Biogeography and evolution of body size in marine plankton

Earth-Science Reviews 78 (2006) 239 – 266 www.elsevier.com/locate/earscirev

Biogeography and evolution of body size in marine plankton Daniela N. Schmidt a,b,⁎, David Lazarus c , Jeremy R. Young d , Michal Kucera a,1 a

c

Department of Geology, Royal Holloway University of London, Egham, TW20 0EX, UK b UK and Department of Earth Science, University of Bristol, Bristol, BS8 1RJ, UK Museum für Naturkunde, Humboldt Universität zu Berlin, Invalidenstrasse 43, 10115 Berlin, Germany d Palaeontology Department, The Natural History Museum, Cromwell Road, London SW7 5BD, UK Received 24 January 2005; accepted 23 May 2006 Available online 26 July 2006

Abstract Body size is a central feature of any organism, reflecting its physiology, ecology and evolutionary history. Marine microplankton are major contributors to the particulate inorganic carbonate (foraminifers and coccolithophorids) and opal f lux (radiolaria and diatoms) in the ocean and, hence, size changes in these organisms can influence global biogeochemical cycles. This paper is discussing abiotic influences on micro- and macroecological size changes among major marine plankton groups, linking these to evolutionary size changes during the Neogene. We review the patterns and outline the causes of size changes geographically and through time in coccolithophorids, foraminifers and radiolarians. The main feature of the Neogene size record is a dramatic size increase in foraminifers, a similarly dramatic reduction in the size range of coccolithophorids and highly variable size patterns in radiolarians. We argue that the observed pattern is too complex to be explained by a simple common forcing and propose that speculations on the response of oceanic biomineralisation to global warming have to consider the scales at which marine plankton evolve. © 2006 Elsevier B.V. All rights reserved. Keywords: planktic foraminifera; radiolarian; nannoplankton; size; biogeography; evolution; palaeoceanography

1. Introduction 1.1. Body size — why does it matter? The origin of major innovations and the underlying causes for the radiation of form, that is size and shape, is one of the most challenging questions in biology ⁎ Corresponding author. Department of Earth Sciences, University of Bristol, Wills Memorial Building, Bristol BS8 1RJ, United Kingdom. Tel.: +44 117 954 5414; fax: +44 117 925 3385. E-mail address: [email protected] (D.N. Schmidt). 1 now at Institut f ür Geowissenschaften, Sigwartstrasse 10, 72076 Tübingen, Germany. 0012-8252/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.earscirev.2006.05.004

(Carroll, 2001). The physical boundary conditions, i.e. environmental influences, controlling rates, magnitudes, spatial scale and frequency of morphological change are still poorly understood (Jablonski, 2000). Recently, there has been an increased interest in the factors controlling size (Peters, 1983; Calder, 1984; Reiss, 1989; Brown, 1995). Body size is a central feature of any organism and it is correlated with many physiological, ecological and life history traits (McKinney, 1990b). Among these are metabolism, respiration, ingestion, predator–prey relations, resistance to starvation and aspects of life history (Peters, 1983). Size depends amongst other factors on the ability to gather and process food, the proportions of acquired energy used

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for maintenance, the allocation of surplus energy to growth and reproduction, and initial size (Kozlowski and Gawelczyk, 2002). It can be limited by the structure of an organism, its physiology and energetic demands and its ecology (Skelton, 1993). Size is a visible proxy for life history events, because changes in growth rate, maturation and death are manifested in body dimensions which therefore, can be used to characterise evolutionary patterns (McKinney, 1990b). Size is an obvious morphological characteristic, readily preserved in fossils, easy to measure, conspicuous, ecologically important, comparable across taxa and extremely variable through time and space (Peters, 1983). Consequently, this parameter has been studied for numerous groups of organisms (see examples in Peters, 1983; Skelton, 1993; Futuyma, 1998). 1.2. Why marine plankton The prerequisites for studies of the evolution of size are well-dated continuous sediment sequences with a high abundance of well-preserved fossils of global occurrence. Planktic organisms (Fig. 1) within Cenozoic marine deep-sea sediments match all of these criteria. Most importantly, they can be found in large numbers to gather statistically significant datasets. For the same reasons, they are extensively applied in palaeoceanographic and palaeoclimatic studies. The analysis of species compositions (e.g., Imbrie and Kipp, 1971; Brathauer and Abelmann, 1999; Gersonde and Zielinski, 2000), stable isotopes (Shackleton and Opdyke, 1973; Hays et al., 1976), and other chemical tracers in their tests, e.g. Mg/Ca (e.g., Nürnberg et al., 1996), Cd/Ca ratios (e.g., Delaney and Boyle, 1987), Zn/Si ratios (Ellwood and Hunter, 2000), Neodymium isotopes (e.g., Vance and Burton, 1999) or Boron isotopes (e.g., Sanyal

et al., 1995) have proven to be valuable tools for palaeoclimatic and palaeoceanographic reconstructions. Morphological criteria used in such studies include size, shape and coiling properties of the test (e.g., Ericson, 1959; Bé et al., 1973; Hecht et al., 1976; Naidu and Malmgren, 1995). Plankton skeletal remains built up the bulk of deep sea deposits (Seibold and Berger, 1993). About half of the deep-sea is covered by oozes, i.e. sediments formed of plankton remains (Seibold and Berger, 1993). The main shell-producing planktic organisms are foraminifers, radiolarians (heterotrophic protists), coccolithophorids, diatoms (algal protists) and pteropods. These organisms are major contributors to the particulate inorganic carbonate (foraminifers and coccolithophorids) and silicate flux (radiolaria and diatoms) in the ocean and thus play an important role in the global carbon and silicate cycles. Most of the skeletal remains are remineralised on the way to the sea floor and are vitally important for the global carbon and silicate cycling in the surface ocean (Fig. 2). 1.3. Body size changes in space and time Pelagic ecosystems are structured both geographically and by water depth. These ecosystems are related to the major surface water masses (Fig. 3). These are the result of wind directions (zonal currents), the position of land masses (boundary currents along the continents) and the balance between precipitation and evaporation. Individual water masses are characterised by variations in e.g. salinity, temperatures, light attenuation, nutrients, oxygen, and productivity. Vertical temperature and salinity gradients create density surfaces, e.g. the pycnocline, which are associated with maxima in plankton abundance (Norris, 2000).

Fig. 1. Illustration of representative species of the discussed plankton groups. From left to right: coccolithophores (Gephyrocapsa muellerae), planktic foraminifers (Globigerinodes sacculifer) and radiolarians (Lamprocyclas maritalis, courtesy K. Bjørklund).

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Fig. 2. Box plot showing the carbonate budgets (modified after Elderfield, 2002), accumulation rates in the marine environments (Milliman, 1993), and relative contribution of calcareous plankton (Schiebel, 2002). Carbonate production is a source of atmospheric CO2 on short time scales and a sink on geological ones. Photo of Great Barrier Reef courtesy of M. Cottam.

Fig. 3. Major current systems of the modern ocean modified after Tomczak and Godfrey (1994) and Stewart (2003). Grey lines indicate warm currents, black ones cold currents. C = current, Cc = countercurrent, Eq = equatorial, N = north, S = south.

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Every organism is adapted to specific “optimum” environmental conditions (Fig. 4), under which it is able to flourish best (e.g., Kennett, 1968a,b; Bé et al., 1973; Hecht, 1976). Optimum environmental conditions can either lead to rapid reproduction, and hence small size (e.g. benthic foraminifers Bradshaw, 1961) or fast growth rates and large size (e.g. coccolithophorids and planktic foraminifers Hecht, 1976; Bollmann, 1997; Schmidt et al., 2004a). It is an oversimplification that large size is associated with slow growth and delayed maturation. If large size is favoured, rapid growth rates and fast maturation are selected for. Large size in plankton is, in general, more likely to result from faster growth than prolonged growth. Planktic foraminifers typically reach maximum size in their preferred water mass, and decrease in size away from such areas (Hecht, 1976; Schmidt et al., 2004a). In contrast, radiolarian test sizes tend to be fairly constant regardless of the environment and, hence, do not show a systematic change of size with changing environmental conditions. Only a few examples of radiolarian size gradients exist (Bjørklund, 1977; Cortese and Bjørklund, 1997) and these might reflect unrecognized taxonomic variation. For planktic organisms, “optimum” environmental distributions are not just geographical but also related to depth, i.e. a shallow water species would be under stress in greater water depth (Hecht and Savin, 1972) where its growth rate will decrease (Fig. 5). Non-optimum growth is a result of stress on all physiological functions. The optimum environmental conditions (black part of the distribution in Figs. 4 and 5) are narrower than the organisms' niche, which we define as an attribute of an environment (environmental niche,

Fig. 4. Idealised temperature growth model for a warm water and a cold water foraminiferal species modified after Hecht and Savin (1972) following Bradshaw (1961). The environmental niche is dived into optimum growth, reproductive range, growth limits and lethal conditions.

