the range of the species? Probably not, for shoals which are determined biotically since there are no factors limiting the size of a shoal other than the number of specimens involved and the range over which they can communicate. Involved are the specimens present in the total area covered by the vectors causing inhomogeneity and the strength of these vectors which are determining the mutual distances between the specimens. However, patches, as aggregations, are caused mainly by abiotic factors since ranges ofpelagic species are determined principally by the environment then probably patch-dynamics are indeed a scaled-down version of range-dynamics. In the patches and shoals we find the biotic and abiotic factors represented but separated, with patches being completely substratum dependent. For the low abundance areas between the aggregations one has to conclude that these are not unsuitable for the species but have only become depauperated by the aggregating forces. However, it must be recognised that mobility plays a key role. A convergence may result in the passive accumulation of planktonic taxa, but the presence of this aggregation may be an attractor for mobile micronekton that actively shoal in the zone where feeding may be better. Thus patches and shoals are formed by some of the factors also determining the range, namely part of the biotic and abiotic factors mainly related to the substrate-biotope. 10. THE GEOGRAPHICRANGESIN THE OCEAN ANDTHE APPROACHTO THEIRSTUDY The first studies on pelagic biogeography recognized only two faunas namely the cold-water and the warm-water fauna while some provincialism in these faunas resulting from isolation by continents was recognised. This simple picture ofbiogeography combined with the supposed very low diversity in the pelagic biota formed the basis for studies until the beginning of the century ( DAHL,1923). Modern approaches to pelagic biogeography were, however, al so born in these early days. HESSE(1924) for example described the maintenance of distribution patterns in relation to gyral (Zirkelstrom) and non gyral (Endstromen) current systems; this biogeographic theory was resurrected 47 years later, with the publication by McGOWAN( 1971 ). The formation of eddies and (cold or warm) core rings was also recognized, though not completelyunderstood by HESSE(1924) and it took another 50 years before studies on this phenomenon were opened again (RICHARDSON, 1976). The concepts formulated by HESSE (1924) and MCGOWAN( 1971) and others is that the environment is mainly determining the range of species. There is another school advocating that the animals themselves are more important in the process. EKMAN(1935) introduced the concept expatriation area and thus indicated the relativity of range borders. In 1953 EKMANdrew the conclusion of this in stating that 'the possibility of unobstructed transport may bring holoplanktonic animals everywhere'. The distribution of the holoplanktonic animals is, therefore, mainly dependent on their own physiological behaviour.
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Recently VAN DER SPOEL(1986) gave a slightly different interpretation of the 'physiological behaviour' in stating 'zooplankton comprises species whose individuals are passively drifted about by water movements within the stable range, defined by population dynamics, and occupied by the large, temporary or permanent populations'. It is self evident that both the organisms themselves as well as the environment influence dispersal. It needs, however, not to stay so vague. An organism, depending on its genetic and phenotypic characters, can live anywhere if it is able to surviveby interacting with the environment, either by flexibility in its responses, like adaptation in behaviour andphysiology, or to the influences which allow only an absolute reaction. Whether there is an absolute or flexible response will depend only on the environmental factors concerned. Studies of vertical distribution and migration illustrate this nicely. Many pelagic species show a vertical distribution induced by the environment; for some, temperature seems the most important factor that determines their depth, and so typically these species show subtropical submergence or comparable patterns. Other species respond to hydrostatic pressure or the light fieldin amore absolute manner showing a very fixed depth distribution independent of characteristics of the water such as currents and temperature, and so they occur within the same depth stratum everywhere. The vertical migration of many species also seems dependent on environmental factors often being triggered by variations in the light cycles. But upward migrations can be halted by high temperatures and the downward movement by low temperatures. If food is in short or abundant supply vertical ranges may be extended or even halted. In an upwelling or downwelling area both vertical migration and distribution are altered by changes in temperatures, food conditions and by active transport by the water circulation. In freshwaters, migration can be switched on in the presence of' chemicals secreted by predators. In some species, especially those with ontogenetic vertical migration, the displacement by upand downwelling is incorporated in the behaviour of the species such that they maintain their geophysical position within an upwelling system. The life history is 'adapted' in such a way that the (we)adult stage development coincides in depth and time with the upwelling so that eggs and juveniles are delivered into the surface waters in time to exploit the high productivity (SMITH, 1984). In this case it becomes very difficult to distinguish between the influence of the environment and that of the species itself. Another difficulty is that in some species vertical migration is more extensive at the periphery rather than at the centre of the range (ANGEL, 1979). So either near the periphery the species behaves differently, or some external factor near the periphery is inducing a different migration pattern, possibly the increasing abundance of a predator or a competitor. One can conclude that geographic ranges of individual taxa are determined by species-specific characteristics. I I. CLIMATEVERSUS WATERMASS The climate seems sometimes to have the greatest in fluence, in other cases the water-mass seems to have predominant infuence on the distribution patterns (VANDERSPOELand HEYMAN,1985). Most patterns are, however, influenced by both phenomena. The climate has its greatest influence on the pelagic realm where it determines the annual cycles of water temperature and daylight through insolation. The most typical feature of the water-mass is its chemical andnutrient contents. An animal digests food with enzymes and the enzyme reaction is temperature dependent. The food available is thus dependent not only on the food actually present, but also the ambient
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temperature. The quantity of food available is determined initially by solar energy and other local conditions such as nutrient concentrations, which are typically stable-biotope components, but its nutritional value is determined by a typically substrate-biotope factor of the in situ water temperature at which digestion takes place. Enzymatic reactions regulating an organism's metabolism (e.g. assimilation and digestion) are temperature dependent. This is of fundamental importance to the niche concept and the treatment of populations and biogeography. The deep-sea biotope is characterized by low temperatures and low food budgets. However, in some oceanic region s normally deep-living animals occur at shallow depth (VAN DERS POELand SCHALK,1988). Surprisingly in these regions (Mediterranean, Banda Sea) the deep temperatures are unusually warm. Since the quantity of food available is low and the animals' metabolic activities are higher as a result of the warm temperatures, the animals are confronted with starvation unless they can shift towards the surface in search of food. This vertical shift, and vertical migration in general, must be dependent on the temperature characteristics of the organisms' enzymes. With unfavourable conditions, the species may be able to change its niche. When food becomes limiting the metabolic activity of the animals may need to be lowered, but when the metabolic rate is increased by high temperature, more food has to be found. The former occurs in diurnal migrants which when they migrate deeper encounter lower temperatures and so their metabolism slows automatically conserving energy. The latter phenomenon occurs in deep-sea animals forced up towards the surface by high temperatures at depth (VAN DER SPOEL, 1994b). When studying evolution in diurnal migrants, it should be borne in mind that their ancestral environment is in the epipelagic. Thus these speciesmay co-occur at night but occupy bathymetrically distinct ranges during day-time. So closely related species may be isolated (sympatric) at night in meso- or bathypelagic strata but co-occur (allopatric) in the day-time. It is clear that organisms in their dispersal are influenced by four types of factors: ( 1) absolute factors, (2) variable factors, (3) factors linked with climate, and (4) factors linked with water mass. 12. CONCLUSION A general conclusion is that in the pelagic realm there are no boundaries or barriers to distribution, and that all environmental changes are gradients between nodal-points-of-stress in a three-dimensional space characterised by factors which are either fixed in space, the locally stable ones, or those moved with the water-masses. Life in general and life of each individual in the pelagic realm is determined by four categories of factors; those related to the gradients, those related to nodal-points-of-stress, those related to stable local conditions, and those related to the moving substrate. To some of these factors a given taxon may react in an absolute fashion and to others flexibly. As in the terrestrial realm pelagic populations, ranges and food chains show stability. This stability is derived from interactions between either gradients and substratum or of nodal-pointsof-stress and stable local conditions. In both the former and the latter case it is the behaviour of the organism that determines the eventual effects of the factors responsible for the stability. Thus behaviour developed during evolution determines population ranges, structures, and migrations. 13. ACKNOWLEDGEMENTS Dr M.V. Angelis kindlyacknowledgedfor the additions,correctionsand polishing ofthis paper.This paper was originally presented at the SCOR WG 93 meeting in Amsterdam in 1993.
