depth coenoclines and environmental ... - GeoScienceWorld

Journal of Foraminiferal Research, v. 34, no. 1, p. 9–33, January 2004

DEPTH COENOCLINES AND ENVIRONMENTAL CONSIDERATIONS OF WESTERN PACIFIC LARGER FORAMINIFERA JOHANN HOHENEGGER1 ¨ sterreich (Austria) Institut fu¨r Palaöntologie, Universita¨t Wien, Althanstrasse 14, 1090 Wien, O

quence of overlapping intervals along the gradient is called a coenocline (Whittaker, 1960, 1967) because the community composition (5 biocoenosis) changes continuously along the environmental gradient. Relations between coenoclines and environmental gradients allow determination of gradient values based on species composition when factor measures are missing. Such determinations are possible using linear or nonlinear transfer-functions (for discussion see Birks, 1995). Water depth is an important factor for sediment deposition in marine environments. Discontinuities in sedimentation, often represented at shallow continental margins, can only be detected using the depth dependence of fossil organisms (Brett, 1995). Symbiont-bearing benthic foraminifera are extremely useful for depth determination in shallow water because they are restricted to the photic zone. The constancy of environments under oligotrophic conditions induces partitioning of the photic zone into numerous habitats of organisms, e.g., larger foraminifers (Hallock 1987), leading to coenoclines corresponding to depth. Until 1984 depth dependence has been documented for different groups of larger foraminifera from the Caribbean (Rose and Lidz, 1977), Red Sea (Hottinger, 1977a, 1980b; Reiss, 1977; Hansen and Buchardt, 1977), Indian Ocean (Hottinger, 1980b) to the Pacific (Hallock, 1979, 1984), when Leutenegger (1984) summarized these results by demonstrating relationships between larger foraminifera, endosymbionts, and water depth. These data were used by Hottinger (1983a) to explain the distributions of larger foraminifera in space and time, providing a tool for the interpretation of ancient shallow marine environments. Hallock and Glenn (1986) exercised a similar approach for analysing Cenozoic carbonate facies. In addition to light and water energy as the main factors influencing the depth distribution of larger foraminifera, the importance of trophic resources, which is reflected in test size and form, was demonstrated by Hallock (1985, 1987). Hottinger (1997) showed the important depth signals contained in the functional morphology of larger foraminifers. Based on quantitative depth distributions of larger foraminifera in the NW-Pacific, Hohenegger (1995) developed transfer equations for estimating water depth. Further quantitative investigations yielded a description of the depth coenocline of larger foraminifera in clear ocean water in front of NW Pacific coral reefs, which is characterized by high diversity (Hohenegger, 2000). Inferences from depth distributions of living larger foraminifers to fossil species for estimating paleodepth in Cenozoic environments are required in many fields of the earth sciences, including sequence stratigraphy, paleoceanography, and oil exploration. Since paleodepth estimation without the consideration of additional factors as climate, water transparency, and hydrodynamic conditions is possible only on the base of stable coenoclines, the stability of the depth

ABSTRACT

Symbiont-bearing benthic foraminifera are restricted to the euphotic zone of tropical and warm-temperate seas. Species distribution is correlated with depth, and the continuous alteration of community structures represents a coenocline. Since depth is a composite environmental gradient, the coenocline of larger foraminifera is not stable but alters with changes in primary limiting factors: temperature, light, water movement, substrate, and nutrients. Temperature determines geographic distribution and affects the depth distribution of larger foraminifera by the development of a shallow thermocline that truncates the distribution of shallower species and excludes species adapted to the deepest euphotic zone. Within these constraints, light is the most important primary factor because larger foraminifera are at least partly dependent upon photosynthesis by their algal endosymbionts for growth and calcification. The microalgae show distinct intervals along the light gradient and the foraminiferal host develops various strategies for regulating light intensity. First, well-structured environments in shallow waters allow shelter against irradiation by protecting in shadow areas. Second, wall and test structures enable regulation of light penetration. A range of mechanisms allows species to resist the highest energies in the breaker zone of the reef edge and crest, where foraminifera attach to inorganic or organic hard substrates. Concentrations of dissolved and particulate organic matter in the water column, as well as sediments or other inorganic particles, influence depth distributions by changing water transparency and, therefore, photosynthesis. Permanent or episodic elevations of concentrations therefore compress the coenocline upward. Species adapted to hard substrates must compete for the reduced space, while species living in the deepest euphotic zone are at a disadvantage because they are insufficiently motile to surmount large depth differences. Changing light transparencies due to nutrient input and different hydrodynamic conditions alter relations between the light coenocline and water depth. Thus, paleodepth interpretations based on larger foraminiferal assemblages should be based not only on foraminiferal taxa and ecology, but also on environmental evidence for climate, terrigeneous influence, water transparency, and hydrodynamic conditions based on sedimentology, geochemistry, and associated fossil biota. INTRODUCTION Species react to an environmental gradient along intervals that represent boundaries of the realized niche. The se1

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HOHENEGGER

FIGURE l.

Distribution skewness caused by nonlinear response of species abundance to an environmental gradient.

coenocline of symbiont-bearing benthic foraminifera has to be verified. FUNDAMENTAL AND REALIZED COENOCLINES A fundamental coenocline is understood as a sequence of species distinguished by their fundamental ecological niches along the environmental gradient. According to Hutchinson (1965), the fundamental niche is determined as the species’ niche in the absence of any interspecific competition, thus representing its physiological capability (Roughgarden, 1974). The range represents the niche width of a species along an environmental gradient. Frequencies of species characterizing the fundamental niche are log-normally distributed (Hohenegger, 2000) and often truncated. They can be fitted by the function

f(x) 5 d exp 2(xc 2 m)2/2s2

(1)

In this equation, x is the metric environmental gradient, d the optimum, m the mean, and s2 the variance of the distribution. The power factor c describes intensities of left- (c . 1) or right-side (c , 1) skewness (c 5 1 in a normal distribution). Truncated distributions are caused either by a stepwise or catastrophic response to the gradient (Poston and Stewart, 1981) or by natural limits (e.g., water surface, thermocline).

FIGURE 2.

Various factors lead to skewed distributions. Species can be restricted at the niche boundaries, being unable to respond in a rectilinear manner to an independent environmental gradient (Fig. 1). In a composite environmental gradient like water depth, different relations between primary factors and the composite gradient can also produce skewed distributions. For example, symbiont-bearing larger foraminifera attaining the niche optimum at the fair weather wave base that cannot resist extreme hydrodynamics near the surface are distinguished by deep-skewed distributions (Hohenegger, 2000). Competition on food and space also cause deviations from normal distributions. Thus, ’realized niches’ (Hutchinson, 1965) are distinguished by left- and right-side skewness, when the competitors’ distributions overlap at the lower or upper distribution limit, or by leptokurtosis, when competitors narrow the fundamental niche at both sides in equivalent intensities (Fig. 2). Competition at both sides with different intensities produces skewed leptokurtic distributions. Competitors occupying similar niche ranges, but possessing narrower widths, affect multimodality or platykurtosis, depending on the intensity and location of competition (Fig. 2). The first step in estimating fundamental niches is the fitting of empirical frequencies by normal distributions. In the case of skewed empirical distributions, only the longer

Deviations from the normal distribution along the gradient caused by competition.

COENOCLINES WESTERN PACIFIC LARGER FORAMINIFERA

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branch of the distribution should be used to determine niche width. This reduces the effects of compression through strong factors acting at the range limits, or through competition as explained above. In the case of multimodality or platykurtosis, frequencies should be decomposed into several normal distributions (Medgyessy, 1977). After calculating normal distributions of a species using geographically and temporally distinct transects, the general frequency distribution can be calculated in two ways. Proportions of the local and temporal distributions are incorporated in the weighted form of generalization, while in the unweighted form only the location and dispersion parameters are averaged. The mean (m) and variance (s2) of the composite transect can be obtained in weighted form by

Opm 5 O p s 1 O p (m 2 m)

m5 s2

i5k

i51

i

i

i

2 i

i5k

i51

(2)

i5k

i51

i

i

2

(3)

where i designates the local and temporal transect, k is the number and p the proportion of the transect. In unweighted form, the general mean and variance are

Om 1 1 5 O s 1 O (m 2 m) . k k

m5 s2

1 k

i5k

i51

i

i5k

i51

(4)

i5k

2 i

i51

i

2

(5)

The unweighted form of generalization gives importance to distributions with low abundance. In the case of strongly overlapping competition, frequencies can be extremely low at the niche optimum due to suppression, while they are higher at the niche boundaries where the influence of the competitor vanishes. Especially in the case of different normalization methods to obtain unit quadrats (Krebs, 1989), this form of generalization is the appropriate method due to its independence from frequencies. High abundance in the weighted form, on the contrary, indicates optimal conditions for species with few restrictions due to competitors, thus better representing niche limits than distributions with low frequencies. THE DEPTH COENOCLINE The procedures for obtaining fundamental niches as basic elements of the depth coenocline are demonstrated using five transects in the Central Ryukyus, NW Pacific. They represent temporally and locally distinct transects, although the investigated area is geographically restricted. Two transects investigated in 1992 and 1993 are located NW of Sesoko Island, Okinawa (Hohenegger, 1994), but differ in substrates. Whereas the first transect is characterized in shallow parts by hard substrates with coral boulders and macroids (Hottinger, 1983b), the second transect shows a higher proportion of sand. In 1996, a detailed study was performed on the coenoclines of living individuals and empty tests (Yordanova and Hohenegger, 2002) as well as the sedimentology using two transects in the same area (Fig. 3). The first transect in the northern part corresponds to the area investigated in 1992/93; thus, it characterizes temporal differences to

FIGURE 3. Proportion of substrate types at two transects NW off Sesoko Island.

both earlier transects. The second transect of 1996 parallels the first, but 500m to the south. Species composition, abundance, and the resulting coenocline are quite different from the northern transect (Hohenegger, 2000). In 1997 and 1998 a third transect off northern Minna Island (location in Hohenegger et al., 1999) was investigated, which is characterized by a dominance of sandy substrates. Therefore, the coenocline again differs from both other transects. Fundamental niches of the Pacific larger foraminifera along the depth gradient were estimated in the ‘Kuroshio Current Province’ (Longhurst, 1998) using the geographically restricted five transects mentioned above. Nevertheless, depth distributions of living larger foraminifera from Belau (Hallock, 1984; Hohenegger, 1996) belonging to the ‘Western Pacific Warm Pool Province’ (Longhurst, 1998) completely fit the results from the Ryukyus. This strengthens the hypothesis of recognizing fundamental niches by the procedures explained above. Since the frequencies at the sampling stations were standardized using different quadrats in 1992/93 (100 cm2 substrate surface) and 1996 (500g sediment), the unweighted form of generalization was calculated to obtain normally distributed frequencies (Fig. 4). All optima of the generalized distributions were normalized to a standard height because abundance differences between species are unimportant for fundamental niches. The genus Peneroplis, attaining its optimum at the surface (P. cf. P. antillarum, P. planatus, P. pertusus), occupies wider niches compared with the genus Dendritina, which lives slightly deeper, avoiding the surface regions.

