Orbitally induced cycles in benthonic foraminiferal morphogroups and trophic structure distribution patterns from the Late Albian “Amadeus Segment” (Central Italy)

A detailed analysis was made of benthonic foraminiferal distribution patterns and morphogroups in the late Albian “Amadeus Segment” of the Aptian-Albian organic-rich Scisti a Fucoidi Formation outcropping over a widespread area of the Umbria-Marche region, Central Italy. Rhythmic changes in the trophic structures and composition of benthonic foraminiferal assemblages suggest cyclical fluctuations of the sea floor environment which appear to be orbitally induced. Benthonic foraminiferal assemblages varied significantly through the section and appear to contain a strong paleoecological signal. Fluctuations in both bottom water oxygenation and the surface primary productivity as a result of the orbital forcing are interpreted to have been the primary controls on benthonic foraminiferal distribution patterns.


INTRODUCTION
Foraminifera h a v e been extensively used for paleoenvironmental interpretation, and the use of various morphological g r o u p s in benthonic foraminiferal assemblages is not new. This approach has been used, especially in the Cretaceous, to study the organic rich strata which were a global component of this period in a variety of lithologies and paleoenvironments. Several studies (Jones & Charnock, 1985;Bernhard, 1986;Corliss & Chen, 1988;Coccioni, 1990a and b;Koutsoukos & Hart, 1990;Coccioni & Galeotti, 1991;Kaiho, 1991, among others) have shown the utility of this method and its potential in detecting the paleoceanographic conditions in which the hypoxic/ anoxic events took place. Moreover, the influence of orbital forcing on benthonic foraminiferal assemblage pattern distribution has been recently recognized by Cottle (1989), Leary r t nl. (1989), and Coccioni & Galeotti (1991).
The present s t u d y aims to document the benthonic foraminiferal distribution patterns from the Late Albian "Amadeus Segment" (Coccioni & Galeotti, 1991) of the Fiume Bosso section (Fig. l), using a morphological approach.

MATERIAL AND METHODS
The A m a d e u s Segment w a s s a m p l e d b e d by b e d ( a t approximately 5-cm intervals) from a deep trench to eliminate surface contamination. The samples were marked as AMS 1 to AMS 38 from bottom to top. The CaCO, content of each sample w a s estimated volumetrically. Sample preparation for foraminiferal study involved: crushing of 150 gr of sampie; disaggregation by diluted hydrogen peroxide; washing through a 32 pm sieve; and drying. All the benthonic foraminifera were picked from the three coarser fractions (> 420 pm, 420-250 pm, 250-125 pm) i n t o n u m b e r e d slides for quantitative analysis. The composition of the remaining fraction ( 4 2 5 pm) was only noted, but in no cases did it contain species not recorded from the other fractions. The classification followed is based on Loeblich & Tappan (1988). Plates 1 and 2 illustrate all identified taxa. The quantitative analysis was carried out by studying the variations i n a b u n d a n c e of the species within the assemblages. O n t h e basis of their shape, chamber arrangement, and inferred mode of life, the recognized species were grouped into 10 morphogroups (see Table 1); then, the variations in relative abundance of these groups w i t h i n the assemblages w e r e observed. To obtain information on the trophic structure variations a number of indices were calculated including: the number of specimens per 100 g of dried sample; the number of genera per sample; the infaunal (I)/epifaunal (E) forms ratio calculated as I / I+E x 100; and the agglutinating (Ag) / calcareous hyaline (CH) forms ratio calculated as A g / A g + C H x 100. The absolute a b u n d a n c e of planktonic foraminifera w a s estimated by counting on a g r a d u a t e d screen a n d comparing obtained values with those from grain-size diagrams (Baccelle & Bosellini, 1965). Finally, to detect periodicity in the foraminiferal data, a fourier function analysis was applied to the abundance records of each species, genus, and morphogroup. This analysis w a s carried o u t by using the Strata Base 6.1 program (Ripepe, 1988). The type of sampling might have affected the result of the spectral analysis since it did not take into account the possible variations within a single layer and because it was too wide. However, detailed study of samples taken in several sites along a single layer s h o w e d consistency of benthonic foraminiferal assemblages. Furthermore, only spectral analyses that showed cyclicity clearly enough to be retained as primary were considered valid.