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14. REFERENCES ANDREWARTHA,H.G. and L.C. BIRCH (1974) The distribution and abundance of animals. University of Chicago Press, Chicago. 782 pp. AN~;EL,M. (1979) Studies on Atlantic halocyprid ostracods: their vertical distribution and community structure in the central gyre region along latitude 30°N from offAfricato Bermuda. Progress in Oceanography, 8, 3124.
BAD('OCK,J. ( 1981 ) The significance of meristic variation in Benthosema glaciale (Pisces, myctophoidei) and the species distribution offnorth west Africa. Deep-Sea Research, 28(12), 1477-1491. BEKLEMISHFN,C.W. ( 1961 ) On the spatial structure of plankton communities in dependence of oceanic circulation. Boundaries of ranges of oceanic plankton animals in the north Pacific. Okeanologia, 5, 1059-1072. BEKLEMISHEV,C.W. ( 1971) Distribution of plankton as related to micropaleontology. In: The micropaleontology of oceans, B.M. FUNNELand W.R. R/EDEL,editors, Cambridge University Press, 75-87. BEKLEMISHEV.C.W. ( 1981 ) Biological structure of the Pacific Ocean as compared with two other oceans. Journal of Plankton Research, 3(4), 53 i-549. DAHL, F. (1923) Okologische Tiergeographie. Fisher Verlag, Jena, 122pp. EKMAN, S. (1935) Tiergeographie des Meeres. Leipzig Akademie Verlagsgesellschaft, 542pp. EKMAN, S. (1953) Zoogeography of the sea. Sidgwick and Jackson Ltd., London, 417pp. HESSE, R. (1924) Tiergeographie. Fisher Verlag Jena 613pp. HII,(;ERSON, P.C.J. and S. VAN DER SPOEL (1987) East-west variation in Diacria off northwestern Africa. Malacological Review, 20, 97-104. MARtIAI,EFF,R. (1978) What is an upwelling ecosystem? In: Upwelling eco.systems, R. BOJE and C. TOMCZAK, editors, Springer Verlag, Berlin, 12-23. MAYR,E. ( 1971 ) Populations, ,s79eciesand evolution. Belknap Press, Harvard University,Cambridge, Massachusetts, 453pp. McG~)WAN,J.A. ( 1971 ) Oceanic biogeography of the Pacific. In: The micropalaeontology of oceans. B.M. Fl ~YYEL and W.R. RIEDEL,editors, Cambridge University Press, 3-74. McGOWAN, J.A. (1974) The nature of oceanic ecosystems. In: The Biology of the Oceanic Pacific', Oregon State University Press, 9-28. PALl~MBI,S.R. (1992) Marine speciation on a small planet. Trends in Ecology and Evolution, 7, 114- I 18. PETIPA, T.S. (1979) Trophic relationships in communities and the functioning of marine ecosystems. In: Marine production mechanisms. M.J. DUNBAR,editor, Cambridge University Press, 233-250. RICHA~)SON, P. (1976) Gulfstream rings. Oceanus, 19(3), 65-68. RINGELBERG,J. (1976) Aquatische Ecologic, Bohn, Scheltema and Holkema, Utrecht, 240pp. SCHALK,P.H. (1988) Monsoon influences on biogeography and ecology of zooplankton and micronekton of the lndo-Malayan region. Phi) Thesis, University of Amsterdam, 144pp. TmmoT, A. ( 1987) Zooplankton communities in the West African upweiling area. In: Upwelling systems, R. BOJE and C. TOMCZAK,editors, Springer Verlag, Berlin, 32-61. SAVID¢;E, G., D.R. TURNER, P.H. BURKJLL, A.J. WATSON, M.V. ANGEL, R.D. PINGREE,H. LEACH and K.J. RICHA~)S, (1992) The BOFS 1990 Spring Bloom Experiment: Temporal evolution and spatial variability of the hydrographic field. Progress in Oceanography, 29, 235-281. SMITH, S. (1984) Biological indications of active upwelling in the northwestern Indian Ocean in 1964 and 1979, and a comparison with Peru and northwest Africa. Deep-Sea Research, 31, 951-967. VAN DER SPOEL, S. (1986) What is unique about open-ocean biogeography, zooplankton? UNES('O Technical Papers, Marine Biology, 49,254-260. VANDERS POEt,,S. (1994a) The biosystematic basis for pelagic biodiversity. Bijdragen tot de Dierlcunde (in press). VAN DER SPOEL, S. (1994b) A warning from the deep. Progress in Oceanography, 34,207-210. VANDERSPOEt, S. and R.P. HEYMAN(1985) A comparative atlas of zooplankton, biological patterns in the oceans. Bunge Utrecht, 186pp. VINOGRADOV,M.E., I.I. GITELZONand Y.I. SOROKIN(1973) The spatial structure of communities in the euphotic zone of the ocean tropics. In: Life activity ofpelagic communities in the ocean tropics, M.E. VINOGRADOV, editor.. Israel Program for Scentific Translations, Jerusalem, 187-298. VORONINA,N.M. (1978) Variability of ecosystems. In: Advances in Oceanography, H. CHARNOCKand S. DEACON, editor,;, Plenum Press, New York, 221-243.