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FIGURE 4.

Fundamental depth distributions of NW-Pacific symbiont-bearing benthic foraminifera in clear ocean water.

Alveolinella quoyi and the soritids Sorites orbiculus and Amphisorus hemprichii show similar distributions, while Parasorites orbitolitoides has a niche optimum at 235m and does not live at the surface. The niche optima of the Amphisteginidae differ strongly. Similar wide ranges can be found in A. lessonii, A. bicirculata, and A. radiata, but a narrow niche combined with a truncated distribution and the optimum at the surface characterizes the shallow-living A. lobifera. The deep-dwelling A. papillosa shows the broadest niche width of all larger foraminifera, with an optimum at 295m. Except in Calcarina hispida, C. mayori, and Baculogypsinoides spinosus, narrow niches distinguish the calcarinids. Niche widths of species attaining their optimum in shallowest regions (reef flat in Neorotalia calcar, Baculogypsina sphaerulata, Calcarina gaudichaudii, C. defrancii) are extremely narrow. Within the Nummulitidae, only Operculina ammonoides and Heterostegina depressa have

wide niches comparable to the Amphisteginidae, while the ranges of all other species are moderate. The differing positions of their niche optima underline the importance of nummulitids for depth determination especially for the deeper euphotic zone (Hohenegger et al., 2000). Since water depth is a typical composite environmental gradient, the question arises as to the stability of the coenocline. Investigating the influence of each primary factor on the depth coenocline may answer this question. TEMPERATURE Temperature is the main factor limiting the geographic (5 latitudinal; e.g., Langer and Hottinger, 2000) distribution of symbiont-bearing benthic foraminifera. The physiological effects of extreme high or low temperatures for the larger benthic foraminifera have not been investigated. Three fac-


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FIGURE 5. A. Temperature related to depth in (sub)tropical (Amami O-Shima) and warm-temperate (Tanegashima) water. B. Seasonal changes of temperature in the upper 50 m of (sub)tropical waters W off Sesoko Jima (data from Sakai et al. 1984, 1986).

tors either independently or combined seems to be responsible for this temperature dependence. First, temperature influences stratification of surface waters and, therefore, both dissolved inorganic and particulate organic resources (Nybakken, 1997) available to the foraminiferal host and their algal symbionts. Metabolic rates in ectotherms (including foraminifera) are directly influenced by temperature, so less food is needed in cooler waters, yet trophic resources are typically higher (Hallock et al. 1991). According to the hostsymbiont model of Hallock (2000), the excess dissolved inorganic nitrogen that cannot be controlled by the host may cause the symbiosis to break down because the algae retain their photosynthates for growth. Second, temperature controls the solubility of carbon dioxide. Low temperatures reduce the availability of bicarbonate and carbonate anions in the seawater that are necessary for the production of calcium-carbonate tests. On the other hand, carbon dioxide concentrations are low in warm seawater, hindering photosynthesis. Therefore, calcification is thought to promote photosynthesis in warm oligotrophic seas (McConnaughey and Whelan, 1997). Carbon dioxide is obtained either by the continuous production of calcium carbonate skeletons/tests, resulting in gigantic forms of long-living hosts (scleractinian corals, giant clams, larger foraminifera), by continuous production of calcareous skeletal elements (coccolithophorids), or by short-lived plankton with calcareous tests (planktic foraminifera; Hohenegger, 1999). Third, microalgae show different niches along the temperature gradient. Nothing is known about niche widths of the symbionts in larger foraminifera, but their lower limit might be an important factor for the temperature dependence of the hosts (Hollaus and Hottinger, 1997). Little is known about temperature-related niche widths of larger foraminifera, either in nature or in experiments. The

lower boundaries, however, were estimated from the geographical distribution limits based on surface temperatures (Langer and Hottinger, 2000). This is correct for shallowliving foraminifera, but not for the deep-dwelling species Planoperculina heterosteginoides, Planostegina operculinoides, Nummulites venosus, Baculogypsinoides spinosus, Amphistegina bicirculata and A. papillosa (Langer and Hottinger, 2000) because no investigations about their northern and southern distribution boundaries have been conducted, nor have the necessary temperature measurements been made. Analogous to scleractinian hermatypic corals, persistent temperatures below 148 C (winter months) seem to hinder the survival of larger foraminifera. They are thus restricted to the marine tropical zone. The exceptions are A. lessonii, A. lobifera, O. ammonoides, H. depressa, peneroplids, and soritids, which can also survive in the shallow warm temperate zone (Hohenegger et al., 2000; Langer and Hottinger, 2000). In the investigated area, temperature decreases gradually with water depth, as is typical for latitudes between 158 and 308 due to Ekman convergence and downwelling (Peixoto and Oort, 1992). Temperature was measured at several depths NW of Amami-O Island (288 31.29 N) in the summer of 1999. These measurements show a weak decrease from 28.58 at the surface to 268 at 2140m, which is the depth limit of larger foraminifera (Fig. 5A). At this depth, temperature is close to the supposed niche optimum of 288 C and far away from the averaged lower niche limit at 148C. Similar depth-related temperatures (Fig. 5A) were recorded at Tanegashima (308 25.89 N), located in the warm temperate zone north of the coral reef distribution boundary. After a strong decrease from 28.38C at the surface to 24.78C at 230m, which marks the lower limit of the warm surface water layer, temperature drop slowly to 198C at 2150m,

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HOHENEGGER

again distinctly above the supposed lower niche limit. This is confirmed by Planostegina operculinoides living at 2100m on the slope of Tanegashima. Summer and winter temperatures do not differ strongly in the study area (Sakai et al., 1984, 1986), remaining relatively high at the February minimum (21.28C at the surface, 19.88C at 250m). Temperature differences between the surface and 250m are strongest in late spring (4.88), remain constant from July until October (28) and decrease to 1.48 in February (Fig. 5B). Since 2420m is the critical depth (temperature: 148C) in the study area and is thus far below the depth limit (2140m) of symbiont-bearing benthic foraminifera, temperature dependence cannot be the source of different depth niches for larger foraminifera. In the warm temperate zone, this factor seems to influence the depth distribution of larger foraminifera during winter by the development of a shallow thermocline (e.g., Hollaus and Hottinger, 1997). This explains the geographical distribution of peneroplids, soritids, shallow amphisteginids and Heterostegina depressa, as well as Operculina ammonoides in the warm temperate zone: all inhabit shallow environments. Deep-dwelling species cannot rapidly move into shallow environments in winter and are therefore absent from the deep sublittoral of the warm temperate zone. Only calcarinids are apparently depth restricted due to temperature: they have narrow niches (Langer and Hottinger, 2000) and are not represented in the shallow warm temperate zone where surface temperatures fall below the critical values during winter. According to their estimated lower niche limit at 218 C, calcarinids could live down to 2180m in the study area if their distribution depended only on temperature (Fig. 5A), but they are apparently restricted to the shallowest regions (Fig. 4). Thus, temperature is an important factor for the geographical distribution in shallow water, but not for depth distribution. LIGHT Photosynthesis of symbiotic microalgae depends on the availability and intensity of light. Irradiance varies with the time of day, season according to latitude, and weather. Beside these externally induced variations, irradiance strongly changes in marine environments with water depth. Following Beer’s Law (Drew, 1983), this correlation is characterized by an exponential decrease depending on the attenuation coefficient. Absorption by water, suspended particles, pico-, nano- and phytoplankton, as well as particulate and dissolved organic matter (e.g., Drew, 1983; Valiela, 1995), restricts photosynthesis to the uppermost water column (euphotic zone). Wavelength is another factor influencing the depth limitation of primary producers. Only a narrow spectrum between 300 and 600 nm penetrates below 210m, whereas blue-green light reaches depths below 2100m in clear ocean water (e.g., Drew, 1983). Endosymbiotic microalgae play an important role for larger benthic foraminifera (e.g., Haynes, 1965; Ross, 1972; Reiss et al., 1977; Hallock, 1979, 1981a,b, 1985; Hottinger, 1980a; Leutenegger, 1984; Ro¨ttger and Institut fu¨r den wissenschaftlichen Film, 1984; Lee and Anderson, 1991; Hottinger, 1997; Lee, 1998; Hohenegger, 1999). Certain physi-