Fig. 5. Idealised growth model applied to depth habitats for a shallow dwelling and a deep dwelling species (Hecht and Savin, 1972).

Grinnell, 1917; Elton, 1927) and not a population niche (population in relation to its environment, Hutchinson, 1957). If environmental conditions change through time, the organism can react either by ecophenotypic plasticity, i.e. the change is within its adaptive range (Mayr, 1970), or by tracking its habitat (e.g., Renaud and Schmidt, 2003). The plasticity can be continuous or discrete; reversible or irreversible and if it is irreversible, it can lead to the origin of ecotypes, i.e. genetically determined phenotypes associated with certain ecological conditions (Gordon, 1992). “Habitat tracking”, an oscillation of species with respect to environmental change, demonstrates the stability of species morphologies despite environmental change, as long as a suitable habitat can be found and occupied. Habitat tracking suggests that stabilising selection, rather than directional selection, will be the rule, as long as species can continue to “recognize” and occupy suitable habitats (Eldredge et al., 1997). Under this model, innovations can only occur in response to extreme amplitudes of environmental change. Several different patterns of size changes over long time scales have been described in the literature. Traditionally, trends are interpreted as evidence for natural selection sorting individuals within species (e.g. Darwin, 1859). More recently, trends have been interpreted as differential speciation and/or survivorship based on morphological characters (Eldredge and Gould, 1972; Stanley, 1975). Morphological evolution is influenced by morphological constraints (Wagner, 1996, and references

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therein). Furthermore, a trend in a character might not reflect selection at all, being simply a by-product of an increase in variance (Gould, 1988b, Fig. 6). Size trends can be active (i.e., biased replacement of morphology) or passive (i.e., increase in variance within a clade or group, Wagner, 1996). The expansion of morphological variance over time (Stanley, 1973; Norris, 1991; McShea, 1994) can be related to the fact that evolution often starts near some “limiting boundary” also termed the “left wall” (Stanley, 1973), i.e. the diffusion away from an originally small-sized ancestor, since small species seem to be less prone to extinction during a catastrophic event (Norris, 1991). Cope's rule, i.e. increase in body-size along a lineage, can be interpreted as an evolutionary trend away from small size (Fig. 6) rather than towards larger size (Stanley, 1973). Limiting boundaries in body size can occur in aspects of shell construction (Norris, 1991) and morphological complexity (McShea, 1994). The position of such barriers is expected to vary through time (Stanley, 1973; Skelton, 1993; Wagner, 1996). The tendency towards larger size within a taxon produces an increase in mean and maximum size, but not necessarily in minimum size (Bonner, 1968; Gould, 1988a; McShea, 1994). Size increase is more common than size decrease, possibly since adaptive breakthroughs leading to new taxa tend to arise at relatively small body size and extinction often occurs in large, structurally specialised lineages (Stanley, 1973). Size changes through time can be attributed either to adaptation or speciation. Adaptation is conventionally

Fig. 6. Idealised graphs illustrating four potential evolutionary changes in body size. Vertical axis represents changes in maximum size, the horizontal in minimum size. The thin grey line represents original population, the thick black one the descendants. The upper right quadrant illustrated Cope's rule sensu stricto, the lower left evolutionary size decrease; the upper left an increase in variance, the lower right a decrease in variance (modified after Jablonski, 1996).

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defined as a process by which an organism is selected to better fit a pre-established environment (Laland et al., 2004). Lineages may change body sizes with or without major niche transitions (Stanley, 1973). The mean overall size trend depends on the position of the ancestor of the higher taxon within the size-frequency distribution of the higher taxon. Stanley (1973) assumes that pronounced size change is associated primarily with speciation events, although trends of gradual intraspecific body size increase are not ruled out. 1.4. The causes of body size variation through time Sudden and profound changes in size demand a causal mechanism. The causes for a change can be internal (allometric changes, e.g. metabolism, physiology) or external, reflecting changes in interaction with abiotic and biotic environment (e.g. predator prey relationships, population density) (McKinney, 1990b). The environment may act directly on body size at a specific stage, growth rate at a certain age, timing of certain events, or all of the above (McKinney, 1990b; Stearns, 1992). Body size is genetically and geometrically constrained (Skelton, 1993) with a heritability of over 50% (Atchley, 1983). Whatever the genetic basis, heritable size change is usually the result of change in the timing or rate of developmental events relative to the same events in the ancestor (Gould and Eldredge, 1977; McKinney and McNamara, 1991; Skelton, 1993). Changes in the timing of developmental events (heterochrony) can be caused either by exaggeration of adult characteristics (peramorphosis) or retention of juvenile characteristics (paedomorphosis) (Fig. 7). An exaggeration of adult characteristics is recognised by an increased rate of shape change or an extension of its period of operation, whereas retention of juvenile characteristics is observed as a reduced rate of change or a contracted period of operation (Gould and Eldredge, 1977; McKinney and McNamara, 1991; Skelton, 1993). Exaggeration of adult characteristics results from faster development (acceleration), earlier onset of a development (predisplacement) or later offset of development (hypermorphosis). Retention of juvenile characteristics results from slower development (neoteny), later onset of development (postdisplacement) or earlier offset of development (progenesis). Neoteny may lead to larger adult size, while acceleration may lead to smaller adult size (McNamara, 1986). Size changes often occur in response to selection pressure resulting from one or more advantages. The intrinsic advantage concept is often oversimplified (Stanley, 1973). Body size within populations and assemblages is roughly log-normally distributed

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of foraminifers (Luterbacher and Premoli Silva, 1964; Norris, 1991). Some processes depend on the surface area, others on volume. Size changes affect these two parameters in different ways: isometric features increase with the cube of linear dimensions, while surface-area related features increase only with the square of linear dimensions. Thus, surface-area-dependent processes, such as feeding, respiration, and skeletal support, have to keep pace with volume and weight increases. We want to note that, although we will concentrate in the paper on size changes of adult organisms, body size changes are often affected by environmental selection not only on size itself, but on developmental rates or shape which can affect final adult size and that all phases of ontogeny are under selection (McKinney, 1990b). 1.5. Aim of the paper

Fig. 7. Morphological expressions of heterochrony modified after McKinney (1986). The plot shows allometric growth trajectories, i.e. bivariate plots of size (as a proxy for time) versus another trait. Note that most of the time the relationships will follow the same trajectories, but organisms may mature at a different size or have a different maximum size.

(LaBarbera, 1989; Schmidt et al., 2004a), i.e. small organisms are more common. For their particular niche, small organisms are as well adapted as large ones (McKinney, 1990b). Proposed advantages of large size are improved ability to capture prey or avoid predators, greater reproductive success, expanded size range of acceptable food, decreased mortality, extended individual longevity and metabolic benefits, e.g. increased heat retention per unit volume (Stanley, 1973). Yet, large size also has disadvantages; for instance, feeding efficiency must increase substantially. Large size and the associated allometric requirements can limit the future evolution of a species (McKinney, 1990b) and, since large species within assemblages usually have lower population densities than smaller ones, they are more prone to extinction as shown for the K/P boundary mass extinction

The goal of this paper is to discuss the palaeoecological, palaeobiogeographical and evolutionary significance of size variability in marine plankton. The geographic and ecological patterns of size variability will be first documented in the Holocene. A set of initial hypotheses linking size with geographic and ecological variables will be tested in the Late Quaternary. Then, size variability will be discussed throughout the Neogene for the most important plankton groups: planktic foraminifers (protista, zooplankton), radiolaria (protista, zooplankton) and coccoliths (haptophytes, phytoplankton). Unfortunately, size in marine diatoms is rarely investigated (Sorhannus, 1990) and hence not included in this review. Sample sets, covering large environmental gradients and long time scales, allow disentangling global, general mechanisms influencing size variability in plankton. Large-scale size trends sacrifice the detail of local-scale studies in the hope of identifying general principles or broad patterns in evolutionary and ecological systems and are known as “Macroevolution” and “Macroecology” (Brown, 1995; Gaston and Blackburn, 2000; Caroll, 2001). We will try to compare global with regional studies to evaluate “macro” and “micro”-scale influences on size of Neogene marine plankton. 2. The ecology of the investigated groups 2.1. Coccolithophores Coccolithophores are unicellular phytoplankton belonging to the phylum Haptophyta. The individual cells are minute, typically 2–20 μm in diameter (Fig. 8), but