JPO 34:2/3-D
Pergamon 0079-6611(94)00014-X
The basis for boundaries in pelagic biogeography S. VAN DER SPOEL
Institute of Taxonomic Zoology, PO Box 94766, 1090 GT Amsterdam, The Netherlands
CONTENTS 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
Introduction The ecosystem The community The biotope and habitat The niche The population The species and biodiversity The range and boundary The shoals and patchiness The geographic ranges in the ocean and the approach to their study Climateversus water-mass Conclusions Acknowledgements References
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"The limits of the habitat are decided arbitrarily by the student as the first step toward his study of the community. Of course 'habitat" has been used loosely and in diverse contexts (such is the fate of a l l ecological terms) "' A~rOP,EW~a~TO_Aand Bmc-a(1974)
1. INTRODUCTION Most ecological terms like 'niche', 'community', 'habitat', and 'ecological system' are frequently used, especially in oceanography, without maintaining the original meaning. Range, population and species are concepts fi'equentlyusedinconsequentlyin taxonomy studies. Taxonomy, biogeography and ecology are studies based on these concepts, which involve the species, their environments and their interrelations. Characters of the species, specimens and environment are studied to provide the data on which conclusions and predictions can then be based. In this short review, the following concepts will be discussed: ecosystem, community, biotope and habitat, niche, population, species and biodiversity, range and boundary, patchiness, shoals and patterns, geographic ranges in the ocean and the approach to their study, climate versus water-mass. 2. THE ECOSYSTEM In marine ecology there are periodic and predictable phenomena like production-maxima, production levels, particle size distribution and diurnal migration, so as in terrestrial ecology, one may expect there to be a system specifically related to these phenomena - the marine ecosystem. Since at different geographic localities the dominant processes vary, different ecosystems may 121
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to be present. Congruency in sometimes disjunct distributions of many species implies (proves) that homologous ecosystems are found in different oceans (BEKLEMISHEV,1981). An ecological system functions and maintains itselfby internal recycling in addition to the import and export of energy and material, which must remain in balance if the system is not to change. Hence in my opinion it is clear that when inputs (normal solar energy excluded) and losses dominate quantitatively over the recycling processes in the area, the identity of the ecosystem is lost. In this case the mechanism controlling the succession of phenomena in that area becomes dominated by external influences. Take any ecological process in the open ocean; at any given place and time it is evident that this process is more dependent on influences from outside the area than on local ones. Thus, locallyisolated ecosystems are not expected to occur in the pelagic ocean. Vertically, all systems are dependent on the autotrophic biota inhabiting the surface layers as solar energy is only supplied through the surface. The nutrients are either recycled, lost through sedimentation or supplied from the deep layers. Aeolian inputs are small but still significant in oligotrophic regions. Horizontally there is always transport of water, particles and biota (thus energy and material) with the currents and turbulent mixing. Thus, superimposed on incidental horizontal fluxes there is the obligate vertical flux. The permanently-stratified tropical waters are essentially different in their ecology from temperate waters where there is deep winter mixing. Similarly, the ecology of the mesopelagic realm is very different from that of the epipelagic. It seems necessary to subdivide the oceanic ecosystem, not into sharply separated systems with clearly defined boundaries, but into ecotones: horizontally into geographical ecotones and bathymetrically into vertical ecotones. It is clear that one ecotone may be more dependent on the surrounding system than another, and M(:GOWAN(1974) distinguished clearly identifiable, and hence isolated, ecosystems and ecotones in the Pacific Ocean. The first objection to be made about McGowan's subdivision is that they are limited to the epipelagic zone, so that their lower bathymetric limits are undefined. The second objection is that all these ecotones are strongly influenced by their adjacent systems by major exchanges of populations (thus energy and material). McGowan's ecotones are so strongly dependent on adjacent ecosystems for the composition of their biota and the exchange fluxes is so extensive that even this well-patterned ecosystem appears to be a network of interdependent geographical ecotones. The gyral current systems in the Pacific were described by VORONINA(1978) as ecosystems each composed of four dependent subecotones. In the centre of each gyral ecosystem Voronina distinguished a region unaffected by its surrounding systems. These more independent areas, however, are not congruent with the ecosystems describedby McGowan. The systems distinguished by both MCGOWAN (1974) and VORONINA (1978) are, like most ecosystems described for the pelagic realm, based on species distributions rather than ecological processes and so their boundaries are blurred by advective processes. For this reason, these divisions should not be taken as a starting point for biogeography. The following theoretical model may give better understanding of the reality. Ecotones are horizontally linked to each otherby lateral and vertical fluxes of material. As the production within each ecotone is largely exported to other systems, and so the sources of energy and material within each ecotone are largely external, one should always consider if a system is predominantly consuming or producing, and in which direction are the fluxes. One should also consider to what degree the water movements influence these fluxes. In general, the upper ecotones are 'producing' and the deeper ones are 'consuming'. Likewise, on average upwelling and divergence-systems are 'producing', i.e. exporting, while convergence-systems are 'consuming', i.e. are predominantly
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importing, but there are times (and seasons) when export-based systems are importing and vice versa.