ological factors acting independently or together seem to be important for the establishment of a host-symbiont system in oligotrophic seas (Hallock, 1999). On the one hand, the host benefits from the microalgae that produce photosynthates. Additional feeding provides dissolved inorganic nutrients and organic matter available for host metabolism, using energy (ATP) from carbohydrates produced by the symbionts (i.e., mixotrophy). The microalgae, on the other hand, benefit by obtaining nutrients from the host metabolites, giving an advantage over free-living algae in nutrientdepleted waters (Hallock, 1981b). Moreover, calcification promotes photosynthesis by microalgae in CO2-depleted warm, shallow, and alkaline waters (McConnaughey and Whelan, 1997). These host-symbiont connections explain the depth dependence of larger foraminifera: they must provide their symbionts with enough light to enable net photosynthesis rates. Microalgae depend on light in two ways. First, photosynthesis increases almost linearly with irradiance until a saturation point, where enzymes cannot process light quanta faster (Valiela, 1995). Beyond these saturation points, microalgae react to increasing light intensity by maintaining photosynthesis either constant or showing decreasing rates. Microalgal species differ in optima as well as saturation points. Second, absorption of energy from different wavelengths depends on the nature of pigments. The main symbionts in larger benthic foraminifera in the Indo-Pacific are diatoms and dinoflagellates, both characterized by the extremely small proportion or lack of chlorophyll b, while chlorophyll a and c predominate (Lee et al., 1980; ter Kuile and Erez, 1984). Only Peneroplidae house red algae (Porphyridium; Leutenegger, 1977a, 1984; Lee, 1990), which use phycobilins and carotenoids as chromophores. While the first pigments absorb blue-green, green, yellow, or orange light, the absorption bands of carotenoids overlap with the Q-band of chlorophyll a and c (Falkowski and Raven, 1997). Carotenoids screen UV-radiation from the photosynthetic apparatus (Dohler and Haas, 1995), thus allowing peneroplids to inhabit strongly illuminated areas. Another method for protecting organisms from dangerous UV-radiation is the production of aromatic aminoacids (S-320; Jokiel and York, 1981; Dunlop and Chalker, 1986). Ter Kuile and Erez (1984) did not find S-320 in Amphistegina lobifera, which houses diatoms (Lee et al., 1989). This explains why A. lobifera hide on the reef crest in shadow areas within filamentous macroalgae or below coral boulders. By contrast, the soritids Marginopora kudakajimaensis and Amphisorus hemprichii are exposed to extreme irradiation on the shallowest reef moat (Hohenegger, 1994; Fujita et al., 2000). They possess zooxanthellae similar to those in scleractinian corals (Pawlowski et al., 2001), which hints at the production of amino acids that protect the photosynthetic apparatus of symbionts as well as the DNA of both the symbiont and host. Light dependence of symbiotic microalgae is known for a few diatom species (Lee et al., 1980), clearly differentiating species growing faster at high light regimes (312 mW cm2) from forms preferring low light (maximum 19 mW cm2). The investigated diatoms demonstrate limitations below 0.5% surface PAR (10klx; Lee et al., 1980). The light dependence of symbiotic microalgae directly influences


depth correlations of the host. Most larger foraminifera cannot survive without symbionts (Ro¨ttger, 1976; Ro¨ttger et al., 1980; Lee et al., 1991). Nevertheless, the hosts show broader depth ranges than their symbionts, since they are not restricted to a single species of microalgae (Lee et al., 1989). The foraminifer can change the symbiont species according to depth and season (Lee et al., 1989), and can also house more than one species belonging to a specific microalgal division (in the systematic sense, e.g., Pyrrophyta, Bacillariophyta; Lee et al., 1989; Lee et al., 1997; Pawlowski et al., 2001) or to different groups (e.g., Pyrrophyta and Cyanobacteria in Amphisorus hemprichii; Lee et al., 1997). The foraminiferal hosts regulate light for their symbionts using different strategies, all extending the niche ranges of the host for irradiation despite the restricted ranges of their symbionts (e.g., Leutenegger, 1984). Regulation by wall ultrastructures is the first strategy. There are two modifications of calcite test walls in symbiont-bearing foraminifera. ‘Porcellaneous’ walls with extremely small needles that are randomly distributed in the test walls allow life in seawater under highest light intensities and exposure to UV-irradiation (Haynes, 1965). For symbiont-bearing benthic foraminifera these walls become problematic because the hosts have to provide their microalgae with light. The thinning of walls to a few micrometers by pore-like pits in peneroplids (Hansen and Dalberg, 1979) or by grooves and windows in alveolinids and soritids (Gudmundsson, 1994) allows light penetration, but still reduces incident light to 30% (Marginopora vertebralis; Ko¨hler-Rink and Ku¨hl, 2000). This strong reduction restricts larger foraminifera with porcellaneous tests to the uppermost part of the euphotic zone (Hallock 1988a,b; Hallock and Peebles, 1993). By contrast, rhombohedral crystallites with the optical axes orientated perpendicular to the test surface (hyaline-radial; e.g., Bellemo, 1974a) promotes test transparency, does not weaken light penetration, and allows photosynthesis by symbionts in light-depleted environments. Focusing structures like hyaline papillae, knobs, or pustules apparently increase light for the symbionts (Hottinger, 1997). To prevent inhibiting irradiation near the water surface, a change from perpendicular orientated optical axes to crystallite units with an orientation of 458 to the test surface (Bellemo, 1974a,b) reduces transparency for incident light. Together with a thick organic lining (Hottinger and Leutenegger, 1980) and the development of thick-lenticular, sometimes spherical tests, this wall ultrastructure, termed ‘hyaline-granular,’ allows exposure of the Calcarinidae to extreme irradiation (Leutenegger, 1984) without hiding in shaded areas. The second strategy to increase transparency of walls in light-depleted regions is thinning of the lamella in foraminifera possessing hyaline-radial walls. By contrast to porcellaneous foraminifers, lamellar walls, where the new chamber wall at each growth step covers the test surface, characterize all modern hyaline foraminifera (e.g., Hansen, 1979). Regulating thickness of the lamella therefore influences wall and test thickness (Hallock and Hansen, 1979; Hallock et al., 1986). Although mean test diameter and cell volumes remain constant or change weakly with depth, the regulation of lamella thickness strongly influences the thickness/diameter-ratio of the tests. This ratio becomes low with increasing depth due to the thinning of the lamella (Hallock

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and Hansen, 1979) and is often used for depth estimation, especially in the amphisteginids (Hansen and Buchardt, 1977; Larsen and Drooger, 1977; Hallock and Glenn 1986). The third strategy to get enough light for symbionts in the deeper euphotic zone is to position the microalgae at the peripheral cell regions just below the test wall. Here, light is attenuated only by the test and not by the less transparent protoplasm (Leutenegger, 1984). The larger the test surface is in relation to test volume, the more symbionts can be positioned close to the inner test surface. This test surface/ volume ratio is thus important for symbiont-bearing foraminifera in light-depleted environments of the euphotic zone (Hottinger, 1977a,b; Hallock, 1979; Leutenegger, 1984). In amphisteginid species, light penetration is promoted primarily by thinning of the lamella, without or with only a weak change in test diameter within a species (Larsen and Drooger, 1977). In nummulitids, however, an increase of the surface/volume-ratio becomes the primary mechanism, especially in Operculina and Heterostegina (Ro¨ttger and Hallock, 1982; Pecheux, 1995). Since the cell volume does not significantly change with depth (Pecheux, 1995), increasing surface/volume ratios are obtained by test thinning in combination with increasing diameters. Size increase in Operculina is achieved by a weaker enrollment of the logarithmic spiral that characterizes the test margin; this is coupled with a significant decrease in the thickness/diameter-ratio. The thickness/diameter-ratio (t/d) remains relatively constant in species with low-trochospiral, lenticular to spherical tests (compare Larsen and Drooger, 1977 investigating the reverse D/T-ratios; amphisteginids and calcarinids in Hallock, 1979). Thus, the t/d-ratio is more or less growth independent in both families. Larger foraminifera with planispiral enrollment (Archaias, Peneroplis, Heterostegina, Nummulites; see Hallock, 1979; Hallock and Peebles, 1993) or cyclic tests (Sorites, Marginopora; see Hallock, 1979; Cycloclypeus) show allometry caused by significantly higher growth rates in the test diameter compared to thickness. Therefore, the thickness/diameter-ratio changes with growth. Since the surface/volume-ratio is correlated with thickness and size, depth estimation by means of the t/d-ratio becomes problematic using this group of larger foraminifers. By contrast to the relations between thickness and diameter, the surface/volume-ratio changes during growth even in the case of constant t/d-ratios. This is demonstrated by the relation between test surface and volume comparing different thickness/diameter-ratios under the assumption of isometric growth (Fig. 6A). The profit of surface increase compared to stable volumes is negligible by lowering the t/ d-ratio from 1.0 to 0.5, but becomes efficient below 0.5 (Fig. 6B). Thickness/diameter-ratios , 0.05 show the best surface/volume relations, but such test shapes are not possible due to the restrictions of construction morphology. This explains the division of extremely flat and large cells (t/dratios , 0.1) by additional partitions (septulae), i.e., in the flat hyaline genera Planoperculina, Planostegina, Heterocyclina, and Cycloclypeus. Together with test strengthening, such compartments help to regulate metabolic processes (Hottinger, 1984; Sernetz et al., 1985).

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FIGURE 6. A. Relations between test surface area and volume based on different thickness/diameter (t/d) ratios. B. Dependence of test surface area from the thickness/diameter-ratio based on different volumes.

Specimens with lenticular tests that start with t/d-ratios around 0.5 at the upper slope—such as Amphistegina lessonii (Larsen and Drooger, 1977) and A. radiata—or with ratios of 0.4 in Operculina ammonoides (Pecheux, 1995) or 0.3 in Heterostegina depressa (Ro¨ttger and Hallock, 1982) can successfully react to the exponential decrease in light intensities by reducing the t/d-ratio. This leads to a significant surface increase (Fig. 6B) and widens their distribution ranges along the depth gradient in clear ocean water (attenuation coefficient 0.035). T/d-ratios . 0.5 characterize thick lenticular tests of the genera Neorotalia and Calcarina, as well as the species Amphistegina lobifera. Test flattening by lamellar thinning and a slight size increase does not effect ratios below 0.4, which explains the narrower depth range and restriction of these species to the shallowest zone. Furthermore, the mechanism of test flattening is impossible for spherical species like Baculogypsina sphaerulata and Baculogypsinoides spinosus. While the former species is restricted to shallowest waters, the latter starts at 230m. Due to the impossibility of test flattening, the depth distribution does not correspond to a Gaussian form, but is restricted in the deepest part as explained above (Fig. 1). A similar depth restriction can be found in the nummulitid Operculinella cumingii, which lives in the deeper euphotic zone. Since this lenticular species starts with high t/d-ratios (;0.5) at 250m, where the similarly shaped Heterostegina depressa is characterized by a t/d-ratio of 0.2 (Ro¨ttger and Hallock, 1982), lowering of the t/d-ratio by lamellar thinning is insufficient to raise the surface/volume-ratio. Therefore, lateral chambers parts become very flat in the last whorl, as is also found in Heterostegina depressa (Hohenegger et al., 2000). Nevertheless, due to the pronounced thickness of O. cumingii, this species also becomes restricted at light-depleted depths. The deepest-living lenticular species, Amphistegina papillosa, starting with very flat tests in the middle part of the photic zone (t/d 5 0.3 at 50m; Larsen and Drooger, 1977) is restricted below 100m due to constructional limitations; it cannot attain t/d values , 0.05 that would be necessary at the base of the photic zone.