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Consequently diversities of coccolithophorids are high, and production rates of coccoliths are significant, even in the most nutrient-poor regions of the oceans, the subtropical gyres. Production of coccoliths is higher in upwelling zones and in temperate/subpolar latitudes where nutrient supplies are higher, but diversities decline. In very high nutrient areas, such as upwelling zones in the eastern tropical oceans (i.e., meridional upwelling), polar divergences and near river mouths, production of coccoliths is reduced and is often minimal. Fig. 8. Relationship of coccolith size to coccosphere size. SEM pictures of three coccolithophores; A. Alisphaera unicornis B. Calcidiscus leptoporus, C. G. muellerae. In placolith-bearing genera such as Calcidiscus and Gephyrocapsa, coccolith length is about 0.5× of coccosphere diameter. However, this relationship does not hold for other coccolith types as exemplified by Alisphaera for which coccolith length is about 0.2× of coccosphere diameter.

occur in high abundances, thousands to millions of cells per litre, throughout the upper layers of the ocean. The cells are surrounded by an exoskeleton, coccosphere, formed of calcareous plates, coccoliths, which significantly contribute to the marine carbonate production (Fig. 2). Today, they are one of the main open ocean primary producers. The first recorded coccoliths occur in the late Triassic (Carnian) and they have a continuous record from then to t present day (Bown, 1998). Individual coccoliths are a few microns (1–15) in diameter (Fig. 8). There are two forms of coccoliths, holococcoliths which are formed from arrays of minute (ca 0.1 μm) euhedral calcite crystals and heterococcoliths which are formed from radial arrays of larger, complex-shaped, calcite crystals (Bown, 1998). Typically coccolithophores have haplo-diplontic life-cycles with heterococcoliths being produced by the diploid phase and holococcoliths by the haploid phase (e.g., Young et al., 1997; Houdan et al., 2004b). The distributions and abundances of coccolithophores depend primarily on nutrient supply and temperature. Coccolithophores, because they are marine algae, require sunlight for growth and are essentially limited to the top 50–200 m of the water column There are often well-differentiated upper photic and deep photic communities, typically separated by the thermocline (Winter et al., 1994). Nutrient supply is the other prime control on phytoplankton distribution, especially concentration of the macronutrients nitrate and phosphate. In the case of coccolithophores this control is complicated by the fact that the group is predominantly K-selected, i.e. adapted to low nutrient oligotrophic conditions (Brand, 1994; Young, 1994). In eutrophic conditions they are typically outcompeted by diatoms.

2.2. Planktic foraminifers Planktic foraminifers are marine, stenohaline protozoa. They originated from benthic foraminifers in the mid Jurassic. Their distribution and carbonate productivity are similar to those of coccolithophorids (Fig. 9). Planktic foraminifers which inhabit the photic zone often live symbiotically with photosynthesising algae such as dinoflagellates, diatoms and chlorophytes. Having algal symbionts is highly advantageous in oceanic waters where inorganic nutrients and food are scarce, so a diverse assemblage of planktic foraminifers thrives in the nutrient-poor subtropical gyres (Bé and Tolderlund, 1971). Greater abundances of fewer species thrive in equatorial upwelling zones and along continental margins, resulting in higher rates of foraminiferal carbonate production (Fig. 9). Planktic foraminifers require deep oceanic waters to complete their life cycles, and are thus known to avoid

Fig. 9. Abundance of planktic foraminifers in the upper 10 m of the modern ocean (modified after Bé and Tolderlund, 1971).

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neritic waters over continental shelves (Hemleben et al., 1989). Foraminifers are preyed upon by many non-selective planktotrophs including worms, crustacea, gastropods, echinoderms, and fish (Lipps and Valentine, 1970). 2.3. Radiolaria Radiolaria are holoplanktic protozoan zooplankton (Casey, 1987). They are divided into several larger taxonomic groups, but only the polycystine radiolarians, whose shells are made from opaline silica, are common as fossils. Radiolaria have a fossil record extending back at least to the Cambrian. In the modern ocean (Fig. 10) they are secondary contributors to biosiliceous sediments after diatoms, but were important sources of chert in older sediments prior to the spread of diatoms in the Cenozoic. Radiolarian ecology is similar in most respects to planktic foraminifers, in that both groups are micro-heterotrophs, and that many photic zone forms possess symbiotic algae. Radiolarians however are much more diverse than planktic foraminifers with several hundred described living forms; they inhabit a much greater range of water depths (many species seem to be found only well below the thermocline); and, because of their use of opal to form their shells, their growth and preservation in the sediment are partially controlled by dissolved silica concentrations in the water. 3. The Neogene climate change The focus of this review is the plankton body-size reaction to environmental change during the Neogene. This change will be assessed in the framework of two different time scales, the late Pleistocene glacial–interglacial cycles and the long term Neogene climatic change.

Tectonically, the major events during the Neogene are the restriction and/or closure of the Tethyan seaways, first between Asia and Africa (Langhian, Sharland et al., 2001) and then between North and South America (Haug and Tiedemann, 1998). The major oceanographic events during the Miocene also include the Monterey Event, a period of enhanced diatom production in vast regions of the Pacific Ocean (18–12.5 Ma, Vincent and Berger, 1985), the “carbonate crash”, a sharp drop in carbonate accumulation (12–8 Ma, e.g. Farrell et al., 1995), the “biogenic bloom” events, a significant increase in opal accumulation (7–4 Ma, Farrell et al., 1995) and the Messinian Salinity Crisis, following the desiccation of the Mediterranean (Hsü et al., 1977). The Neogene climate (Fig. 11) is dominated by an overall cooling (e.g. Zachos et al., 2001). Global circulation patterns changed as Antarctica became increasingly isolated and the circum-polar circulation (Fig. 3) strengthened. This reduced significantly the mixing of warmer tropical water and cold polar water, and permitted a second phase of build-up of the Antarctic polar cap after its Eocene initiation. The mid-Miocene Climatic Optimum, around 17 to 15 Ma (Zachos et al., 2001), was the last significant period of global warmth, followed by global cooling linked to the expansion of a major ice-sheet in East Antarctica (Vincent et al., 1985). Additional cooling and ice-sheet expansion in West Antarctica (Kennett and Barker, 1990) is indicated by rising of δ180 values into the early Pliocene. The early Pliocene was characterised by a subtle warming trend lasting until 3.2 Ma (Pliocene Climate Optimum). Since 2.6 Ma, pronounced cyclic changes (Shackleton, 1984; Shackleton et al., 1990) in ice volume (onset of Northern Hemisphere glaciations) are indicated by δ180 values in benthic foraminifers, associated with sea level fluctuations and a higher oceanic turnover rate.

Fig. 10. Flux of siliceous fossils to the sea floor (after Berger and Herguera, 1992). The flux is dominated by diatoms.

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Fig. 11. Global deep-sea oxygen isotope record representing Cenozoic polar cooling and ice accumulation (modified after Zachos et al., 2001).

One of the most conspicuous changes in the Neogene sediments is the increased importance of siliceous biogenic productivity and sedimentation at high latitudes during. During the gradual cooling, siliceous biogenic production at high latitudes increased reducing the extent of carbonate sediments (Kennett, 1977). In addition, enhanced opal deposition was documented in the equatorial Pacific (Barron and Baldauf, 1989) and in the upwelling systems (e.g., Berger et al., 2002). 4. Methodology 4.1. Body size proxies Body size is a highly derived composite variable and virtually impossible to measure completely even in living organisms. Fortunately, growth of many components constituting size is so highly covariant that any one will usually serve as a good approximation (McKinney, 1990a). Size or some reasonable proxy for body size is preserved in most fossilised organisms (McKinney, 1990b). The most important size parameters in unicellular plankton are cytoplasm volume, the shell size, and the total weight. All are presumably correlated, but could vary to a significant degree depending upon taxonomic groups. Ecologically, the volume of the biomass is the most important size parameter, but it cannot be directly measured in the fossil record. In planktic foraminifers, cytoplasm weight is linearly correlated with test size (Spero et al., 1991). Similar correlation can be expected

for radiolaria, although this assumption has never been tested. Furthermore, at least among many nassellarian species, the main cytoplasmic mass occupies only a fraction of the shell, which extends like a funnel beyond it. The shell is covered with a thin coating of cytoplasm. The effective size of the radiolaria and foraminifers is much larger due to the extended pseudopods and actinopods, and the varying development of the external bubble layer in radiolaria and some foraminifers. For coccolithophores assessment of size variation is complicated by the fact that complete coccospheres are too rarely preserved to be used for size variation study. Consequently, isolated coccoliths have to be studied and these do not have a simple relationship to coccosphere size. Across the total diversity of extant coccolithophores there is enormous variation in the number of coccoliths per coccosphere (Fig. 8), from several hundred in genera such as Polycrater, Pleurochrysis and some holococcolithophores to 10 to 20 in genera such as Pontosphaera, Coccolithus or Gephyrocapsa (Yang and Wei, 2003). Consequently, at this level, there is no consistent relationship between coccolith size and cell size, indeed the ratio of coccolith length to cell length varies from about 0.8 to <0.1 (Young, unpubl. data). However, within most families of coccolithophores the variability of coccolith number per coccosphere is much lower and there is good correlation of coccolith size with cell size. In particular this holds within the heterococcoliths of the dominant well-fossilised families, the Coccolithaceae, Calcidiscaceae and Noelaerhabdaceae (including