The influence of currents on fluxes means that there is a gradual decline in flux strength from the major exporting ecotones; e.g. as found in the Gulf Stream, to the more or less independent ecotone found in the centre ofgyres and in semi-enclosed basins. The delimitation of such ecotones is arbitrary and prone to errors resulting from either inadequate sample coverage or the variability of the community structure, which was already clear from the maps ofecotones given by McGowan and Voronina. The smaller the system considered the less valuable it is for research, the larger it is, however, the more arbitrary its boundaries become. Systems which are well definedby local periodic and predictable processes include the Sargasso Sea area and the NW African upwelling area. The former is typifiedby small export fluxes, the latter by large export fluxes. But how should these systems be delimited?'Upwelling can be understood only in the frame of models covering a large space, perhaps all the ocean, where the upwelling centres appear as nodal points-of-stress' (MARGALEF,1978). The NW African and the Sargasso system can probably be best described as being bounded by nodal-points-of-stress (sensu Margalef). VINOGRADOV,GITELZONand SOROKIN(1973) studied the systems of tropical divergence and convergence and illustrated the vertical and lateral fluxes in the upper 100m by means of vertical distribution ofphytoplankton. This showed that the spatial structure of the system varies and that the type of flux is related to this spatial structure. Recent investigations in upwelling regions have shown that not only is the type of flux related to the spatial structure of the system, but also to the behaviour of the community (SCHALK, 1988). A community changes in composition as the upwelling conditions vary, and is dependent on the physiology and migratory behaviour of the organisms advected into the upwelling region. Another problem arises when we consider a latitudinal ecotone with similar characters and fluxes through out. In spring, and to a lesser extent in autumn, the production maximum represented by the phytoplankton bloom develops initially at low latitude and propagates polewards as a result of seasonal heating. However, superimposed on and sometimes obscuring the seasonal trends is a mesoscale pattern of cold-core and warm-core eddies (e.g. SAVIDGE, TIIRNER, BIIRKILL, WATSON,ANGEL,PINGREE,LEACHand R/CHARDS,1992). Consequently no single system has a uniformity of seasonal cycle or fluxes because of the con stant change in the physical environment. Seasonally the nodal-point-of-stress shifts polewards across the system. Thus any boundaries described for ecosystems are always arbitrary, and only ecotones (with arbitrary limits) and nodal-points-of-stress can be recognized. The centres ofecotones forming the opposite of nodal-point-of-stress can be distinguished as nodal-points-of-flux. 3. THE COMMUNITY The community or biocoenosis is the total assemblage of individuals ofdi fferent species living in a certain limited space variously defined as: a biotope (RINGELBERG,1976); a water-mass (PETtPA, 1979); a gyral system (McGOWAN, 1971 ); or an ecosystem (VrNOGRADOV et al, 1973; THIRIOT, 1987). The different interpretations of'space' make the community concept already very vague. Still, the term is frequently used in studies on pelagic organisms and among others McGOWAN (1971) advocated the interrelation of species as fundamental for the community concept. A community is then the total mixed population of species that are related ecologically to each other. This concept of community is comparable to that of an ecosystem but with the fundamental difference thatit isbiotic rather than abiotic factors which are the primary con sideration.
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Ifa community is nothing more than the specimens and species inhabiting an ecosystem, or in the pelagic realm of an ecotone, it seems logical to expect there to be dependent or relatedcommunities in the ocean. There will be strong interactions between members of relatedcommunities but still more so within a related-community. For pelagic communities there is little or no information on the actual interactions between specimens and species. The communities described are, until now, based on presence and absence of species in a certain area (MCGOWAN, 1971). Thus biogeographicai data and not ecological data have been used to distinguish communities, and for this reason operationally the community concept is not an ecological concept. The same objection can be made with regard to ecosystems, so that at the moment both (relatedcommunities and eco(tones) systems are only useful as refinements of the biogeography of the pelagic biota. The only promising, and really ecological, research on communities at the moment are the studies of food-chains, symbiotic relations and behaviour. Space limitation in the pelagic realm is a contradictio interminis, so that a related-community can never be based on the space in which it is located. When related-communities are considered as the biological basis for the ecosystem, one should realise that these are considered to comprise both nodal-points-of-stress, and ecotones of the oceans. BEKLEMISHEV(1961, 1971) described the ecotones as being found in secondary (mixing) water-masses with secondary (mixed primary) communities, and the ecosystems as found in primary (cyclical) water-masses with primary communities. A clear distinction between ecotones and ecosystems is notpossible. All areas of the ocean show characteristics of ecotones. For this reason, I consider most 'communities' or better relatedcommunities as secondary and thus dependent, with the restriction that related-communities in gyral systems are less dependent than others outside. The related communities in nodal-points-ofstress are the best described as primary related-communities. The nodal-point-of-stress applied to an upwelling system gives problems as it does not correspond to the primary community proposed by BEKLEMISHEV(1961, 1971). We know that in the upwelling area offNW Africa local races, forms and subspecies of several species are found (BADCOCK, 1981; HILGERSONand VAN DER SPOEL, 1987). These still apparently form a primary related community inhabiting the nodal-point-of-stress of the upwelling. Another, more promising, approach is to consider the communities ofecotones to be composed o ftwo parts: the biota linked with a stable-biotope component and the biota linked with a substratebi otope part of the ecotone. The biota linked with the stable-biotope component form a community of geographically stable nature, a primary related-community. The biota linked with the floating substrate-biotope form a community of 'pelagic nature' the secondary related community. The more a system has the nature of an ecotone, the more dominant will be the secondary relatedcommunity. How are we to discriminate between species comprising the secondary community and the primary community? We can use basic principles: the more planktonic (i.e. passively drifting) a species is, the more it belongs to the secondary community, the more nektonic, the more it belongs to the primary community. Diatoms, thus, are more likely to belong to the secondary community, whereas myctophid fish form part of the primary community. Species distributed over latitudinal climatic belts belong to the primary, whereas those species distributed according to the watermasses in general belong to the secondary communities. Summarising: in the ocean the associations of organisms are thus represented by related- or dependent communities, composed of primary and secondary elements.