Deviations from normal distributions in deeper waters can be measured by comparing empirical (x) with theoretical depths (j) using the empirical frequency f(x) at depth x and the distribution parameters of the theoretical normal distribution. The theoretical depth j is calculated by the equation j5

2m 6 Ï4m 2 2 4[m 2 2 2s 2 (ln d 2 ln f (x)] 2

(6)

where d is the optimum, m the mean and s the standard deviation of the theoretical normal distribution. In the case of congruence between empirical and theoretical distributions, residuals (x 2 j) along the depth gradient must be normally distributed around 0. Additionally, there should be no significant regression between residuals and the gradient, as is demonstrated by Nummulites venosus (Fig. 7A). Restrictions in the three species A. papillosa, B. spinosus, and O. cumingii are characterized by left-side skewness in the frequency distribution of residuals (x 2 j), and by significant curvilinear regressions between residuals and depth (Fig. 7A). They can be fitted by second order polynomial regressions

y 5 b0 1 b1x 1 b2x2,

(7)

where only the deep-side branch of the parabola is developed (Fig. 7A). The different intensities of depth restrictions for the three species mentioned above that are caused by test form can now be demonstrated by these regression functions. While restriction starts in the spherical B. spinosus at 243m, both species with lenticular tests are characterized by a 10m deeper start. Restriction intensities are expressed in the multiplicative constant (2b2) of the first derivative

y9 5 b1 1 2b2x

(8)

It is strongest (20.033) in the spherical B. spinosus, weaker (20.029) in the thick-lenticular O. cumingii, and weakest (20.017) in the thin-lenticular A. papillosa. The depth-restricted frequency distributions (Fig. 7B) of the three species are now characterized by equations


17

FIGURE 7. Restriction of depth distributions towards light depleted environments of four species with spherical to thin-lenticular tests. A. Residuals between empirical and normal depth distributions in meters, fitted in the deeper part by second order polynomial regressions. B. Depth restricted distributions of three deep-dwelling species possessing lenticular tests.

5

f (x) 5 d exp 2

[

f (x) 5 d exp 2

6

[x 2 (b0 1 b1 x 1 b2 x 2 ) 2 m] 2 2s 2

(x 2 m) 2 2s 2

]

x.2

b1 2b2

x,2

b1 . 2b2

and

(9) (10)

Depth distributions of species using the fundamental coenocline (Fig. 4) and including restrictions caused by test morphology (Fig. 7B) primarily reflect the dependence on irradiation in clear ocean water. Measurements of light extinction in the study area during summer 1996 yielded attenuation coefficients between 0.04 (clear ocean water) and 0.06 (Hohenegger et al., 1999, 2000). The slightly higher attenuation is caused by turbidity in regions exposed to the predominant southern summer winds (Sakai et al., 1984; Hohenegger et al., 1999; Fig. 8). Regarding seasonal changes here, attenuation becomes stronger in late spring due to a weak phytoplankton bloom and the terrestrial input during the rainy season, but never exceeds values of 0.07 (Sakai et al., 1984, 1986). Therefore, transparency remains rather constant over the year (mean value 0.056 6 0.009 amplitude), which is typical for oligotrophic seas (see also Hallock 1987). Attenuated transparencies are caused by colored dissolved organic matter and suspended particles, whether inorganic or organic, originating from terrestrial runoffs and upwelling (Hallock, 1987). In the subtropics, both factors strongly correlate with season (Valentine, 1973) because runoff increases during rainy periods, while topographic upwelling depending on topography and currents vary seasonally. Inorganic particles that lower transparency mainly originate from runoffs by large rivers during the monsoon season. The effect of decreasing transparency due to terrestrial runoff was measured in the 18m-deep lagoon west of Motobu Peninsula, Okinawa, where nutrient-rich fine sediments originate from a small river (Ujiıé and Shioya, 1980). Transparency is significantly lower in the lagoon (mean value 0.127 6 0.019 amplitude) compared to the shelf (mean value 0.056 6 0.009 amplitude), not only in the monsoon season

but also during the rest of the year (Sakai et al., 1984, 1986). Here winter rains and summer typhoons are responsible for the constant input of fine sediments. Decreasing transparencies raise the compensation depth (1% surface radiation) where photosynthesis balances the metabolic losses due to respiration (Valiela, 1995) from 2115m in clear ocean water (attenuation coefficient 0.04) to 235m in less transparent water (attenuation coefficient 0.13; Fig. 8). Therefore, in-

FIGURE 8. Decreasing transparency with water depth according to different light attenuation.

18

HOHENEGGER

creasing attenuation continuously restricts distribution ranges towards the shallower parts (Hallock, 1987). Thus, when the density of suspended particles is high and water transparency remains constant over the year, all larger foraminifera are able to inhabit the photic zone, but in a strongly compressed distribution form. Seasonally unstable transparencies force light dependent-organisms to move up and down the slope. Larger foraminifera are handicapped in this situation because they are unable to surmount larger depth differences, especially on flat slopes. Species that are restricted to the deeper euphotic zone and possess ‘normal’ depth ranges cannot survive strong seasonal changes in transparency (see Hallock, 1987) due to the total depletion of light in the deepest parts of their range (Dendritina zhengae, D. cf. D. zhengae, Parasorites orbitolitoides, Amphistegina bicirculata, A. papillosa, Baculogypsinoides spinosus and most nummulitids; Fig. 9). Species that are distinguished by wide depth ranges and that inhabit the middle part of the euphotic zone, like Amphistegina radiata, Operculina ammonoides, and Heterostegina depressa, reach the shallowest parts due to their upper distribution range (Fig. 9). They easily survive long-termed seasonal changes in transparency on the shallow slope, as Hallock (1987) predicted from distribution models based on light attenuation. In conclusion, low and stable transparencies compress depth distributions, but do not reduce species diversity. Unstable transparencies favor shallow-living species and those deeper-living forms with wide depth ranges, but are disadvantageous for deep-living species with narrow ranges (Hallock 1987). The lack of deep-living species in combination with the presence of diverse shallow-living larger foraminifera can thus be explained by seasonal changes in transparencies (Renema and Troelstra, 2001). WATER MOVEMENT AND SUBSTRATE Besides light, hydrodynamics are also an important factor influencing the distribution of organisms in shallow-water environments. Tropical shallow-water environments, especially reefs, where larger foraminifera live, are always affected by waves. Water movement is typically multidirectional in the wave-breaking zone and becomes bi-directional in the surge zone (Riedl, 1964; Hiscock, 1983). The velocity of bi-directional movement decreases exponentially with depth. Under fair weather conditions the sediment is disturbed down to 220m, but can be affected during tropical storms down to 2200m (Bearman, 1989). Since larger foraminifera are restricted to the euphotic zone, they always can be moved by waves, although entrainment is rare in deeper environments on the fore reef. Species of larger foraminifera that are adapted to intense illumination have to resist extreme water movement in the high-energy environments of the breaker zone and the reef crest (e.g., robust calcarinids), whereas they need to develop less strong adherence mechanisms in the lower-energy backreef area (e.g., Marginopora). Larger foraminifera develop various mechanisms to improve attachment. Multiplication of pseudopods is the first method. The highly motile amphisteginids show a knobbed area in front of the apertures (Larsen, 1976) that clearly raises the attachment points of pseudopods at the test (Hoh-

enegger, 1994; Hottinger, 2000). Peneroplids use complex (Dendritina) or multiple apertures (Peneroplis) to spread a bundle of pseudopods. Multiple apertures at the vertices of alveolinids act in a similar manner (Lipps and Severin, 1986). The second way to attain strong attachment is by special fixing mechanisms. Nummulitids (e.g., Heterostegina) protect their tests by ectoplasmic sheets that furthermore enable fixing to the substrate (Ro¨ttger, 1973, 1976). Small gamonts of the giant Cycloclypeus carpenteri are totally covered by these sheets (Kru¨ger et al., 1997). Most soritids (Sorites, Amphisorus, Marginopora) attach to flat surfaces (Ross, 1972; Hottinger, 1977a; Kloos, 1980; Ro¨ttger and Institut fu¨r wissenschaftlichen Film, 1984). The strongest fixing mechanisms are developed by calcarinids, in which organic elastic and flexible sticks extrude from the top of spines and glue to the substrate; this resists entrainment under the strongest hydrodynamic conditions (Ro¨ttger and Kru¨ger, 1990). Since larger foraminifera predominantly inhabit oligotrophic environments, the inorganic substrate on which they settle consists largely of calcium carbonate. On arid coastlines like the west Australian shelf (James et al., 1999) or the Red Sea (Reiss and Hottinger, 1984; Piller and Mansour, 1990) the episodic input of terrigeneous siliciclasts is the norm. In calcium carbonate sediments, gravel- and sandsized particles originate from calcareous skeletons. Additionally to calcareous silt and mud produced by the decay of coral skeletons and thalli of the green algae Halimeda and Penicillus (Folk and Robles, 1964; Tucker and Wright, 1990), terrigenous input by rivers leads to the deposition of fine-grained siliciclasts in quiet water. While grain size and the deposition of inorganic substrate depend exclusively on hydrodynamics, the form, size, and structure of organic substrates like macroalgal thalli or seagrass leaves reflect a combination of the three important environmental conditions light, nutrients, and water movement. The structured surface of a coral cobble as well as the infinite variety of large and small holes within a reef structure provides shelter for larger foraminifera against entrainment at the uppermost slope, especially under extreme hydrodynamic conditions. Species like Alveolinella quoyi, Amphistegina lobifera, A. radiata, Operculina ammonoides (flat form), and Heterostegina depressa—only attached to the substrate by pseudopods or protected and fixed by an ectoplasmic sheet—can be found in these small holes. Coated larger sediment particles at the deeper photic zone are the main substrate for larger foraminifera preferring firm substrate (Alveolinella quoyi, Sorites orbiculus, Amphisorus hemprichii, Amphistegina lessonii, A. bicirculata, Calcarina hispida, Baculogypsinoides spinosus, and Heterostegina depressa; Hohenegger, 1994). Larger foraminifera inhabit sandy substrates at the high-energy upper reef slope only in protected areas where they are less affected by water movement. Thick lenticular foraminiferal tests can be found in this region as an adaptation to highly movable sands (Dendritina ambigua, D. cf. D. zhengae, and the umbiliconvex form of Amphistegina lessonii; Hohenegger et al., 1999). From the fairweather down to the storm wave base, where water motion is less intensive, A. radiata, Operculina ammonoides (involute form), and Nummulites venosus settle between sand grains at the bottom surface (Hohenegger et al., 1999). The