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Gephyrocapsa and Emiliania). All these families are characterised by non-motile diploid phases bearing robust heterococcoliths formed of two shields (placoliths) which interlock to produce robust coccospheres with typically 10 to 20 coccoliths per coccosphere. In some of these species, most notably Emiliania huxleyi, multi-layered coccospheres are formed with much higher variability in coccolith number but this does not affect the ratio of coccolith length to cell diameter which is typically in the range of 0.6 to 0.8 (Young, unpubl. data). Hence an analysis of coccolith size variability confined to these groups should allow meaningful comparisons with foraminifers and radiolarians. Fortunately these three families are also the most abundant and best studied groups of coccolithophores. A wide range of methodologies have been used over the past two decades to measure coccolith size (Young et al., 1996). Fortunately, coccolith size is a very simple parameter to measure and our inter-calibration experiments have consistently shown that different methodologies produce directly comparable results (Young, unpublished data). 4.2. Size measurements Size can be expressed in several different ways, e.g. as the maximum diameter or area. Sometimes a specific part of the organism (e.g., the width of the 4th segment within the radiolarian test, Kellogg and Hays, 1975) is used to express size changes. Surface area is important for any kind of interaction with the environment. In foraminifers cross-sectional area and diameter are highly correlated (Schmidt et al., 2004a). To assess the impact of size changes in microorganisms on biogeochemical cycles, the weight of the tests is the most important factor. Weighing microfossils is a tedious job, but unless shape changes during the life cycle (see Young and Ziveri, 2000), it can be approximated by the cube of a linear size measure (Schiebel and Hemleben, 2000; Young and Ziveri, 2000). 4.3. Taxonomic level Changes in size can be considered at different taxonomic levels, in individual species, along a lineage, in families and orders. All taxonomic levels are based on the morphological species concept. Recent genetic work has indicated that many planktic “morphospecies” (see Lazarus, 1983 for discussion) consist of distinct “genetic species” (e.g., Huber et al., 1997; de Vargas et al., 1999, 2001, 2004; Darling et al., 2004; Geisen et al., 2004). Such cryptic species often exhibit distinct distributional

patterns and their succession in space could represent latitudinal clines in morphology (de Vargas et al., 2001). Any size trends in “morphospecies” can be thus “invisibly” influenced by species replacement through “cryptic species”, which are morphologically very similar. In a population, the size of several specimens, on average typically around 50 individuals, is used to express mean size. Sometimes these specimens are “randomly” picked (e.g., Malmgren and Kennett, 1972), sometimes a representative split is analysed (Renaud and Schmidt, 2003). Next to populations, some studies have worked on the entire order of planktic foraminifers (Gould, 1988b; Arnold et al., 1995; Schmidt et al., 2003, 2004a,b,c) or radiolarians (Moore, 1969; Harper and Knoll, 1975), to analyse macroevolutionary/macroecological (evolutionary/ecological change above the species level) processes. These have either been done by analysing several species per time interval or by analysing entire assemblages. Working on entire assemblages is a taxon-free approach which avoids bias of any kind of grouping. Investigating entire assemblages enables the analysis of long-term and global processes, since the datasets can be complied globally and stratigraphically with the same method. Schmidt et al. (2004b,c), found that the 95-percentile, the value separating the 95% smallest from the 5% largest in the assemblage was most useful to characterise changes in size within assemblages of planktic foraminifers. 4.4. Age models The age models for all datasets presented herein were recalculated following Berggren et al. (1995) for the Cenozoic and Shackleton (1996) for the Pleistocene. For the G. tumida lineage (Malmgren et al., 1983) the amended age model of MacLeod (1991) was used taking an unconformity in the record into account. 5. Body size of modern plankton The factors influencing size vary with the taxonomic level and on spatial scales for the different groups. Intraspecific size variability also depends on physicochemical and biotic constraints. Since the organisms have very different environmental demands we will discuss these influences for each group individually. 5.1. Coccolithophorids Reproduction in coccolithophorids, as in many other protists, is by simple asexual binary fission (e.g. Klaveness, 1972; Hori and Green, 1994; Pienaar, 1994). There is also a sexual life-cycle with meiosis producing haploid, typically

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holococcolith-bearing, cells followed by syngamy to produce diploid, typically, heterococcolith bearing, cells (e.g. Cros et al., 2000; Houdan et al., 2004a). However, meiosis and syngamy are infrequent events in coccolithophore life-cycles and have no significant role in controlling size variation within each phase. Asexual binary fission results in equal division of the cell contents between the daughter cells. In coccolithophores there are no significant vacuoles and the predicted halving of cell volume corresponds reasonably close to observations. Halving of cell volume will only result in a reduction of cell diameter to 0.8 times the predivision diameter (since 3 √0.5 = 0.794). Following mitosis cell size recovers toward the pre-division size. The effect on coccolith size of this rather slight cell-size variation is buffered by the fact that the new cells are not naked but inherit coccoliths from the parent cell, with about half the coccoliths going to each daughter cell. Thus regular cell growth does not have a strong effect on cell size and even less on coccolith size. However, cellular division rate does affect cell size. The critical factor controlling division rate is accumulation of the nutrient elements required for the biosynthesis associated with mitosis and especially the macronutrients nitrate and phosphate. Accumulation of these can occur independently of biovolume. As a result, in cultures mean cell size decreases during exponential growth and increases during the stationary phase (Fig. 12), which is normally nutrient limited. Therefore, within species, small cell size in coccolithophores is an indicator of optimal growth. Large cell sizes are also associated in culture with low phosphate conditions. Culture experiments have also shown that temperature, salinity, and light levels can all affect coccolith and cell size (e.g. Watabe and Wilbur, 1966; Paasche et al., 1996; Quinn et al., 2003) but the effects are not particularly strong or consistent. Whilst phenotypic size variation produces moderate size variation, rather larger variation can be produced by genotypic variation within conventionally recognised species. As with phenotypic variation, the key data on this has come from study of cultures, since field data is inevitably ambiguous. Young and Westbroek (1991) showed that E. huxleyi could be divided into at least three types (termed type-A, type-B and Type-C) characterised by different coccolith morphologies and sizes. Culture experiments showed that coccolith type remained constant within unialgal cultures even under varying temperature, light or nutrient conditions. From this they inferred that coccolith type was under genotypic control, this was tested by serotaxonomic work. Antibodies produced against coccolith associated poly-

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Fig. 12. Data from a batch-culture laboratory experiment on E. huxleyi type A (strain L), grown at 25 °C, 3000 lux, f/50 culture medium (see Young and Westbroek, 1991 for details). After inoculation the culture shows exponential growth for 6 days to a cell concentration of ca. 500 million cells/litre (top plot), followed by an extended stationery phase during which the cells are viable but are not dividing. Cell size decreases significantly during exponential growth then increases during early stationary phase (middle plot — NB this is cell diameter, measured by light microscopy, not coccosphere diameter). Coccolith size shows a similar trend but with lower amplitude (lower plot; mean and standard deviation shown, based on 60 measurements per sample).

saccharide were used as an independent test of strain classification and produced results which paralleled the classification based on coccolith type (van Bleijswijk et al., 1991; Young and Westbroek, 1991). Field-sample based studies of other coccolithophores, notably Gephyrocapsa (Bollmann, 1997) and Calcidiscus (Kleijne, 1993; Knappertsbusch et al., 1997; Renaud and Klaas, 2001), produced several examples of apparently similar variation, but in most cases the authors were unable to conclude whether this was result of phenotypic plasticity or genotypic variation. In the CODENET project (Thierstein and Young, 2004) this phenomenon was systematically studied in six key taxa through a combination of, physiological experiments using laboratory cultures, field-sample studies, and molecular genetics (Geisen et al., 2002; Saez et al., 2003; Geisen et al., 2004; Quinn et al., 2004). In addition for several taxa the identification of alternate life-cycle phases provided a new source of