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4. THE BIOTOPE AND HABITAT The area in which a community is living is usually named a biotope and that inhabitedby a single species (ofa community) is named a habitat. The biotope is thus, in principle, the total of abiotic components of an ecosystem, the community being the biotic part. It is an academic question to look for boundaries and limited areas for ecotones and related-communities. The biotope is, however, strongly linked with the concept of'area', with the conditions linked to a locality in the ocean. There are two types of abiotic component in each pelagic biotope. Firstly those that are geographically bound, including solar energy flux, day length, ice cover, bottom topography and current direction, and secondly those that are geographically independent and shift with the watermass and eddy-structure, including salinity, temperature, 0 2 content, associated organisms and nutrients. When discussing the habitat we encounter the same problem. There are geographically-fixed components, which are stable and predictable, forming the stable niche- orbiotope component, and geographically independent components which tend to be determined by the hydrodynamics of the system which are linked to the 'real substratum' forming the substrate habitat or biotope components. In a completely stable area the substrate-biotope part and stable-biotope component are identical. When, however, a current flows through the area it gives rise to instability such that the sustrate-biotope component advects through the stable-biotope component, sometimes with varying speed and direction which results in differential mixing of elements ofsubstrate-biotope component. The responses of organisms is largely determined by whether their species is linked either to the substrate-biotope part (members of the secondary community part) or to the stable-biotope component (members of the primary community part). Logically it can be assumed that those species distributed over latitudinal belts, i.e. with distributions determined by the latitudinally different factors of the climate, are linked to the stable-biotope component and those distributed according to specific water-masses or currents are more bound to the substrate-biotope component. In an ecotone the assemblage of species includes both those linked to the stable-biotope component and those linked with the substrate-biotope component. The latter are largely responsible tbr passive (in and out) fluxes, the former largely determine the inner cycles and active vertical fluxes between ecotones through their vertical migration. In a region which is a nodal-pointof-stress, the dominant species are bound to the stable-biotope component either actively (e.g. through vertical migration as in the NW African upwelling system) or passively if the area is stable (e.g. the Sargasso Sea). In systems that are usually considered ecotones in literature, the species linked to the substrate-biotope component are dominant. BEKLEMISrtEV( 1961 ) is of the opinion that all species which are characteristic ofecotones and so are assembled into secondary communities (i.e. are linked to the substrate-biotope component) are of tropical origin. Most tropical waters are strongly stratified with small orno vertical mixing. The more vertically mixed the water column is, the less stable is the substratum, and so the more likely the species become adapted to factors associated with the local stable-biotope component. Thus systems with communities originating largely from ecotones contain more species typical of stratified warmer waters, whereas systems with community input from nodal-point-of-stress contain more species typical o funstratified cool waters. This difference is generated by the species which are related to the substrate-biotope component being more tolerant of dispersion, and so are readily advected systems, than species bound to stable-biotope components. dPO 34:2/3-C
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The conclusion is that the biotope is composed of two components, viz: one which is stable and determined by the geographic locality, the other which is substrate dependent and so is determined by the dynamics of the water mass. 5. THE NICHE A species can tolerate specific ranges of environmental conditions but outside these ranges it cannot survive in the long term. For each condition, biotic or abiotic, a maximum and a minimum value exists between which a species survives, contained within each range but not necessarily coincident. In pelagic biota, the factors are partly linked with the substrate-biotope, and partly with the stable-biotope component. Dependent upon the nature of each species the prevailing factors which are predominant in limiting distributions may either be related to the sub strate-bio tope component or the stable-biotope component. In tropical, stratified waters, in species which undertake pronounced diurnal vertical migrations and in distributions tightly linked to the water-masses, predominantly factors related to the substrate-biotope component are found; whereas cold-water species inhabiting waters of mixed origin, species distributed in latitudinal belts and species with ontogenetic vertical migrations have distributions largely determined by factors related to the stable-biotope component. However, even in those species mainly determined by stable-biotope factors, the substratebiotope component will still have an impact especially if the advection of a water mass through the region results in the niche being decreased. The same holds good for species mainly determined by the substrate-biotope factors; since they, too, may find themselves approaching or exceeding one or more ranges of tolerance as they are carried through a region. The less tolerant a species is to variations in those factors related to the stable-biotope component, the more restricted it is to nodal-points-of-stress. Similarly, the less tolerant a species is to variations in those factors related to the substrate-biotope components, the more restricted it is to stratified waters. In a species showing vertical migration, there are in principle three sets of factors influencing the species' s distribution, viz: the stable-biotope component factors related to the ecotone in which the species lives, the substrate-biotope related factors of the water layer the species occupies during the shallow phase of its migration and the substrate-biotope related factors of the water layer it occupies during its deep phase. Thus en vironmental factors limiting the distributi on of specimens and species are related to both the stable-biotope and of the substrate-biotope throughout the total depth range the specimens live at all stages of their life cycle, the range that equals the tolerance limit of the species. 6. THE POPULATION Taxonomists and biogeographers tend to be vague about their concept of population. It is a concept which strictly speaking should be used only for groups belonging to one species (the mathematical use of population is not considered). Definitions of populations are seldom closelyreasoned. MAYR (1971) defines the population as: 'a population or local population is the community of potentially interbreeding individuals at a given locality'. A difference between 'population' and 'local population' is not made. The use of community in this context is confusing and even what is meant by locality is vague, especially in the ocean. A better definition seems: 'a population is the group of potentially interbreeding individuals in an area surrounded by a
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discontinuity in interbreeding andnot crossed by such discontinuities'. For the pelagic system we can 'translate' this into: A population is a group of individuals living in one water-mass of the dynamic circulation system which have the potential to interbreed. This statement is probably easily understood but is scientifically empty. The oceanic circulation system, though dynamic, occurs over a complex spectrum o fspatial variability such that the water mass distribution does not match any simple circulation pattern, nor is there a realistic potential to interbreed throughout the whole system determinedby a water mass, so 'populations' even when restricted to well-defined watermasses are not biological entities. The problem is that a water-mass is described on the basis of physico-chemical properties to make it an identifiable entity. The biologist needs a water-mass to be based on not only physicochemical properties but also its biological characteristics assuming that it can be described as a limited biologically homogeneous space. Although distinct boundaries in the ocean are scarce or absent there is no homogeneity. Conditions are always changing and rates at which the biological characteristics respond to these changes is highly variable, so watermass will probably always have to be defined according to its non-biological properties. Populations are also strongly dependent on water circulation and as there is no match between circulation patterns and water mass distributions a second problem arises. This can be tackled only by omitting either water-mass or circulation from the definition of population. The concept of water-mass is simplest to omit, the definition of population then becomes: 'A population is a group of potentially interbreeding specimens in a closed (oceanic) circulation system'. This statement is equally valid for awater body which is at rest. The full implication of the phrase 'a group of potentially interbreeding specimens' is that the population is the smallest category above the level of the individual specimen that has biological meaning, and into which a species can be split. However, within a species there will be intermittent interbreeding between populations (i.e. gene flow) otherwise in time genetic drift will result in their divergence. We can only recognise populations when some degree of divergence has occurred, usually in some characteristic of reproduction. Thus in these smaller groups the possibility of interbreeding is equally represented, interbreeding is of the same nature, or interbreeding is occurring in the same time period. The possibility for specimens meeting, mating andreproducing in the pelagic realm is dependent on the number of specimens per volume of water, the movement and structure (stratification) of the water, the mobility of the specimens, and themode offertilisation (internal or external). Mobility of specimens (mainly by vertical migration) frequently results in the active or passive formation of aggregations. Water movements which result in aggregations can be small (e.g. Langmuir cells) or larger (e.g. eddy structure), and once formed behavioural responses by the individual may maintain the aggregation long beyond the lifetime of the physical process which formed them. Consequently local swarms, shoals or patches may function as population in the pelagic (see also Section 9). However, patches and shoals or swarms are of short duration relative to the process of interbreeding and speciation. For example many fish species are known to congregate into shoals mainly at dusk and dawn, and tend to disperse at other times. Eddies with diameters of 200m persist for about a day and even mesoscale features like rings have durations of months, far too brief to allow the formation of populations. Consequently only within the large oceanic circulation systems like the West Wind Drift or the Sargasso Sea gyre which time characteristics of a decade or more, can identifiable population develop. However, at such large scales other mechanisms ofspeciation are theoretically possible (PALl/MBI, 1992). This supports also the definition given above.