19

FIGURE 9. Depth distribution at different transparencies. Black signatures characterize the proportion of individuals surviving seasonally changing transparencies between low (0.04) and high (0.13) attenuation.

flat, plate-like Parasorites orbitolitoides lies on the substrate, weakly attached by pseudopods to larger sand grains and gravel. Storm events often disturb these sediments and larger foraminifera with lenticular tests behave in the same way as the surrounding grains. After deposition, buried individuals must actively crawl to the sediment surface in order to provide their symbiotic algae with light. Lenticular tests are advantageous for active movement between grains. The high buoyancy of flat discoidal tests (P. orbitolitoides) promotes entrainment into suspension and reduces sinking velocity during settlement (Maiklem, 1968). After a storm event, these tests are the last to be deposited; thus they are not buried and can be found on the surface. Fine sands near and below the storm wave base are inhabited by flat-lenticular amphisteginids (Amphistegina radiata, A. papillosa) and thin discoidal, plate-like nummulitids (Operculina cf. O. complanata, Planostegina, Planoperculina, and the gi-

ant Cycloclypeus carpenteri). These sediments are only disturbed during major storms. Plate-like tests will not be buried after suspension as described above. All larger foraminifera avoid attachment to animal tissue (e.g., sponges, corals, or larger protists like Gypsina), but prefer to settle on or between branches of living plants (e.g., Brasier, 1975; Fujita and Hallock, 1999). Disc-shaped soritids settle on smooth surfaces such as corallinacean algae or seagrass leaves in high-energy, but not extreme-energy, environments. The genus Sorites has thin tests that often copy the surface, preferably when attached to corallinacean thalli, whereas the genera Amphisorus and Marginopora have thicker tests that retain their plane form. Deviations from the plane tests (Reiss and Hottinger, 1984) reflect either the test growth regime (undulating margins; Hottinger, 2000) or repair after damage. Both genera prefer seagrass leaves and flat thalli of brown algae (Sargassum, Ro¨ttger

20

HOHENEGGER

TABLE 1.

Parameters of the exponential decrease in distribution shift caused by hydrodynamics according to equations 11 and 12. Parameter a

Calcarina hispida Calcarina defrancii Dendritina ambigua Amphistegina lessonii Peneroplis pertusus Alveolinella quoyi Amphistegina radiata Peneroplis planatus Amphisorus hemprichii Amphistegina lobifera Sorites orbiculus Heterostegina depressa

144.34 115.99 115.64 107.44 103.25 101.42 93.64 87.35 85.20 74.94 68.61 64.91

and Institut fu¨r den wissenschaftlichen Film 1984; Turbinaria, Hohenegger, 1994); they also settle on rounded boulders and unstructured carbonate rocks, where they strongly attach with organic glue (glycosaminoglycans ?; Langer, 1993) to numerous fine algal filaments. These filaments, often found as epiphytes on larger macroalgae, belong to different groups (e.g., Sphacelaria, Cladophora, Acetabularia; Hohenegger, 1994) and densely cover the surface of boulders and rocks. Filamentous algae are the preferred substrate for peneroplids (Peneroplis cf. P. antillarum, P. pertusus) and A. lobifera in high-energy zones, especially on the reef crest. Here, species with weak pseudopodial attachment are protected against entrainment by these dense filaments. A loose meshwork of filamentous algae or branched rhodophycean macroalgae (e.g., Laurencia, Hypnaea, Gelidiella, Coelothrix; Hohenegger, 1994) enables larger calcarinids to hook within the algal meshwork, and additionally fix to algal thalli with elastic sticks that protrude from the tips of spines (Ro¨ttger and Kru¨ger, 1990). Such substrate dependence to resist entrainment by hydrodynamics strongly influences the depth distribution of larger foraminifera. Despite identical light conditions (e.g., same attenuation), depth distributions can be dissimilar between high-energy fore-reef areas and low-energy backreef regions, especially deep lagoons. The star-shaped foraminifers Calcarina hispida and C. defrancii have peak abundances near the water surface, clinging with spines to macroalgae. Both species are extremely abundant in the lowerenergy backreef environments (e.g., reef moats in Ishigaki Island, Japan; Hohenegger, 1994) compared to the highly turbulent reef crests and fore-reef areas, where C. gaudichaudii and Baculogypsina sphaerulata, which are better adapted to resist extreme water movement, dominate. Therefore, both C. hispida and C. defrancii are rare at the reef edge and the uppermost reef slope, but become abundant in the deeper upper slope where turbulence decreases. With the exception of Peneroplis cf. P. antillarum, Neorotalia calcar, Calcarina gaudichaudii, and Baculogypsina sphaerulata, all investigated larger foraminifera living at the shallower slope show restricted distributions towards the water surface that are affected by hydrodynamics. Depth distributions thus become deep-skewed. For estimating restriction intensities, the same method as described for light restrictions can be used. Empirical depths (x) are compared with theoretical depths (j) showing identical frequencies and

Parameter b

20.048 20.070 20.101 20.107 20.113 20.117 20.117 20.129 20.143 20.201 20.252 20.259

Amphisorus hemprichii Sorites orbiculus Heterostegina depressa Alveolinella quoyi Calcarina defrancii Calcarina hispida Peneroplis pertusus Amphistegina lobifera Peneroplis planatus Amphistegina lessonii Dendritina ambigua Amphistegina radiata

using the parameters of the fundamental depth niche. Differences y 5 x 2 j indicate distribution shifts towards the deeper part. The continuous change of these differences with depth can be fitted by the regression

y 5 aebx

b,0

(11)

Restricted depth distributions are then characterized by the equation

f(x) 5 d exp {2x 2 aebx 2 m2/(2s2)}

(12)

where the constant a of equations 11 and 12 mirrors intensities of hydrodynamics at the water surface, while constant b is correlated with the decrease of water movement with depth. Equation parameter a differs between species in being negatively correlated with attachment strength. It also differs between transects due to different hydrodynamic intensities. Highest values can be found in the calcarinids C. defrancii and C. hispida. This seems to contradict the above hypothesis, but the upper slope is densely settled by C. gaudichaudii and Baculogypsina sphaerulata. Therefore, distribution restrictions of the former two calcarinids may also represent competition with both relatives that are better adapted to extreme water movement. The order of species based on decreasing values in parameter a (averaged over transects; Table 1) confirms the assumption of correlation with attachment strength. While peneroplids, alveolinids, and amphisteginids show high values that correspond to their weak attachment, low values of soritids and H. depressa indicate stronger attachment. Arrangement of species according to parameter b of equation 11 clearly demonstrates the correlation between this parameter and test buoyancy. Weak decreases in equation 11 characterize species with plate-like tests, while peneroplids and amphisteginids with lenticular tests show steep function curves. Therefore, these species are less disturbed by hydrodynamics at the deeper slope than individuals with flat, plate-like tests (Table 1). The latter are more easily transported during storm events into environments having unfavorable conditions than individuals with spherical or thick-lenticular tests. To recognize the influence of hydrodynamics, general functions are calculated based on differences between empirical and theoretical depths of the shallow species. According to similarities in species functions, species are grouped into two classes based on test form. Since hydro-


21

FIGURE 10. Restriction of depth distributions by hydrodynamics. Residuals between empirical and normal depth distributions fitted by exponential regression.

dynamics depend on exposure to the open sea, the topographical position leads to different function intensities. Thus, four general functions have to be calculated in the investigation area, two based on test form and the others characterizing transects (Fig. 10). Whereas parameter a of equation 11 differs between transects (with higher values in the southern transect), the decrease of function 11 (parameter b), by contrast, differs significantly between test forms but shows identical intensities within groups in both transects. These generalized functions can now be used to determine the hydrodynamic influence on the depth distributions of species inhabiting the deeper slope (Fig. 11). Whereas species with lenticular tests like Amphistegina bicirculata, A. papillosa, Baculogypsinoides spinosus, Nummulites venosus, Operculinella cumingii, and Operculina ammonoides are not affected by hydrodynamics, species with plate-like tests inhabiting the middle slope (Operculina cf. O. complanata, Cycloclypeus carpenteri) show weak but significant distribution restrictions toward shallower waters. Similar to restrictions in calcarinids as mentioned above, the deep-skewed distribution of O. cf. O. complanata might be primarily caused by competition with its close relative O. ammonoides, because both distributions strongly overlap. Depth distributions whose upper part are restricted by hydrodynamics must be examined in combination with light attenuation. In the study area, transparency is close to clear ocean water (Hohenegger et al., 1999). Reduced transparency in combination with strong water movement, as can be found in tropical and subtropical continental margins with terrestrial input, impede or prevent settlement of deeper-living species in shallow regions. Species adapted to low light can survive in regions with less, but constant transparency by shifting their distributions to the shallower slope. Such shifts are possible under quiet water conditions such as in backreef areas. Turbulent water in the fore-reef hinders these shifts, especially for species that are adapted to lower light conditions and less water movement. Figure 12 shows the proportions for each species that can survive in the deep part of the shallow-shifted depth distributions. Peneroplis cf. P. antillarum, Neorotalia calcar, Calcarina gaudichaudii, and Baculogypsina sphaerulata are adapted to highest water movement and are thus char-