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morphological data complimentary to that from the better known life-cycle phase (Geisen et al., 2002, 2004). The results of this work were surprisingly consistent, in each case the dominant control on morphotypic variation, including size variation, was shown to be genotypic variation. Each taxon consists of a few morphotypes which apparently correspond to discrete species with divergence times ranging from a few hundred thousand years to a few million years. Within each morphotype/species the range of size variation observed is rather slight. One essential conclusion of this is that major shifts in coccolith size, as recorded in the fossil record of taxa such as Reticulofenestra (Young, 1990) or Calcidiscus (Knappertsbusch, 2000) must be the product of evolutionary change and are likely to have occurred through selection of closely related species/sub-species rather than by anagenetic change within a single lineage. It is less clear whether size variation between morphotypes/closely-related species is in any way consistently related to ecological adaptation of the species. In Coccolithus of the two recently separated species the smaller species, C. pelagicus (sensu stricto), is restricted to sub-arctic waters and temperatures below 10 °C whilst the larger species C. braarudii occurs in temperate upwelling zones at temperatures of about 12 to 18 °C (Saez et al., 2003; Geisen et al., 2004). Gephyrocapsa arguably shows a similar pattern with G. muellerae typically replacing the larger species G. oceanica at higher latitudes/cooler water. However, the still smaller species G. ericsonii does not fit this pattern and can cooccur with either of the larger species. In Calcidiscus productivity seems to be the main control with the smaller species C. leptoporus (sensu stricto) being replaced by the larger species C. quadriperforatus (Fig. 13) in higher productivity environments (Renaud et al., 2002). Again there is a smaller morphotype — small “C. leptoporus”. Its distribution is poorly understood (Quinn et al., 2004). In other cases the ecologies of the sibling species/ morphotypes are poorly understood (Geisen et al., 2004). Overall thus although several examples of size-separated sibling species are now well-documented and many others are suspected there is as yet no clear ecological pattern to their distribution. 5.2. Planktic foraminifers Foraminiferal life cycles are significantly different from those of coccolithophorids. Foraminifers undergo sexual reproduction forming minute juveniles which then grow by serial addition of chambers. Final size is determined by the onset of reproduction, during which

Fig. 13. Seasonal size variations of the coccolithophore C. leptoporus off Bermuda (modified after Renaud and Klaas, 2001).

gametes are released and the empty test sinks to the ocean floor. The size of the proloculus, the first chamber has a large influence on the final size because of its influence on the geometry of the shell (Berger, 1969; Wei et al., 1992). In most low-latitude planktic foraminifers, species reproduction is known to be triggered by the synodic lunar cycle (Spindler et al., 1979; Bijma et al., 1990a; Schiebel et al., 1997). A single specimen can grow to different adult sizes, depending on environmentally controlled growth rate (Caron et al., 1981, 1987a; Bijma et al., 1990b). Work on ecological influence on the adult test size of planktic foraminifers was pioneered by Hech (1976) and Bé et al. (1973). Hecht (1976) defined “environmental optima” for temperature and salinities for several species in the North Atlantic (Fig. 14). For example, G. bulloides populations show largest sizes around 50°N whereas the subtropical to tropical G. ruber attain their maximum sizes around 10°N (Hecht, 1976). Polar species will, reach largest size in cold environments (N. pachyderma (s)), whereas tropical species (G. menardii) reach their optimum size in warm waters (Fig. 15). This model appears robust and could be reproduced in all other oceanic basins (Malmgren and Kennett, 1976; Schmidt et al., 2004a). Several physical and chemical properties of the ambient sea water, such as temperature, nutrient availability, carbonate saturation, and oxygen availability have been shown to influence size (e.g. Berger, 1969; Bé and Tolderlund, 1971; Hecht, 1976; Caron et al.,

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Fig. 14. Geographic variation in average body size of the subtropical species G. ruber (dashed lines) and temperature species G. bulloides (solid lines). Modified after Hecht (1976).

1981, 1987a; Bijma et al., 1992; Ortiz et al., 1995; Naidu and Malmgren, 1996; Schiebel et al., 2001; Schmidt et al., 2004a). Some of them, e.g. temperature and carbonate saturation but also temperature and productivity, are globally highly correlated with each other and their specific effects are difficult to disentangle. Temperature-related effects appear to be the most important controls on body size of planktic foraminifers, both on a species level (e.g. Bé et al., 1973; Hecht, 1976) and in the assemblage (Schmidt et al., 2004a). Temperature ranges leading to largest size and highest relative abundance of individual species coincide (Fig. 16, Schmidt et al., 2004a), indicating that largest size is obtained under optimum environmental conditions. This confirms earlier observations by Kennett (1976) and Hecht (1976) that abundance and size maxima of many taxa tend to occur at specific temperatures. The temperature size relationship in foraminiferal species is not a linear one. There are several different patterns discernable depending on the optimum temperature of the species (Fig. 16), a) size decrease with increasing temperature (for polar species), b) an optimum size at a specific temperature, c) size increase with increasing temperature (for subtropical and tropical species) and d) no reaction at all (Fig. 17). Some species have more than one optimum (Fig. 17). This points to different environmental adaptations and potentially to the presence of cryptic species as in G. truncatulinoides and O. universa (de Vargas et al., 1999, 2001; Kucera and Darling, 2002).

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Temperature influences foraminifers directly, since cell physiology is known to accelerate with temperature and approximately doubles when temperature increases by 10 °C (Caron et al., 1987a,b; Bijma et al., 1990b; Spero et al., 1991). The increasing enzymatic activity with rising temperature will lead to faster growth (Spero et al., 1991) and hence larger test size. A large number of oceanic parameters are related to or correlated with temperature. Hence, temperature can also act indirectly on size, e.g. via increased stratification, i.e. a larger vertical temperature gradient, provides more niches and may minimise interspecific competition (Schmidt et al., 2004a). Enhanced calcification, i.e. fast biomineralisation rates, in foraminifer tests could be a direct consequence of higher carbonate supersaturation. Since CO2 is less soluble in warmer waters, calcium carbonate supersaturation increases from the poles to the tropics (Buddemeier and Fautin, 1994), paralleling the observed trend in planktic foraminifera size. In laboratory experiments, the rate of chamber formation increases with increasing food availability (e.g., Bé et al., 1981; Faber et al., 1988), but a negative correlation is observed between survival time and feeding frequency (Bé et al., 1981). This explains the optimum primary productivity of about 150 g C m− 2 y− 1 found globally in surface samples (Schmidt et al., 2004a). At very high primary productivity, the shell size decreases. Symbiont activity influences the growth of their hosts (Fig. 15, Bé et al., 1982). Symbiont-bearing species, such as G. ruber, G. sacculifer, and G. conglobatus, reach larger maximum sizes than asymbiotic species, but the size difference between G. tumida (asymbiotic) and G. menardii (facultative symbiotic) are minor. Furthermore, species reaching largest adult shell size are found amongst both symbiont bearing and asymbiotic species (Schmidt et al., 2004a). Planktic foraminifers are broadly divided based on their habitat depth in surface-dwelling, intermediatedwelling and deep-dwelling species. Interestingly, most of the largest species (G. menardii, G. ruber, G. sacculifer, and G. conglobatus) are surface dwellers, though the large size increases the weight and hence should make it more difficult for the species to keep their buoyancy. Furthermore, globulose and inflated species, such as G. ruber, G. sacculifer, and G. conglobatus, have a lower buoyancy than conical forms (McNown and Malaika, 1950) such as G. tumida and G. truncatulinoides. Despite the different buoyancy, the former species are all surface dwellers whereas the latter are deep dwellers. This interpretation is corroborated by the different habitat depth of G. menardii (intermediate, 25–100 m) versus G. tumida

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Fig. 15. Largest species in polar, temperate and tropical foraminiferal assemblages. All specimens are at the same scale. Map in upper left corner illustrates the geographic extent of individual biogeographic zones (modified after Hemleben et al., 1989 and Bé and Tolderlund, 1971).

(deep, 200 m) despite their very similar shape (Hemleben et al., 1989; Kemle-von Mücke and Oberhänsli, 1999).

Fig. 16. Optimum temperature conditions for species populations determined by their maximum relative abundance (Prell et al., 1999) and their maximum sizes (Schmidt et al., 2004a).

Therefore, the size and weight of foraminifers does not seem to force a specific habitat depth, though changes in shape and increases in size can allow to change the habitat depth and hence open new ecological opportunities (Norris et al., 1993; Wei, 1994). Test sizes of foraminiferal species are smaller in frontal and upwelling areas (Ortiz et al., 1995). These environments are characterised by high turbulence along different water masses, frequently appearing eddies (Beckmann et al., 1987), and storm events (Schiebel et al., 1995), all of which lead to expatriation (Berger, 1970; Weyl, 1978) and vertical displacement of biota. Reduced light attenuation in frontal and upwelling areas caused by high plankton standing stocks, may inhibit growth via lowered symbiotic activity (Bijma et al., 1992; Ortiz et al., 1995). The subtropical and tropical environments apparently allow for growth to larger test sizes by the single or combined effects of factors such as higher temperatures, increased surface water stratification, enhanced calcium carbonate saturation, and high light intensity (Fig. 18) (Schmidt et al., 2004a).