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There are two consequences of the given population concept. Firstly most species with limited distribution in the ocean are composed of only one population. For example some circum-Antarctic species which are restricted to the West Wind Drift may be composed of a single population. In the absence of separate populations, there is a concomitant absence of geographical differentiation and so no geographical speciation. Secondly, species with wide distribution have populations which are limited by climatic belts of water-masses, and they show geographic variations across their range. 7. THE SPECIESAND BIODIVERSITY Before attempting to define what a species is, or what diversity is, one should consider their manifestations in the different realms of the world. The concepts of species and diversity are rather different for an ocean or a freshwater system because the geological history of the two types of system are of such different time-scales. The oceans are all interconnected but with the degree ofinterconnection varying, for example the Panama Isthmus was open about 5 million years ago and the ocean basins themselves are quite ancient - the Atlantic for example is some 200 million years old. The freshwater systems (and certainly also the brackish water systems) are all isolated from each other and only a few have a geological history of more than a few million years, and at high latitudes glacial periods cause major changes to the freshwater systems. The continental terrestrial environments have a long history with many vicariant events. The non-continental terrestrial biota are isolated and of very limited geological age. These differences result in different development of variation in the species; the rates of evolution and extinction in each realm are very different and so are their patterns of biodiversity. The oceanic realm probably shows the most biological influences, say: 'natural evolution', or the most species-dependent evolution; while terrestrial environments give the most environmentaldependent evolution. In the ocean the continuity of the environment provides very limited scope for isolation to assist in creating differences in, and between, species, so that many related species merge into each other gradually. In many cases the (morphological) differences between individual pelagic species are no greater than is seen between populations of a single terrestrial species. In taxonomy, 'taxonomic difference' describes the unique differences between taxa, and in this sense variation between populations is not representative of'taxonomic difference'. Hence 'clear taxonomic differences' are not found between many related species in the ocean. The words 'difference', 'taxonomic difference', (bio)diversity', 'variation' and the opposites 'monotypic', 'equality' need to be used carefully in the oceanic context, and can not be translated directly from terrestrial to oceanic conditions. Differences and variation cover the same phenomena, but diversity may result from variation as well as from taxonomic difference, while differences and monotypy are in some cases hard to separate. A more detailed approach and calculations of pelagic biodiversity are given by VAN DER S~'OEL(1994a). Thus, in the ocean, taxonomic differences between species tend to be small, within species variation or infraspecific variation and intraspecific differences are important but often merge almost seamlessly.
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8. THE RANGE AND BOUNDARY In the pelagic ocean the environment is continuous enough and dynamic enough for ranges to be determined by the species itself. Ranges are defined by: (a) environmental factors that are limiting and can only be met by the species with an absolute reaction of either being absent or present; (b) environmental factors with ranges that the species can tolerate for example by adaption; and (c) the genotypic variation which gives rise to characters which interact with the climate and with the water-mass factors. Biotic factors, i.e. mutual exclusivity between species, is not mentioned as in feeding and mobility pelagic species did not develop competitive adaptations. For (a) and (b) remember that the environment comprises the stable-biotope and substrate-biotope components. The transition s between (a) and (b) are gradual in that the extreme limits of tolerance may only be approached if at all, by a very few factors in any particular environment. In the latter situation we are dealing with the absolute reaction and in the former with the flexible reaction. There is a relation between (b) and (c) as a species' genotype cannot determine a range if the environment offers no possibility for a flexible response. Moreover, situations in which an absolute reaction has existed in the past may have changed, and a present day flexible reaction may have evolved in response to this past situation giving rise to races or subspecies within a species adapted to the extremes of the environment. In a previous attempt to describe ranges and evolution in plankton (VAN DER SPOEL, 1986) special attention was given to population dynamics. It was postulated that: 'In plankton it is not the influence of the environment but the characters of the organism that chiefly determine the ranges of the species. As population dynamics restrict the dispersal and distribution of species ... to an ... area smaller than the niche available... Evolution in the pelagic environment (in large populations) is too slow to reach optimal adaptation to the conditions of the large area available, resulting in a smaller range than possible ... Or environmental changes are still too quick which is the same as evolution is too slow.' To use 'population dynamics' in this postulate was probably an acceptable simplification. However, by replacing the concept o fpopulation dynamics by 'species specific genetic characters and adaptation developed in the species', the hypothesis better fits in the present theory. The statement 'evolution is too slow to reach optimal adaptation' seems incomplete. In reality, environmental changes in the ocean are, or were, too quick relative to the size of the habitats in the ocean. In this very large realm the changes prevent evolution from proceeding. Ranges thus are shaped by a multitude of influences in the present and past, among these are the genetic factors. All ranges have borders and though these are influenced by the same ecological factors so that with the obvious exception of the land/sea interface, the variations in responses to the various factors and the lack of sharp changes in the abiotic environment results in the borders for different species seldom coincide. The key to whether coincidence at present is important or not relies on the mechanism by which the borders are being maintained; this is an ecological question. For biogeography the question of coincidence of borders of different organisms in the open ocean is, though difficult, very relevant, since the geological history has influenced present day borders of ranges. A zone where borders of the distributions of many species are found close together, like near 42°N in the Atlantic is termed a boundary zone. It is evident that to the north and to the south of 42°N different faunas are found with cold- and warm-water representatives respectively, but exactly where is the transition between these fatmas? It is clear that all borders in a boundary zone show similar patterns, but no two are identical.