acterized by 100% survival. Within the peneroplids, P. pertusus is least affected by the combination of strong light attenuation–high water movement (26% survival), whereas the morphologically similar Dendritina zhengae (13%) and P. planatus (6%) as well as the thick D. ambigua (9%) are greatly restricted. Dendritina cf. D. zhengae (1%) cannot live at depths characterized by low transparency and high water energy. While Alveolinella quoyi (25% of total abundance) possibly survives in deeper parts of light-restricted environments with strong hydrodynamics, the soritids Amphisorus hemprichii (9%), Sorites orbiculus (4%), and Parasorites orbitolitoides (2%) avoid this combination of environmental parameters. Amphisteginids are better adapted to survive under these conditions. Amphistegina radiata (38%) and its deeper relative A. papillosa (46%) are much less affected than the peneroplids. Similar, but weaker tendencies can be found in A. lessonii (23%) and A. bicirculata (35%), whereas the shallowest living A. lobifera strongly depends on substrate. In the case of well-structured substrates, where this species is able to resist extreme water movement, no restriction can be detected. Otherwise, this species is the most affected within amphisteginids (10% survival) as far as the shallowest habitat is concerned. All calcarinids are strongly fixed to the substrate and therefore are least restricted by the combination low transparency and high water energy. The deepest-living Baculogypsinoides spinosus (81%) and Calcarina mayori (57%) are less affected by hydrodynamics according to their distribution shift into shallower environments. Species that need stronger light are more affected (C. defrancii: 24%, C. hispida: 16%). Nummulitids with lenticular tests (Operculina ammonoides 57%, Nummulites venosus 40%) best resist the combination of low transparency and high water energy, followed by species with plate-like tests that are adapted to light-depleted environments (Planoperculina heterosteginoides 26%, Planostegina cf. P. operculinoides 22%). Weakest resistance is demonstrated by nummulitids with flat tests living in the middle part of the euphotic zone (O. cf. O. complanata 16%, Cycloclypeus carpenteri 12%, Heterostegina depressa 12%, Operculinella cumingii 8%, Planostegina operculinoides 4%).

22

HOHENEGGER

FIGURE 11.

Substrate preference and depth distribution of larger foraminifera restricted near the surface by hydrodynamics.

TROPHIC RESOURCES AND COMPETITION Trophic resources in the sense of Hallock (1987) include inorganic nutrients such as nitrogen, phosphorus, iron, silica and other trace elements available for uptake by primary producers and organic carbon available to consumers. Trophic resources are important for the vertical and geographical distribution of larger foraminifera (Hallock, 1987, 1988a,b; Langer and Hottinger, 2000). Stable oligotrophic, nutrient-depleted environments provide the potential for fine subdivision of resources (Valentine, 1973), and cause long and complex food chains leading to K-strategies in consumers (Hallock, 1987). Mixotrophy (Hallock, 1981b) is advantageous over heterotrophy because it permits nearly total use of digestible organic matter for the host’s growth and reproduction, whereas symbiotic algae provide enough energy for respi-

ratory needs (Falkowski et al., 1984; Hallock, 2000). Hallock (2000) developed models to explore the regulation of algal growth by controlled nutrient transfer to the endo-symbionts. Low-molecular carbohydrates produced by symbiotic microalgae due to the restricted nutrient transfer cannot be used for symbiont growth and are exuded into the host protoplasm where they function as energy sources for the host’s respiration. The microalgae are protected from digestion by different mechanisms (Chai and Lee, 2000), though digestion of symbionts has been documented in Heterostegina depressa (Ro¨ttger et al., 1980, 1984), Calcarina gaudichaudii (Ro¨ttger and Kru¨ger, 1990), and Amphistegina gibbosa (Talge and Hallock, 1995). Trophic resources thus influence depth distributions of larger foraminifera in two ways. First, more nutrients stimulate plankton growth which reduces water transparency and


FIGURE 12.

23

Depth distribution at low transparencies exposed to strong hydrodynamics.

thus diminish the depth ranges of symbiont-bearing forms towards the shallower parts, as explained above. Diminution reduces the available space for settlement and causes competition between species showing similar depth ranges. This type of competition is not yet fully understood. Substrate preference could be the main factor because larger foraminifers mostly prefer firm substrates (Hohenegger, 1994; Hohenegger et al., 1999). When space is reduced and soft substrates predominate due to river runoff or high organic production, species with weak substrate preferences prevail over competitors restricted to hard substrates. Reproduction is another important factor in interspecific competition (Begon et al., 1996). Advantages in space occupation can be gained by differing reproduction times, offspring numbers and longevity, or by the dominance of asexual reproduction in high-energy environments where sexual reproduction is suppressed (Leutenegger, 1977b; Ro¨ttger et al., 1990; Fujita et al., 2000). Second, food preferences may lead to corre-

lations between foraminifera depending on extracellular food and the depth distributions of free-living microalgae. This has been proven for porcellaneous larger foraminifers (Lee et al., 1991). Food preferences may cause interspecific competition, which is also coupled to space requirements (Valiela, 1995). Although competition between larger foraminifera has been suggested (Hallock, 1987), evidence was assumed between Amphistegina lobifera and calcarinids (Hallock and Larsen, 1979). Extreme densities of Calcarina gaudichaudii and Baculogypsina sphaerulata (Sakai and Nishihira, 1981; Hohenegger, 1994) coexisting in the same habitat (and thus contradicting space competition) can be found on most NWPacific coral reef crests, giving the impression of ‘living sand’ (Lee, 1998). Similar coexistence, especially between Sorites orbiculus and Amphisorus hemprichii, and the coevolution in fossil porcellaneous larger foraminifera led to the ‘odd partnership’ hypothesis. This hypthesis involves a

24

HOHENEGGER

FIGURE 13.

Distributions of Amphistegina radiata and Heterostegina depressa restricted by a theoretical competitor.

response of similarly structured and phylogenetically related species to seasonality in oligotrophic environments by ‘pushing the carrying capacity to a level never to be reached by one partner alone’ (Hottinger, 1999). The carrying capacity of larger foraminifera is not explained in the model, but food requirements maybe involved, as is the case for porcellaneous larger foraminifers (e.g., Lipps and Severin, 1986; Faber and Lee, 1991a; Lee et al., 1991). The local coenoclines revealed a bimodal depth distribution of Amphistegina radiata in the northern transect of Sesoko, whereas it is unimodal in the south (Hohenegger, 2000). Comparison with the 1992/93 transects in the northern part of the study area (Hohenegger, 1994) confirms the bimodal distribution found in 1996 (Fig. 13). This distribution form is thus not accidental but significant. Heterostegina depressa, whose depth range is comparable to A. radiata, shows similar depth distributions. While bimodality in the 1996 northern transect is not as significant as in A. radiata, the distribution in the south shows unimodality, and bimodality is again characteristic for distributions of both transects in 1992/93 (Fig. 13). Except Dendritina cf. D. zhengae, which shows bimodality in the 1996 northern transect, all other species having comparable depth ranges (Alveolinella quovi, Parasorites orbitolitoides, Amphistegina lessonii, Calcarina mayori, Baculogypsinoides spinosus, Operculina ammonoides, Nummulites venosus) are distinguished by unimodal depth distributions in all transects of

1996 as well as 1992/93. This hints at a species competing with A. radiata and H. depressa with a narrower distribution range and similar location parameter as both suppressed species. Additionally, this species must be abundant in the northern transect, where it causes bimodal distributions in the suppressed species, and is either much less abundant or absent in the southern transect, where both species show more or less undisturbed normal distributions. The search for a competing species that meets the above criteria is supported using statistical methods. The form and intensity of competition between two species can be expressed by the equations

[ [

] ]

f 1comp (x) 5 f 1 (x) 1 2

a21 f 2 (x) , a12 f 1 (x) 1 a21 f 2 (x)

(13)

f 2comp (x) 5 f 2 (x) 1 2

a12 f 1 (x) , a12 f 1 (x) 1 a21 f 2 (x)

(14)

where f1comp(x) represents the frequency distribution of species 1 restricted by species 2 and f2comp(x) the distribution of species 2 in competition with species 1. Functions f1(x) and f2(x) characterize distributions undisturbed by competition. Besides the effect of competition based on pure frequencies, competition intensities may differ because of species fitness (Hedrick 2000). Differing fitness is expressed in equations 13 and 14 by the coefficient aij, which character-

25


TABLE 2. Distribution parameters and competition fitness of Amphistegina radiata and Heterostegina depressa in competition with a theoretical competitor and comparison with Calcarina mayori. Theoretical competitor

Amphistegina radiata

Sesoko north 1996 Sesoko 1993 firm Sesoko 1993 soft Average Fundamental distribution

Distribution optimum

Distribution mean

Distribution s.d.

Competition fitness


Distribution mean

289.29 41.49 95.42

33.76 31.32 33.63 32.90

21.25 13.51 16.18 16.98

0.184 0.200 0.038 0.141

275.79 48.10 238.51

37.50 33.87 42.82 38.07

8.93 5.55 6.04 6.84

34.47

18.87

31.12

13.17

Ampistegina radiata

Calcarina mayor

Sesoko north 1996 Sesoko 1993 firm Sesoko 1993 soft Average Fundamental distribution

66.06 91.96 13.19

Heterostegina depressa

Distribution mean

Distribution s.d.