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Fig. 17. Examples for temperature-related size changes in planktic foraminiferal species, from top left to bottom right: N. pachyderma (polar), G. bulloides (temperate), G. menardii (subtropical and tropical), O. universa (temperate and subtropical), G. truncatulinoides (temperate and subtropical type) and G. inflata (no clear optimum environmental adaptation), data from Schmidt et al. (2004a).

Biogeographic size changes in foraminiferal assemblages are influenced by additional factors. The range of body size in an assemblage is a cumulative result of distinct environmental adaptations of individual species. Therefore, species replacement as in upwelling zones, will influence the size range in assemblages (Fig. 19). The absence of many subtropical species in upwelling

Fig. 18. The effects of light on symbiont activity and the consequences for final test size of G. sacculifer (modified after Bé et al., 1982). Both experiments started with the same initial size. The specimens in the top panel have been kept continuously in darkness, whereas the specimens in the lower panel have had full light exposure.

zones leads to a dominance of temperate Globigerina bulloides, a comparably small species (Schmidt et al., 2004a). 5.3. Radiolaria Radiolarian shell morphology is extremely diverse. This not only reflects the relatively high species diversity of the group, but also a fundamentally different type of morphologic variance than is displayed by the other groups of organisms reviewed here. While other plankton groups have cells and skeletons with one basic topological form, or at least a few closely related variants, radiolarian shell forms are much more diverse, with numerous basic geometries: segmented cones, nested spheres, spongy discs, spider-web like networks, tent-like structures and many more. Some forms do grow in size in a sequential way, but in most species the shell growth appears to be relatively determinate — that is, shells grow by building a few primary elements of a fixed-sized framework early in ontogeny and adding, or filling in, other elements in later growth phases. Mature polycystine radiolarian species skeletons range in size by at least an order of magnitude, from

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Fig. 21. Latitudinal variation in outer (cortical) shell diameter (μm) in the radiolarian A. haysi. Data (Bjørklund, 1977) from core-top assemblages in a tropical to southern Atlantic transect; same samples as in Fig. 20.

Fig. 19. Size in A) foraminiferal assemblages (Schmidt et al., 2004a,b) Gephyrocapsa species (Bollmann, 1997) plotted against mean annual sea surface temperature (SST in °C, Levitus et al., 1994). Arrows indicate the areas of minimum size at 2 °C and 17 °C, corresponding to the polar and the subtropical front, respectively. The black line in a) represents the 5-point moving average. Biogeographic zones: polar (filled circles), subpolar (files triangles), temperate (open triangles), subtropical (open circles), tropical (open squares), upwelling zone (filled squares). The symbols in B) represent different morphotypes of Gephyrocapsa.

not found in the fossil record; further, radiolarian colonies, in colonial groups, can even reach dimensions of a meter or more, although the individual cells and their skeletons are generally only around 100 μm or so). This taxonomic variation, together with a high degree of variation in relative abundances of species within assemblages, makes it essential to consider within versus between species sources of variation when examining differences in average skeleton size between assemblages. Information about size variation within living radiolarian species is rather sparse, and mostly qualitative. For example, radiolaria inhabiting cold water tend to develop thicker-walled skeletons, sometimes with additional secondary external ornamentation, than

ca. 40 μm for many small nassellarians, to several hundred μm for large species of spumellarians. (Note — phaeodarian taxa can be much larger, but are generally

Fig. 20. Variation of outer (cortical) shell diameter (μm) within latitudinal populations of the radiolarian A. haysii (Bjørklund, 1977).

Fig. 22. Latitudinal variation in average volume (μm3) of shells in populations of Antarctissa spp. in a transect of south Atlantic core top samples (after Granlund, 1986).

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members of the same species living in warmer waters (Hays, 1965; Kellogg, 1975a, Lazarus, unpubl. obs.), but there is no obvious tendency towards larger (or smaller) shell sizes, beyond the minor effect of wall thickening itself. In general, most described species appear to have a relatively constant shell size, or at least do not show systematic variations with geography or environment. Quantitative studies of shell size variation are very rare, and may reflect variation between species as much as within species. Bjørklund (1977) studied variation in outer shell diameter in the spumellarian Actinomma haysi, and noted a ca. 25% variation in average diameter between tropical and subantarctic populations of this species (Figs. 20, 21 and 22). Granlund (1986) noted a similar range in average shell size (200% variation in total shell volume, or ca. 25% in linear dimension) in samples of Antarctissa spp. taken across a subantarctic– antarctic transect (Fig. 22). However, in both cases the taxonomic unit analysed may not be (or in Antarctissa spp., clearly is not) a single species. A. haysi was defined by Bjørklund (1977) to clarify the conflation of these forms with a closely related but smaller species, A. leptodermum, and noted that A. haysi itself formed two distinct morphologic/geographic populations (tropical and subantarctic). Given recent data on cryptic species in similarly broad-ranging, morphologically simple taxa such as planktic foraminifers (Huber et al., 1997; de Vargas et al., 2001), it is at least possible that the size variation in A. haysi documented by Bjørklund is mostly interspecific in nature. 6. Controls on size changes through time 6.1. Glacial interglacial size changes in planktic foraminifera The Quaternary period is characterised by large environmental variations, related to the glacial–interglacial cycles. These cause changes in ice volume, temperature, seasonality, and upwelling and can be detected in changes in δ18O values of benthic foraminifers in sediment cores (e.g. Shackleton, 1996, see Fig. 23). Related changes in the atmospheric pressure system influence the position and the intensity of the major current systems (Fig. 24) and hence the stability of pelagic ecosystems and their boundaries. All plankton groups are influenced by these environmental parameters (e.g., temperature, primary productivity and stability of frontal systems), species replacement (Schmidt et al., 2003), exchange of morphotypes/genotypes (Lohmann and Malmgren, 1983; Renaud and Schmidt, 2003). Size changes in assemblages are the

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Fig. 23. Marine isotope stages (italic numbers) indicating the glacial interglacial climatic changes during the last 1 Ma (based on Shackleton, 1996).

result of species replacement and/or interspecific size variations (Schmidt et al., 2003). Size changes of Pleistocene plankton have been used to quantify environmental changes. The response of size and morphology to palaeoceanographic changes has been variable, depending on species and location. Several studies have shown that, in the vicinity of frontal systems or in upwelling areas, species size and assemblage size fluctuates in the Quaternary (Bé and Duplessy, 1976; Malmgren and Healy-Williams, 1978; Naidu and Malmgren, 1995; Schmidt et al., 2003), whereas in other environments nearly no change was found (Malmgren and Healy-Williams, 1978; Schmidt et al., 2003). Most of the foraminiferal studies have focuses on surface dwelling species (Fig. 24), such as O. universa (Bé and Duplessy, 1976) and G. bulloides (Malmgren and Kennett, 1978a,b) as their main aim was to use foraminiferal size changes as a proxy for temperature variation. Deeper living species are less likely to be influenced by temperature changes, since the amplitude of glacial/interglacial temperature variation is dampened in their habitat. In addition, because of the smaller amplitude of forcing and presumably response, the signal to noise ratio is expected to be small among deepdwelling planktic foraminifera. O. universa shows significant size reduction in glacials in comparison with interglacials in the Agulhas current (Bé and Duplessy, 1976). The investigated Site (RC17-69) has modern sea surface temperatures of 22.2 °C, which is the optimum growth temperature of O. universa (Fig. 17). During glacials, the colder temperatures at this Site (Bé and Duplessy, 1976) were less optimal for O. universa and therefore, its size decreased. In the absence of large environmental changes, e.g. in the Caribbean, the amplitude of size change in O. universa

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Fig. 24. Late Pleistocene size changes in N. pachyderma (Huber et al., 2000; Kucera and Kennett, 2002), O. universa (Bé and Duplessy, 1976), G. bulloides (Malmgren and Kennett, 1978a,b), and foraminiferal assemblages (Schmidt et al., 2003) during the late Quaternary. Numbers represent the isotope stages, and grey bars indicate glacial stages. The map displays the core locations and the major currents influencing the Sites. Bold arrows indicate major changes in the currents systems. ATL = Atlantic.