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9. THE SHOALSAND PATCHINESS Individuals of pelagic species are never distributed homogeneously over the total range of the species; there are areas of high abundance interspersed with areas of low abundance or even absence. The high abundance can be divided into two types: shoals and patches. Shoals are determined actively by the animals' behaviour and are usually structured groups of specimens with a certain orientation in space moving in the medium. Patches are more or less unstructured aggregations of specimens moving with the environment and sometimes are generated by passive response to the phytodynamics of the physical environment. Is the heterogeneous distribution within a species's range just a smaller scale repetition of the phenomena that determine the range of the species? Probably not, for shoals which are determined biotically since there are no factors limiting the size of a shoal other than the number of specimens involved and the range over which they can communicate. Involved are the specimens present in the total area covered by the vectors causing inhomogeneity and the strength of these vectors which are determining the mutual distances between the specimens. However, patches, as aggregations, are caused mainly by abiotic factors since ranges ofpelagic species are determined principally by the environment then probably patch-dynamics are indeed a scaled-down version of range-dynamics. In the patches and shoals we find the biotic and abiotic factors represented but separated, with patches being completely substratum dependent. For the low abundance areas between the aggregations one has to conclude that these are not unsuitable for the species but have only become depauperated by the aggregating forces. However, it must be recognised that mobility plays a key role. A convergence may result in the passive accumulation of planktonic taxa, but the presence of this aggregation may be an attractor for mobile micronekton that actively shoal in the zone where feeding may be better. Thus patches and shoals are formed by some of the factors also determining the range, namely part of the biotic and abiotic factors mainly related to the substrate-biotope. 10. THE GEOGRAPHICRANGESIN THE OCEAN ANDTHE APPROACHTO THEIRSTUDY The first studies on pelagic biogeography recognized only two faunas namely the cold-water and the warm-water fauna while some provincialism in these faunas resulting from isolation by continents was recognised. This simple picture ofbiogeography combined with the supposed very low diversity in the pelagic biota formed the basis for studies until the beginning of the century ( DAHL,1923). Modern approaches to pelagic biogeography were, however, al so born in these early days. HESSE(1924) for example described the maintenance of distribution patterns in relation to gyral (Zirkelstrom) and non gyral (Endstromen) current systems; this biogeographic theory was resurrected 47 years later, with the publication by McGOWAN( 1971 ). The formation of eddies and (cold or warm) core rings was also recognized, though not completelyunderstood by HESSE(1924) and it took another 50 years before studies on this phenomenon were opened again (RICHARDSON, 1976). The concepts formulated by HESSE (1924) and MCGOWAN( 1971) and others is that the environment is mainly determining the range of species. There is another school advocating that the animals themselves are more important in the process. EKMAN(1935) introduced the concept expatriation area and thus indicated the relativity of range borders. In 1953 EKMANdrew the conclusion of this in stating that 'the possibility of unobstructed transport may bring holoplanktonic animals everywhere'. The distribution of the holoplanktonic animals is, therefore, mainly dependent on their own physiological behaviour.
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Recently VAN DER SPOEL(1986) gave a slightly different interpretation of the 'physiological behaviour' in stating 'zooplankton comprises species whose individuals are passively drifted about by water movements within the stable range, defined by population dynamics, and occupied by the large, temporary or permanent populations'. It is self evident that both the organisms themselves as well as the environment influence dispersal. It needs, however, not to stay so vague. An organism, depending on its genetic and phenotypic characters, can live anywhere if it is able to surviveby interacting with the environment, either by flexibility in its responses, like adaptation in behaviour andphysiology, or to the influences which allow only an absolute reaction. Whether there is an absolute or flexible response will depend only on the environmental factors concerned. Studies of vertical distribution and migration illustrate this nicely. Many pelagic species show a vertical distribution induced by the environment; for some, temperature seems the most important factor that determines their depth, and so typically these species show subtropical submergence or comparable patterns. Other species respond to hydrostatic pressure or the light fieldin amore absolute manner showing a very fixed depth distribution independent of characteristics of the water such as currents and temperature, and so they occur within the same depth stratum everywhere. The vertical migration of many species also seems dependent on environmental factors often being triggered by variations in the light cycles. But upward migrations can be halted by high temperatures and the downward movement by low temperatures. If food is in short or abundant supply vertical ranges may be extended or even halted. In an upwelling or downwelling area both vertical migration and distribution are altered by changes in temperatures, food conditions and by active transport by the water circulation. In freshwaters, migration can be switched on in the presence of' chemicals secreted by predators. In some species, especially those with ontogenetic vertical migration, the displacement by upand downwelling is incorporated in the behaviour of the species such that they maintain their geophysical position within an upwelling system. The life history is 'adapted' in such a way that the (we)adult stage development coincides in depth and time with the upwelling so that eggs and juveniles are delivered into the surface waters in time to exploit the high productivity (SMITH, 1984). In this case it becomes very difficult to distinguish between the influence of the environment and that of the species itself. Another difficulty is that in some species vertical migration is more extensive at the periphery rather than at the centre of the range (ANGEL, 1979). So either near the periphery the species behaves differently, or some external factor near the periphery is inducing a different migration pattern, possibly the increasing abundance of a predator or a competitor. One can conclude that geographic ranges of individual taxa are determined by species-specific characteristics. I I. CLIMATEVERSUS WATERMASS The climate seems sometimes to have the greatest in fluence, in other cases the water-mass seems to have predominant infuence on the distribution patterns (VANDERSPOELand HEYMAN,1985). Most patterns are, however, influenced by both phenomena. The climate has its greatest influence on the pelagic realm where it determines the annual cycles of water temperature and daylight through insolation. The most typical feature of the water-mass is its chemical andnutrient contents. An animal digests food with enzymes and the enzyme reaction is temperature dependent. The food available is thus dependent not only on the food actually present, but also the ambient
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temperature. The quantity of food available is determined initially by solar energy and other local conditions such as nutrient concentrations, which are typically stable-biotope components, but its nutritional value is determined by a typically substrate-biotope factor of the in situ water temperature at which digestion takes place. Enzymatic reactions regulating an organism's metabolism (e.g. assimilation and digestion) are temperature dependent. This is of fundamental importance to the niche concept and the treatment of populations and biogeography. The deep-sea biotope is characterized by low temperatures and low food budgets. However, in some oceanic region s normally deep-living animals occur at shallow depth (VAN DERS POELand SCHALK,1988). Surprisingly in these regions (Mediterranean, Banda Sea) the deep temperatures are unusually warm. Since the quantity of food available is low and the animals' metabolic activities are higher as a result of the warm temperatures, the animals are confronted with starvation unless they can shift towards the surface in search of food. This vertical shift, and vertical migration in general, must be dependent on the temperature characteristics of the organisms' enzymes. With unfavourable conditions, the species may be able to change its niche. When food becomes limiting the metabolic activity of the animals may need to be lowered, but when the metabolic rate is increased by high temperature, more food has to be found. The former occurs in diurnal migrants which when they migrate deeper encounter lower temperatures and so their metabolism slows automatically conserving energy. The latter phenomenon occurs in deep-sea animals forced up towards the surface by high temperatures at depth (VAN DER SPOEL, 1994b). When studying evolution in diurnal migrants, it should be borne in mind that their ancestral environment is in the epipelagic. Thus these speciesmay co-occur at night but occupy bathymetrically distinct ranges during day-time. So closely related species may be isolated (sympatric) at night in meso- or bathypelagic strata but co-occur (allopatric) in the day-time. It is clear that organisms in their dispersal are influenced by four types of factors: ( 1) absolute factors, (2) variable factors, (3) factors linked with climate, and (4) factors linked with water mass. 12. CONCLUSION A general conclusion is that in the pelagic realm there are no boundaries or barriers to distribution, and that all environmental changes are gradients between nodal-points-of-stress in a three-dimensional space characterised by factors which are either fixed in space, the locally stable ones, or those moved with the water-masses. Life in general and life of each individual in the pelagic realm is determined by four categories of factors; those related to the gradients, those related to nodal-points-of-stress, those related to stable local conditions, and those related to the moving substrate. To some of these factors a given taxon may react in an absolute fashion and to others flexibly. As in the terrestrial realm pelagic populations, ranges and food chains show stability. This stability is derived from interactions between either gradients and substratum or of nodal-pointsof-stress and stable local conditions. In both the former and the latter case it is the behaviour of the organism that determines the eventual effects of the factors responsible for the stability. Thus behaviour developed during evolution determines population ranges, structures, and migrations. 13. ACKNOWLEDGEMENTS Dr M.V. Angelis kindlyacknowledgedfor the additions,correctionsand polishing ofthis paper.This paper was originally presented at the SCOR WG 93 meeting in Amsterdam in 1993.