Competition fitness


Distribution mean

29.38 36.71 28.68 31.59

24.01 12.19 18.19 18.13

0.682 0.333 0.255 0.423

56.21 431.88 69.77

41.24 37.23 38.49 38.99

7.92 6.70 5.41 6.67

31.56

17.71

31.12

13.17

izes fitness of species i versus species j (Roughgarden, 1972). This coefficient varies between 0 (no competition fitness) and 1 (maximum competition fitness). Statistical estimation of the competitor’s distribution parameters in the northern part of the investigation area using empirical depth distributions of A. radiata and H. depressa yielded very similar distributions for the theoretical competitor that demonstrate smaller standard deviations (6.84 and 6.67) than both suppressed species (16.98 for A. radiata and 18.13 for H. depressa, Table 2). The average distribution means and variances of the suppressed species correspond perfectly with the distribution parameters of the fundamental niches as gained by equations 4 and 5 (Table 2). While the competition coefficient of the theoretical competitor is close to the maximum (mean a 5 0.916 against A. radiata and 0.802 against H. depressa), which means that the competitors’ distribution is mainly disturbed by frequencies of the suppressed species, the competition coefficients of A. radiata (mean a 5 0.141) and H. depressa are small (mean a 5 0.423). The search for competitors that meet the distribution parameters of the theoretical suppressor leads to Calcarina mayori. Using a slightly changed and hydrodynamically influenced fundamental distribution (equation 12) for this species, empirical distributions of A. radiata and H. depressa are optimally fitted in the north. They show a low competition fitness for A. radiata (a 5 0.216), a high coefficient for H. depressa (a 5 0.780) and a maximum value (a 5 1) for C. mayori (Fig. 14). Distribution differences between the northern and southern transect in both A. radiata and H. depressa can now be explained by the high frequency of C. mayori in the north and its rareness in the south. This calcarinid strongly depends on firm substrates that dominate in the north down to 40m (Fig. 3), whereas H. depressa and A. radiata are less dependent on substrate. Both species prefer hard substrates, but are also abundant on sand (Hohenegger et al., 1999). The rather unaffected distributions in the 1996 southern transect can now be explained by low frequencies of C. mayori, which nevertheless influence the

Competition fitness

0.797 0.950 1.000 0.916

Theoretical competitor

Heterostegina depressa Distribution optimum

Distribution s.d.

Calcarina mayor

Distribution s.d.

Competition fitness

0.405 1.000 1.000 0.802

distributions of A. radiata and H. depressa. Using the hydrodynamically influenced fundamental distributions of both species, their empirical distributions are again optimally fitted in the south (Fig. 14). Calcarina mayori has a fitness of 0.932 against A. radiata and 0.862 against H. depressa. The competition fitness of A. radiata is higher (0.414) compared to the north, while it is much lower (0.286) for H. depressa. Although competition is supported, a more detailed explanation is difficult. Competition between A. radiata and C. mayori may be based on food, because amphisteginids grow better when feeding on extracellular microalgae: both C. mayori and its close relative C. hispida show multiple apertures that hint at food uptake. Food competition between the calcarinid and H. depressa is improbable, since the latter species does not depend on extracellular food. Furthermore, food competition cannot explain the strong suppression by C. mayori and non-competition by the extremely abundant C. hispida, which coexists in the shallow distribution parts of A. radiata and H. depressa. The latter observation hints at space competition. Amphistegina radiata attaches to the substrate less strongly than A. lessonii, and much weaker than all calcarinids. Heterostegina depressa is also characterized by weaker attachment than calcarinids. Therefore, A. radiata and H. depressa prefer to settle in small holes of coral rubble and the upper reef rock to resist entrainment by hydrodynamics, whereas all calcarinids and A. lessonii can also attach to the smooth surface of hard substrates. In the northern transect, hard substrates are well structured from the water surface to 220m and become smoother with depth (Hohenegger et al., 1999). This explains the higher abundance of A. radiata and H. depressa in their upper distribution range (hiding in small holes), whereas they compete for space with calcarinids in the middle part of their range (on smooth hard surfaces). Sandy substrates—poorly suited for calcarinids but less unfavorable for A. radiata and H. depressa—dominate beneath 250m in the northern transect (Fig. 3); this reduces

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HOHENEGGER

FIGURE 14.

Distributions of Amphistegina radiata and Heterostegina depressa restricted by competing Calcarina mayori.

competition between calcarinids and both suppressed species. Competition is important in related species that react similarly to an environmental gradient. Calcarina gaudichaudii and C. hispida are in competition, sharing the same habitat, but avoiding co-occurrence (Hohenegger, 1994; Hohenegger et al., 1999; Renema and Troelstra, 2001). Statistical investigation using equations 13 and 14 (Fig. 15) resulted in much higher competition fitness for C. hispida (0.732) compared to C. gaudichaudii (0.034). This could be based on active feeding by the former species, while the latter is restricted to glycerols produced by endosymbionts or to digestion of microalgae. Calcarina gaudichaudii, on the other

hand, is better adapted to extreme hydrodynamics, especially when filamentous algae provide shelter against traction. Competition explains the predominance of C. gaudichaudii down to 230m in swell zones, whereas C. mayori is abundant in hydrodynamically less affected surface water (e.g., Renema and Troelstra, 2001). By contrast, the closely related Calcarina hispida and C. mayori are not in competition although their depth distributions strongly overlap (Fig. 15). Competition is possible for nummulitids inhabiting the deeper euphotic zone. The morphologically related Nummulites venosus and Operculinella cumingii show similar depth distributions, with N. venosus living slightly shallow-

FIGURE 15. Competition between Calcarina gaudichaudii, C. hispida, and C.mayori, and between Nummulites venosus and Operculinella cumingii at the nothern transect of Sesoko Island.


27

FIGURE 16. Competition between Operculina ammonoides–O. complanata, and between Planostegina longisepta–P. operculinoides at the northern transect of Sesoko Island.

er (mean 5 247.3m) than Q. cumingii (mean 5 259.3m). Wide ranges (standard deviation ; 13m for both species) lead to strong overlap in the event of co-occurrence, such as in the NW-Pacific (Hohenegger et al., 2000). Nummulites venosus shows an unrestricted depth range in the Indian Ocean (Hottinger, 1980b) where the competitor is lacking, and O. cumingii is undisturbed by N. venosus in the SWPacific (Debenay, 1988). The statistical analysis shows frequency competition that is manifested by equal competition fitness (a12 and a21 5 1). This means that all factors influencing fitness like offspring number, reproduction periods, and alteration of generations are apparently similar, although these species are phylogenetically not closely related (Fig. 15). Competition is also apparent between Operculina ammonoides and O. cf. O. complanata. They co-occur in the Pacific, with the former being the shallower, and the latter the deeper species. Since O. cf. O. complanata is present only in the Pacific, the unrestricted depth range of O. ammonoides extends in the Indian Ocean and Red Sea to 2130m (Fermont, 1977; Reiss and Hottinger, 1984; Pecheux, 1995). Investigation of competition between O. ammonoides and O. cf. O. complanata confirms the wide depth range of O. ammonoides (mean 5 258.8m, s.d. 5 20.3m) in the W Pacific, similar to the proposed range in the Red Sea (Fig. 16). In the Pacific Ocean, O. cf. O. complanata is adapted to the deeper euphotic zone (mean 5 272.1m, s.d. 5 14.8m). The higher competitive fitness of O. cf. O. complanata (a 5 1) compared to O. ammonoides (a 5 0.472) intensively restricts the latter species in the overlapping zone, shifting its lower distribution limit from 2120 to 285m. Using the hydrodynamically restricted fundamental distribution, theoretical distributions based on competition optimally fit the empirical frequencies of O. ammonoides and O. cf. O. complanata (Fig. 16). Similar fitness due to offspring number, reproduction periods, etc. is supposed for the closely related shallower Planostegina longisepta and deeper P. operculinoides, which compete in overlapping regions (Fig. 16). Equivalent fitness is reflected in the similar extension of distribution ranges (standard deviation ; 11m). Competition between

related species showing identical distribution variances thus solely depends on frequencies, as is the case in N. venosus versus O. cumingii. In closely related species, lower abundance of the shallower O. ammonoides and P. longisepta compared to the deeper-living O. cf. O. complanata and P. operculinoides can be explained by the greater space competition with other species in shallow regions. The diversity of larger foraminifera significantly decreases between 240 and 280m (Hohenegger, 2000), which influences specimen abundance. This observation follows the basic relationship: high diversity → low abundance versus low diversity → high abundance. Competition in larger foraminifera is possibly caused by space requirements and thus depends on abundance. Realized coenoclines can now be calculated for each transect using the total individual number of every species. Differences between the northern (Fig. 17) and southern transect (Fig. 18) are obvious: peneroplids, alveolinids, and especially calcarinids are extremely abundant in the northern and less frequent in the southern transect. Soritids, nummulitids, and amphisteginids show similar abundance in both transects, whereby Amphistegina radiata and Heterostegina depressa are relatively unaffected by calcarinids in the south, but demonstrate restricted distribution in the north. CONCLUSION The depth dependence of mixotrophic organisms like larger foraminifera cannot be expressed in the form of a fundamental coenocline because water depth is typically a composite environmental factor. The primary factors are correlated to depth in a non-linear and sometimes discontinuous manner, resulting in complex relationships between these factors and depth. Temperature restricts larger foraminifera to those geographical regions or water depths characterized by temperatures never falling below 148 C for several weeks. Temperature decreases somewhat linearly in surface waters, but can abruptly change due to different water masses, leading to step-wise functions. A deep and constant thermocline in

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HOHENEGGER

FIGURE 17.

Realized depth coenocline at the northern transect NW off Sesoko Island.

tropical seas of the equatorial region as well as weakly decreasing temperatures without a thermocline in subtropical waters does not influence the depth distribution of larger foraminifers because the depth limit based on light is located much shallower than the minimum temperature limit. The much shallower thermocline of warm temperate seas changes with season. This leaves longer periods of cold water at depths where mixotrophic organisms live, which certainly influences depth distributions. This thermocline cuts distributions of shallow-living mixotrophic species in deeper parts, while depth-adapted species of larger foraminifers cannot survive in environments that fall constantly or even temporarily beneath the thermocline. Light is the main factor influencing depth distributions of mixotrophic organisms because the endosymbiotic algae depend on light intensity. The various species occupy different niches along the light gradient. The fundamental coenocline

in Figure 4 therefore does not reflect depth, but light intensity. Relations between the fundamental light coenocline and water depth alter due to changing transparencies. Differences in light intensity are caused by absorption through suspended inorganic particles, plankton, and particulate and dissolved organic matter. Except inorganic particles, all other factors belong to trophic resources. The more abundant resources in mesotrophic or eutrophic environments reduce water transparency and thus diminish the depth coenocline towards the shallower parts. This restriction influences the depth distribution of mixotrophic organisms in two ways. Under constant mesotrophic conditions, the reduced space for settlement—especially the hard substrates that larger foraminifera mostly prefer—leads to competition. Only species tolerating hard substrate as well as sand (Peneroplis pertusus, Alveolinella quoyi, Amphisorus hemprichii, Amphistegina lessonii, A.


FIGURE 18.