is reduced by half (Malmgren and Healy-Williams, 1978). Since the size–temperature relationship in O. universa is not strictly linear, but shows much scatter in the subtropics and tropics (Bé et al., 1973; Schmidt et al., 2004a), regions with a small environmental variability do not produce significant correlations of size with palaeotemperature proxies in this species (Malmgren and Healy-Williams, 1978). Other species show more ambiguous results. G. bulloides has been analysed in two cores near the subtropical front in the Indian Ocean (Malmgren and Kennett, 1978a,b) representing optimal growth environments today. Recent G. bulloides decreases in size from temperate to cold Antarctic waters (Malmgren and Kennett, 1976; Schmidt et al., 2004a) which is reflected by larger sizes in the temperate Site (E49-19) than in the subpolar (E48-22) one. Both cores show similar amplitudes of size change with larger sizes during glacials. The temperatures at E48-22 approached optimum temperatures during glacials and hence size increased (Fig. 24). Interestingly, the same is true for E49-19 despite the fact that the temperatures decreased below the optimum growth temperatures defined by Schmidt et al. (2004a,b,c) and

hence the size should be smaller during glacials. The calibration of environmental optima for G. bulloides (Schmidt et al., 2004a) has a clear bias towards the Atlantic and Pacific Ocean. G. bulloides has several cryptic species (Darling et al., 2003) and hence, the calibration might not be applicable to the Indian Ocean. Malmgren and Kennett (1976) found the largest sizes in the Indian Ocean at temperatures around 6–7 °C which would explain the observed pattern. This problem demands further investigation into potential size differences of cryptic species. Interestingly, the size variations in O. universa in the Agulhas current (>200 μm, ∼ 10 °C based on the calibration in Bé et al. (1973) are significantly larger than the ones of G. bulloides in the frontal systems of the Indian Ocean (60 μm, ∼ 10 °C based on the calibration in Malmgren and Kennett, 1976). This large difference in the amplitude of size changes is difficult to explain by temperature alone, since these ranges are very similar. In addition, both species inhabit the upper surface waters and hence a dampening of the signal due to habitat depth can be excluded. However, bearing in mind that symbiotic activity is increasing growth, and that G. bulloides has no

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symbionts, we speculate that symbionts have an active role in increasing the amplitude of the glacial interglacial size changes in Orbulina universa. Other species, such as Neogloboquadrina pachyderma (s), do not appear to show any size changes related to glacial interglacial cycles but rather a gradual increase in size throughout the late Quaternary (Huber et al., 2000). The changes observed are attributed to an improved adaptation of N. pachyderma (s) to the cold Arctic conditions. This is evident, if one compares the size record from the polar Arctic Ocean (Huber et al., 2000) with a record from the temperate Pacific ocean (Fig. 24, light grey curve). The similarity in the patterns indicates a response to a common forcing mechanism (Kucera and Kennett, 2002). The clear net increase in the mean size by 50 μm during the last 600 kyrs suggests adaptation to the conditions in the high Artic. Size changes in foraminiferal assemblages reflect the combined effect of size changes in species and species replacement. Body size ranges in assemblages are directly correlated to the amplitude of environmental change (Fig. 24). The balance between interspecific size changes and species replacement reflects the geographic setting, especially the temperature variability. The size optima are not equally distributed along the temperature gradient (Fig. 15, Schmidt et al., 2004a). In the subtropics and tropics, a small temperature variation has a large impact of species replacement, since these optima are densely clustered. In the subpolar environment, species optima are less closely clustered and temperature tolerance of species is wider (Schmidt et al., 2004a). Therefore, intraspecific size changes rather than species replacement are more likely to occur in subpolar environments. 6.2. Neogene size changes in marine plankton Climatic changes influenced the morphology of planktic organisms in different ways. As discussed in Section 6.1, on short time scales (100 thousands of years), ecophenotypic size variability and adaptive responses are the most important driving factor. On long time scales (millions of years), however, evolutionary size variations may become important. The main macroevolutionary trends throughout the Cenozoic are a disappearance of large forms in coccolithophorids (Young, unpubl. obs), a weight reduction to a quarter from the Eocene to today in radiolaria (Moore, 1969) and a dramatic size increase in subtropical and tropical foraminifers (Schmidt et al., 2004b,c). The reduction in radiolarian weight, though linear through most of the investigated time interval, slowed down

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around 7 Ma (Moore, 1969). If it had continued at the average reduction rate (0.0047 μg/Ma), radiolarians would have stopped silicifying by now. In contrast, foraminifers started to grow to sizes which are unprecedented in their fossil record (Figs. 25 and 26). To improve our understanding of underlying causes, we focus on the better resolved and analysed part of the record, the Neogene. In the following, we will compare size changes in coccolithophorids, foraminifers and radiolarians during the last 16 Ma. The data we compiled had to match the following criteria: data had to span times of several million years and be measured in actual marine samples, not a compilation from published photographs, e.g. in a stratigraphic atlas. Unfortunately, there is no data on diatoms which would match these criteria. The only available data (Sorhannus, 1998; Sorhannus, 1999) document a divergence of the diatom Rhizosolenia praebergonii and R. sigmoida from R. bergonni and covers only a short time interval. The Neogene size record of the investigated groups shows both abrupt and gradual changes, increases and decreases through time. The patterns are not necessarily synchronous in the different fossil groups, neither within the groups although there are time intervals, where changes can be found in several records. A pronounced size increase is seen in warm-water planktic foraminifer assemblages up to unprecedented values (Fig. 25), whereas in high-latitudes sizes remain rather constant (Schmidt et al., 2004b,c). This size increase is evident in the entire assemblage (Schmidt et al., 2004b), lineages (e.g. Malmgren and Kennett, 1981) and within species (e.g. Malmgren et al., 1996). However, the trend is not unidirectional but shows a brief reversal, which is not synchronous in all foraminifers (Fig. 25). Similar to the assemblages, G. tumida also shows a reversal in the size trend (Malmgren and Kennett, 1981), but it is restricted to the interval from 4.7 to 4.1 Ma. The beginning of the size reduction is associated with a major divergence event in the Globoconella lineage with the newly arising G. pliozea increasing dramatically in size directly after its first appearance (Wei and Kennett, 1988). Therefore, these size trends cannot be interpreted as simple increases in variance but must be guided by other factors which allow the trends to reverse. Little is known about the environmental pressures that cause evolutionary change. The most often used explanation in the literature for size changes are climatic changes. It has been suggested that size increase in planktic foraminifers is caused by an increase in selection pressure due to changes in density (Wei, 1994), altering the pycnoclines, as well as vertical water mass structure (Malmgren et al., 1983), causing an elevation of the

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Fig. 25. Cenozoic changes in test sizes of planktic foraminiferal assemblages in low and high latitudes, high latitude cooling represented by δ18O ratios of benthic foraminifers, and global species richness. Test sizes are given as the 95-percentile. (A) 1-My means for planktic foraminiferal assemblage sizes from tropical and subtropical sites (squares) and from temperate and subpolar sites (triangles). Vertical line is the mean size95/5 of all assemblages. Dark grey (temperate and subpolar) and light grey (tropical and subtropical) shading show ± 1 standard deviations for mean sizes per million year interval. (B) Average weight of radiolaria (Moore, 1969). Note that the scale is inversed. (C) Global deep-sea oxygen isotope record representing Cenozoic polar cooling and ice accumulation (Zachos et al., 2001). (D) Total number of planktic foraminiferal species globally known per 1-My interval (Norris, 1991).

thermocline into the photic zone (G. crassaformis, Arnold, 1983). The best studied example is the Globoconella lineage (Wei, 1994). Wei (1994) suggested that the shift towards more inflated and larger specimens from G. puncticulata to G. inflata allowed the latter species to adapt to a larger depth. The depth migration became possible as surface water stratification increased, creating new ecological niches. The same size increase reflecting an adaptive response to increased stratification is well discernible in the assemblage size data (Schmidt et al., 2004c). The increase in stratification is the result of major cooling in high latitudes reducing the bottom water temperatures and increasing the vertical temperature gradient. The additional increase in the vigour of circulation further adds to the increased stratification in the tropics. Hence, though the cooling is a high latitude phenomenon, tropical ecosystems are strongly influenced by these changes. Other major changes in the turnover of the oceans and the vertical water structure are associated with the Late Miocene carbonate shift and the Late Miocene carbonate crash (Bender and Keigwin, 1979; Lyle et al., 1995). The Late Miocene carbonate crash coincides with global cooling, northward expansion of Antarctic waters and increase in polar glaciation, causing changes in the upper

water column. Parallel to the cooling, vertical temperature gradients in the surface water increased. Malmgren et al. (1996) concluded that the morphological change in the intermediate-dwelling Sphaeroidinella dehiscens may be a response to changing surface water properties reflecting an attempt by the species to remain in the same niche. The size decrease from 5.5 to 4.1 Ma starts at the end of the Late Miocene glaciations and the beginning of the Pliocene climate optimum (Hodell et al., 2001). The size reduction stops parallel to the closure of the Panama Isthmus and the related reorganisation of the tropical surface waters (Haug and Tiedemann, 1998). Hence, in multiple cases, changes in stratification seem to influence size of planktic foraminifers on evolutionary time-scales. In contrast to the size increase in foraminifers, coccolith sizes decreased, as shown by C. leptoporus and reticulofenestrids (Fig. 26). Within the last 10 million years, the size decrease in C. leptoporus (Knappertsbusch et al., 1997) is linearly correlated with the size increase in foraminiferal assemblages (Schmidt et al., 2004b) (r2 = 0.491, p < 0.001). The interpretation of this correlation suffers from the fact that these samples are not derived from the same cores, the biogeography is not the same and most of all, the biology is significantly