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BAD('OCK,J. ( 1981 ) The significance of meristic variation in Benthosema glaciale (Pisces, myctophoidei) and the species distribution offnorth west Africa. Deep-Sea Research, 28(12), 1477-1491. BEKLEMISHFN,C.W. ( 1961 ) On the spatial structure of plankton communities in dependence of oceanic circulation. Boundaries of ranges of oceanic plankton animals in the north Pacific. Okeanologia, 5, 1059-1072. BEKLEMISHEV,C.W. ( 1971) Distribution of plankton as related to micropaleontology. In: The micropaleontology of oceans, B.M. FUNNELand W.R. R/EDEL,editors, Cambridge University Press, 75-87. BEKLEMISHEV.C.W. ( 1981 ) Biological structure of the Pacific Ocean as compared with two other oceans. Journal of Plankton Research, 3(4), 53 i-549. DAHL, F. (1923) Okologische Tiergeographie. Fisher Verlag, Jena, 122pp. EKMAN, S. (1935) Tiergeographie des Meeres. Leipzig Akademie Verlagsgesellschaft, 542pp. EKMAN, S. (1953) Zoogeography of the sea. Sidgwick and Jackson Ltd., London, 417pp. HESSE, R. (1924) Tiergeographie. Fisher Verlag Jena 613pp. HII,(;ERSON, P.C.J. and S. VAN DER SPOEL (1987) East-west variation in Diacria off northwestern Africa. Malacological Review, 20, 97-104. MARtIAI,EFF,R. (1978) What is an upwelling ecosystem? In: Upwelling eco.systems, R. BOJE and C. TOMCZAK, editors, Springer Verlag, Berlin, 12-23. MAYR,E. ( 1971 ) Populations, ,s79eciesand evolution. Belknap Press, Harvard University,Cambridge, Massachusetts, 453pp. McG~)WAN,J.A. ( 1971 ) Oceanic biogeography of the Pacific. In: The micropalaeontology of oceans. B.M. Fl ~YYEL and W.R. RIEDEL,editors, Cambridge University Press, 3-74. McGOWAN, J.A. (1974) The nature of oceanic ecosystems. In: The Biology of the Oceanic Pacific', Oregon State University Press, 9-28. PALl~MBI,S.R. (1992) Marine speciation on a small planet. Trends in Ecology and Evolution, 7, 114- I 18. PETIPA, T.S. (1979) Trophic relationships in communities and the functioning of marine ecosystems. In: Marine production mechanisms. M.J. DUNBAR,editor, Cambridge University Press, 233-250. RICHA~)SON, P. (1976) Gulfstream rings. Oceanus, 19(3), 65-68. RINGELBERG,J. (1976) Aquatische Ecologic, Bohn, Scheltema and Holkema, Utrecht, 240pp. SCHALK,P.H. (1988) Monsoon influences on biogeography and ecology of zooplankton and micronekton of the lndo-Malayan region. Phi) Thesis, University of Amsterdam, 144pp. TmmoT, A. ( 1987) Zooplankton communities in the West African upweiling area. In: Upwelling systems, R. BOJE and C. TOMCZAK,editors, Springer Verlag, Berlin, 32-61. SAVID¢;E, G., D.R. TURNER, P.H. BURKJLL, A.J. WATSON, M.V. ANGEL, R.D. PINGREE,H. LEACH and K.J. RICHA~)S, (1992) The BOFS 1990 Spring Bloom Experiment: Temporal evolution and spatial variability of the hydrographic field. Progress in Oceanography, 29, 235-281. SMITH, S. (1984) Biological indications of active upwelling in the northwestern Indian Ocean in 1964 and 1979, and a comparison with Peru and northwest Africa. Deep-Sea Research, 31, 951-967. VAN DER SPOEL, S. (1986) What is unique about open-ocean biogeography, zooplankton? UNES('O Technical Papers, Marine Biology, 49,254-260. VANDERS POEt,,S. (1994a) The biosystematic basis for pelagic biodiversity. Bijdragen tot de Dierlcunde (in press). VAN DER SPOEL, S. (1994b) A warning from the deep. Progress in Oceanography, 34,207-210. VANDERSPOEt, S. and R.P. HEYMAN(1985) A comparative atlas of zooplankton, biological patterns in the oceans. Bunge Utrecht, 186pp. VINOGRADOV,M.E., I.I. GITELZONand Y.I. SOROKIN(1973) The spatial structure of communities in the euphotic zone of the ocean tropics. In: Life activity ofpelagic communities in the ocean tropics, M.E. VINOGRADOV, editor.. Israel Program for Scentific Translations, Jerusalem, 187-298. VORONINA,N.M. (1978) Variability of ecosystems. In: Advances in Oceanography, H. CHARNOCKand S. DEACON, editor,;, Plenum Press, New York, 221-243.
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