29

Realized depth coenocline at the southern transect W off Sesoko Island.

radiata, Operculina ammonoides, O. cf. O. complanata, Heterostegina depressa) or are restricted to soft substrate (Dendritina ambigua, D. zhengae, Parasorites orbitolitoides, Nummulites venosus, Operculinella cumingii, Planostegina operculinoides, P. cf. P. operculinoides) tolerate these conditions. A few symbiont-bearing larger foraminifera (Operculina discoidalis) seem to be restricted to muddy substrates with high organic content, becoming the monospecific larger foraminifer dominating in these environments. Species adapted to low light intensities are at a disadvantage under rapid seasonal alterations. Larger foraminifera, especially the deep-living nummulitids, are handicapped due to their slow movement: they cannot surmount seasonal depth differences in light intensity. Species adapted to high or medium light intensities, often combined with wide depth ranges (Heterostegina depressa, Operculina ammonoides, Nummulites venosus), can survive such rapid change in light conditions because movement is unnecessary. Hydrodynamics is the third factor that influences distributions of larger foraminifera. Only water motion by windinduced waves is continuously correlated with depth under constant wind force, again showing an exponential decrease. Different wind intensities influence water motion, whereby the sea bottom can be affected during storms down to 2200m. Foraminifera living in shallowest regions exposed to the open sea are affected by these extreme forces and have to develop attachment mechanisms that resist entrainment. Some species (Peneroplis antillarum, Amphistegina lobifera), especially calcarinids, are adapted to high-energy environments, whereas most shallow-living species avoid

such conditions. Unidirectional water movement like weather-band, tidal and ocean currents depends on topography. They are also correlated with depth, although, according to topographical differences (i.e., width and depth of sea passages) in combination with current strength, hydrodynamics can differ extremely between locations of equal depth. High current velocities up to 3m sec21 can occur at 2100m. Larger foraminifera that are adapted to low light (Operculina cf. O. complanata, Planoperculina heterosteginoides, Planostegina operculinoides, Cycloclypeus carpenteri) cannot resist such extreme energies. Although light conditions are identical, depth coenoclines can therefore strongly differ between low- and high-energy environments, especially near the surface, but also with different intensities in deeper parts due to topographically-related current strength. Inorganic and organic substrates are affected by water energy. While inorganic and organic hard substrates provide shelter against entrainment, movable soft substrate requires other life strategies for larger foraminifera. Thick-lenticular tests are ideal for crawling back to the surface when species are embedded in the sediment during storms, while platelike tests with high buoyancies and low sinking velocities are deposited directly on the surface after sedimentation of grains during the waning storm. Since hydrodynamics are not linearly correlated with depth, substrates reflecting water energy also show complex depth relations. The foraminiferal fauna differs between substrate types. Where hard substrates predominate in deep environments, Amphistegina bicirculata, A. radiata, a few Calcarina mayori, Baculogypsinoides spinosus, Cycloclypeus carpenteri are found, whereas on soft bottom Planostegina operculinoides, Plan-

30

HOHENEGGER

operculina heterosteginoides, and Operculina cf. O. complanata occur. Amphistegina papillosa is abundant on both substrates. Space is apparently the main factor governing competition in larger foraminifera. Besides competition between phylogenetically unrelated species like Amphistegina radiata and Heterostegina depressa on the one hand and Calcarina mayori on the other, space competition is important in habitat partitioning between closely related species (Operculina ammonoides–Operculina cf. O. complanata, Planostegina longisepta–P. operculinoides). When a competitor is missing due to geographical differences, the depth distributions of the partner become wider, thus complicating depth estimation. Resource competition can be supposed for porcellaneous foraminifers that depend on food, but this remains to be investigated. This study clearly demonstrates the difficulties of estimating depth by coenoclines of larger foraminifera, since relations between temperature, light, hydrodynamics, and substrate to depth are mostly non-linear and often discontinuous. Only with the knowledge of all relation types between depth and primary factors, does a non-linear multiple regression analysis based on species frequencies allow inferences about depth. ACKNOWLEDGMENTS This paper is the result of several projects. The main work was done within the three projects P 10946-GEO (Relations between Bio- and Taphocoenoclines of Larger Foraminifera), P 11107-GEO (Population Dynamics of Larger Foraminifera on West-Pacific Reef Flats), and P 13613-BIO (Morphoclines and Depth Dependence of Metrical Test Characters in Larger Foraminifera from the West-Pacific) of the Austrian Science Fund. Thanks are due to the Tropical Biosphere Center, Sesoko Station, University of the Ryukys, Japan (directors Prof. K. Takano and Prof. K. Yamazato), where fieldwork was performed as a visiting scientist from September 1992 to August 1993 and from June 1996 to September 1996. Research was conducted as a guest professor at the Research Center for the South Pacific, Kagoshima University, Japan (director Prof. A. Inoue), from September 1997 to March 1998. This institution enabled participation at an excursion to Belau, Caroline Islands, on the research vessel ‘Keiten Maru’ in 1995. The author investigated larger foraminifera under support of the Japanese Society for the Promotion of Science (JSPS) at Sesoko Station, Okinawa, Japan (host Prof. K. Yamazato) in 1986 and at the Kagoshima University (host Prof. K. Oki) in July/August 1999, where samples at Amami-O Shima and Tanegashima were collected during a trip on the research vessel ‘Keiten Maru’ of the Faculty of Fisheries, Kagoshima University. Personal thanks are due to the colaborators E. K. Yordanova and Ch. Baal (Vienna University), to the Japanese collegues and friends K. Oki and A. Hatta (Kagoshima University), to Y. Nakano, S. Nakamura (Sesoko Station, University of the Ryukyus) and F. Tatzreiter (Vienna) for their help in sampling, and to all the technical and scientific staff at the Institute of Paleontology University of Vienna, the Tropical Biosphere Center in Okinawa, the Reserch Center for the South Pacific in Kagoshima, the Department of

Environmental Science in Kagoshima, and the research vessel ‘Keiten Maru’ (Faculty of Fisheries, Kagoshima University). Several discussions with J. Erez (Jerusalem, Israel), L. Hottinger (Basel, Switzerland), and especially R. Ro¨ttger (Kiel, Germany), who cultured living foraminifera from the investigation area, were extremely helpful for this work. M. Stachowitsch (Vienna) as a native English speaker corrected the text. Thanks are due to the reviewers E.C. Sullivan (Houston, Texas) and especially P. Hallock (St. Petersburg, Florida), which corrected the manuscript and gave many comments and hints. The editor, Ron Martin, made constructive suggestions for better presentation. REFERENCES BEARMAN, G. (ed.), 1989, Waves, Tides and Shallow Water Processes: The Open University, Pergamon Press, Oxford, 187 pp. BEGON, M., MORTIMER, M., and THOMPSON, D. J., 1996, Population Ecology. 3rd Ed.: Blackwell Science, Oxford, 247pp. BELLEMO, S., 1974a, Ultrastructures in Recent radial and granular Foraminifera: Bulletin of Geological Institute University Uppsala, N. S. 4, p. 117–122. , 1974b, The compound and intermediate wall structures in Cibicidinae (Foraminifera) with remarks on the radial and granular wall structures: Bulletin of Geological Institute University Uppsala, N. S. 6, p. 1–11. BIRKS, H. J. B., 1995, Quantitative palaeoenvironmental reconstructions, in Maddy, D., and Brew, J. S. (eds.), Statistical Modelling of Quaternary Science Data. Technical Guide 5: Quaternary Research Association, Cambridge, UK, p. 161–254. BRASIER, M. D., 1975, Ecology of recent sediment-dwelling and phytal foraminifera from the lagoons of Barbuda, West Indies: Journal of Foraminiferal Research, v. 5, p. 42–62. BRETT, C. E., 1995, Sequence stratigraphy, biostratigraphy and taphonomy in shallow marine environments: Palaios, v. 10, p. 597– 616. CHAI, J., and LEE, J. J., 2000, Recognition, establishment and maintenance of diatom endosymbiosis in foraminifera: Micropaleontology, v. 46, suppl. 1, p. 182–195. DEBENAY, J.-P., 1988, Foraminifera larger than 0.5mm in the southwestern lagoon of New Caledonia: distribution related to abiotic properties: Journal of Foraminiferal Research, v. 18, p. 158–175. DOHLER, G., and HAAS, F. T., 1995, UV effects on chlorophylls and carotenoids of the haptophycean algae Pavlova: Photosynthetica, v. 31, p. 157–160. DREW, E. A., 1983, Light, in Earll, R., and Erwin, D. G. (eds.), Sublittoral Ecology. The Ecology of the Shallow Sublittoral Benthos: Clarendon Press; Oxford, p. 10–57. DUNLOP, W. C., and CHALKER, B. E., 1986, Identification and quantification of near-UV absorbing compounds (S-320) in a hermatypic scleractinian: Coral Reefs, v. 5, p. 155–159. FABER, W. W., and LEE, J. J., 1991, Feeding and growth of the foraminifer Peneroplis planatus (Fichtel and Moll) Montfort: Symbiosis, v. 10, p. 63–82. FALKOWSKI, P.G., and RAVEN, J. A., 1997, Aquatic Photosynthesis: Blackwell Science, Malden, Mass, 373 pp. , DUBINSKY, Z., MUSCATINE, L., and PORTER, J. W., 1984, Light and the bioenergetics of a symbiotic coral: BioScience, v. 34, p. 705–709. FERMONT, W. J. J., 1977, Biometrical investigation of the genus Operculina in Recent sediments of the Gulf of Elat: Utrecht Micropaleontological Bulletin, v. 15, p. 111–147. FOLK, R. L., and ROBLES, R., 1964, Carbonate sand of Isla Perez, Alacran Reef complex, Yucatan: Journal of Geology, v. 72, p. 255–292. FUJITA, K., and HALLOCK, P., 1999, A comparison of phytal substrate preferences of Archaias angulatus and Sorites orbiculus in mixed macroalgal-seagrass beds in Florida Bay: Journal of Foraminiferal Research, v. 29, p. 143–151. FUJITA, K., NISHI, H., and SAITO, T., 2000, Population dynamics of Marginopora kudakajimaensis Gudmundsson (Foraminifera: Sor-


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Received 15 October 2002 Accepted 13 February 2003

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