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Fig. 26. Size change during the Neogene for the coccolithophorids C. leptoporus (Knappertsbusch, 2000) and reticulofenestrids (Young, 1990), foraminiferal assemblages (Schmidt et al., 2004b) and lineages: Globoconella conoidea – G. inflata lineage (Malmgren and Kennett, 1981), the Globoconella clade (stars = Globoconella puncticulata; black squares main stock = G. conomiozea, G. sphericomiozea; grey circles = G. pliozea) (Wei and Kennett, 1988); Sphaeroidinellopsis – Sphaeroidinella lineage (black square = Site 502, open circles = Site 503A) (Malmgren et al., 1996); Globorotalia tumida lineage (Malmgren et al., 1983) age model modified after MacLeod (1991); radiolarian lineages and species: the Pterocanium clade (back squares = P. praetextum; open circles = P. charybdeum, open stars = P. prismatum) (Lazarus et al., 1985), P. vema (Kellogg, 1975b), Cycladophora davisiana (Motoyama, 1997) and E. matuyamai and E. cavertense (Kellogg and Hays, 1975).

different. The question arises if there is a causal relationship or if this is a simple coincidence, we will discuss this subsequently. If change in carbonate saturation is a cause for size changes, the question arrives why coccoliths decrease in size while foraminifers increase. The ocean is supersaturated in respect to carbonate, so foraminifers and coccolithophorids are not competing for the resource. Foraminifers (protozoa) and coccolithophorids (phytoplankton) have very different life strategies. An increase in stratification prevents deep vertical mixing. This vertical mixing brings nutrients to the surface and promotes growth to large size in certain coccolithophorid species (Renaud and Klaas, 2001). Hence increased stratification could promote increases in foraminiferal size and restrict coccolith growth. Amongst coccolithophores, the groups which dominate the fossil record are non-motile placolith-bearing species which are dependant on turbulent mixing to maintain their position in the water column. Thought the increased equator to pole temperature difference (Schmidt et al., 2004c and references therein) increased the heat transport and hence atmospheric circulation (Rea, 1994), this increase in surface water turbulence was counteracted by the increase temperature difference in the upper water column leading to increased stratification, the strengthening of

pycnoclines and hence reduced nutrient mixing (Schmidt et al., 2004c; Finkel et al., 2005). Finkel et al. (2005) make this increase in stratification responsible and the consequent reduction in nutrient mixing responsible for a dramatic size decrease in diatoms which, like coccolithophores, depend on the nutrient availability in the upper water column. Therefore, it is reasonable to predict increased stratification would lead to size reduction, as observed. The coccolithophore size reduction is absolutely unambiguous and most pronounced in the late Neogene which is also the time interval with the largest change in stratification as indicated by oxygen isotope differentials between shallow and deep living planktic foraminifers (Chaisson and Ravelo, 1997; Chaisson and Ravelo, 2000; Schmidt et al., 2004c). Radiolarians show very diverse patterns of increase, decrease and stability (Fig. 26). Pterocanium praetextum and P. charybdeum show a slight gradual decrease during the last 4.2 respectively 5.9 Ma, whereas P. prismatum increases in size directly after the splitting event (Lazarus et al., 1985). Increase in size around the same time are documented for Pseudocubus vema (Kellogg, 1975b) and in Cycladophora sakai (Motoyama, 1997). From 3 million years onward, the C. sakai- davisiana lineage and P. prismatum decrease

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in size, parallel to Eucyrtidium calvertense (Kellogg and Hays, 1975). E. matuyamai, in contrast, increases in size until its extinction at 1 Ma and also P. vema continuously increases in size. The size decrease can be observed for cosmopolitan species (Motoyama, 1997) or like P. prismatum and P. charybdeum for tropical/subtropical species (Lazarus et al., 1985). Interestingly, the C. sakai-davisiana size decrease is related to cooling (Motoyama, 1997), whereas in foraminifers size increase is related to cooling. In summary, the radiolarian data show no noticeable general trend in size change. The few lineages studied often show complementary patterns of increase and decrease in size associated with cladogenesis, but no obvious overprint of net change in size among the taxa studied. It should be emphasised however that the number of lineages studied so far is far too few, when compared with the high diversity of radiolarians, to allow any general conclusions to be drawn about size variation in radiolarians. The trend towards lower shell weights documented by Moore (1969) is an important feature of the Cenozoic microfossil record, and may indeed be related to a decrease in Cenozoic oceanic dissolved silica concentration caused by the expansion of diatoms, as hypothesised by Harper and Knoll (1975). However, without additional data, it cannot be determined how this pattern was produced. Change in average size of

species, in relative abundance of different sized taxa, and decreases in the average shell weight of species without decrease in size (due to thinner shell walls etc.) are all possible factors that could have produced the observed weight trend. Radiolarians also have a significantly different ecologic distribution than the other groups considered here, being more common at deeper water depths and in regions of higher productivity than is true of planktic foraminifera and coccolithophores. Changes in water stratification and nutrient availability (other than silica) may have driven size changes in several plankton groups, but radiolarians might be expected for this reason alone to show at least a partially different pattern of change than for the carbonate shelled microfossil groups. This in particular is true of changes due to changing latitudinal provinciality over the Cenozoic. As polar regions cooled, carbonate microfossil abundance and diversity declined dramatically. Radiolarians by contrast, at least at first radiated into distinct high latitude faunas, although as polar environments became more extreme, diversity declined in the late Neogene (Lazarus, 2002). The radiolarian response thus consists, to a much greater degree than for carbonate microfossils, of distinct regional signals, which will need to be separately examined to understand the overall pattern of change in radiolarian shell size.

Fig. 27. Compilation of climate, tectonic and biotic events during the last 16 million years. Climatic events are indicated by oxygen and carbon isotopes (Zachos et al., 2001). Oxygen isotopes are influenced by changes in ice volume, temperature and the isotopic values of ocean water. Carbon isotopes are influenced by weathering of rocks and production of organic carbon.

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Size changes may be related to multiple independent environmental parameters and not to one variable, such as stratification or density, i.e. the evolution of pycnoclines. The latter stand as measurable parameters which themselves affect a large number of other facts, e.g. food webs, light intensity, gamete distribution, or changing patterns of niche richness. The different environmental prerequisites of species, lineages and whole plankton groups will lead to important differences in their size evolution though time. 7. Plankton size and marine biogeochemical cycles Biologically mediated fluxes of elements between the upper and deep ocean depend on calcification and silicification of microfossils and lead, over geological time, to a massive accumulation of calcite, opal and organic matter in oceanic sediments. Changes in the size of microfossils can influence the amount of material exported to the deep ocean. Size changes reflect amongst other factors changes in growth rates, reproduction, and the genetic makeup of an organism. It has been suggested (Riebesell et al., 2000), that anthropogenic climate change will significantly reduce calcification of coccolithophorids. Will photosynthetic carbon fixation be compensated by more successful diatoms, will foraminifers balance the calcification loss? Unfortunately, interpretations of causes for these size changes are limited by a lack of studies combining several microfossil groups to understand ecosystem wide interactions of size changes. Hence, the effects of climate change on size of main producers of carbonate and silica in the ocean remain unknown (Fig. 27). Nevertheless, it is clear that ecological and evolutionary processes influence the body size of marine plankton at different time scales and the consequence of these changes for accumulation of carbonate and silicate are not trivial. Models of global elemental fluxes and cycles must consider the effects of changes in body size of marine plankton and the parametrisation of body size response to external forcing remains an important question for micropalaeontologists. Acknowledgements This research used samples and/or data provided by the Deep Sea and Ocean Drilling Program (DSDP/ ODP). We thank Kjell Bjørklund, Mike Cottam and S. Renaud for the use of their illustrations. This research has been supported by the German Research Foundation (DFG SCHM 1668/1-1/2) and NERC (NE/ B500874/1).

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