RESULTS
The CaC03 content of the Amadeus Segment ranges from 50 to 75% (Fig. 4), with minima of 50-55% in the blackshales. Planktonic foraminifera are more abundant in s a m p l e s with l o w carbonate content w i t h greatest abundance in the marly layers, whereas they decrease in abundance in samples rich in carbonate (Fig. 4).
The benthonic foraminiferal assemblages of the Amadeus Segment are composed of calcareous hyaline and both calcareous a n d silicified-walled agglutinating forms. Preservation is moderate to good. Forty-two species were identified belonging to twenty-two genera among which Gyroidinoides, Arenobulimina, Dorothia, and Clavulinoidcs predominate.
The benthonic foraminiferal assemblages change with lithology and three distinct associations can be recognized ( Table 3) (iv) Small size of the specimens (< 250 ym); (v) Predominance of high surface to volume ratio morphotypes.
The distribution of many species, genera, and morphogroups through the Amadeus Segment appears to be cyclical (Figs. 5 and 6). However, some of them (e.g. M a r s s o ri e 11 a ox y co n a, P 1 e u r o s t o m e 11 a, and branching morphotypes) exhibit such a discontinuous distribution that i t would be very difficult to carry out a significant evaluation. On the basis of an assumption of uniform sedimentation rate, the spectral analyses support the hypothesis that, in some cases, the cyclicities appear to be astronomically driven (Fig. 7). In addition, since other workers (Herbert & Fischer, 1986;Herbert, 1987;Fischer & Herbert, 1988;Premoli Silva et al., 1989a and b;Fischer et al., 1991) have already provided strong evidence of Milankovitch Cyclity influencing sedimentation in this sequence, then it is reasonable to interpret the benthonic foraminiferal patterns in this context.
Based on these works the benthonic foraminiferal distribution patterns in the Amadeus Segment can be largely explained in terms of oxygen content variations. Both the composition and the abundance of the benthonic foraminiferal assemblages are different in the different lithotypes. The BSA composition suggests a high degree of oxygen depletion on the bottom water. In contrast, both the MA and the CMA compositions are indicative of well oxygenated bottom water. The MA assemblage displays highest abundance of benthonic foraminifera in the fraction greater than 125 pm. This measure of the benthonic foraminiferal assemblages (benthonic foraminiferal flux) has been shown to be directly linked to organic flux rates (Herguera & Berger, 1991) suggesting fluctuation in primary productivity. The low abundance in the CMA is, probably, a reflection of rapid sedimentation, which may dilute the benthos.
On the basis of the distribution of species, genera and morphogroups in the different lithotypes which are assumed to reflect different oxygenation conditions, we have tried to identify aerobic, intermediate, and anaerobic forms (Table 3). According to some authors (Bernhard, 1986;Coccioni, 1990a and b;Kaiho, 1991) infaunal anaerobic forms have higher surface area-to-volume ratios than aerobic ones. Leutenegger & Hansen (1979) suggested that high surface area-to-volume ratios and high porosity tests could provide a greater area for mitochondria1 oxygen uptake. Moreover, we suggest that tapered and elongate morphologies could facilitate movement towards the watersediment interface where the quantity of dissolved oxygen is greater.
The infaunal assemblages are devoid of intermediate forms (Table 3). This suggests, the infaunal forms were highly sensitive to dissolved oxygen content changes. Conversely, the epifaunal assemblages are almost entirely represented by intermediate forms, suggesting less sensitivity of these assemblages to oxygen content variations.
The aerobic assemblages include a good percentage of Pleurostomella specimens which, on the contrary, was suggested as an anaerobic index by Bernhard (1986) and Kaiho (1991). Moreover, other forms considered aerobic by these authors (e.g., planoconvex, lenticular, globular / sphaerical morphotypes) or anaerobic (e.g.,

Nodosaria and D e n t a l i n o i d e s ) are here considered intermediate indices of dissolved oxygen content.
The infaunal anaerobic forms from the Amadeus Segment have a high surface area to volume ratio, while epifaunal forms with a very high surface area to volume ratio represent intermediate or even aerobic indices. This implies that, in certain conditions, a particular morphology can be adaptive for an infaunal strategy but not for an epifaunal strategy. In conditions where oxygenation is low, for example, an infaunal species with a cylindrical and elongate morphology may have had an advantage because it could move more easily towards the water-sediment interface      Fig. 7 Spectral analyses of the benthonic foraminifera1 assemblages distribution throughout the Amadeus Segment. For each spectrum, the vertical axis represents power, the horizontal axis is harmonic number. Particularly strong peaks are labelled with their periodicity, in Ma.  AMS 16, x53. Fig. 15. Pyramidulina ohscura (Reuss), sample AMS 2, x35. Fig. 16. Pyramidulina pnuprrcola (Reuss), sample AMS 2, x35. Fig. 17. Nodosaria lirnbata d'Orbigny, sample AMS 30, x53. Fig. 18. Nodosavia sp. 1, sample AMS 26, x70. Fig. 19. Nodosaria sp. 2, sample AMS 1, x70. Fig. 20. Nodosaria sp. 3, sample AMS 2, x70. where there is a greater quantity of dissolved oxygen. In the same oxygenation conditions an epifaunal species with the same morphology might have been at a disadvantage because it would tend to sink into the substrate where the dissolved oxygen content is lower. Furthermore, it is possible that similar morphotypes can be characterized by a different feeding strategy. In this case the distribution of the morphogroups would be influenced not only by the dissolved oxygen content but also by the availability of nutrients on the sea floor.

Explanation of
Most of morphological studies on benthonic foraminiferal assemblages in dysaerobic environments have been carried out on sediments deposited under conditions of high epipelagic produbtion. The high primary productivity levels contribute to high nutrient fluxes in the form of particulate organic material inducing oxygen deficiency in bottom waters. Deposited organic matter and bacteria are the primary trophic resource for the microbenthos thriving under such conditions. Contrary to this model, the black shale layers from the Amadeus Segment represent conditions of moderate to low fertility (Premoli Silva et al., 1989a;Erba, 1988 and; this helps to explain the different behaviour of the epifaunal assemblages from the Amadeus segment to those studied by Bernhard (1986) and Kaiho (1991) (see above).
The cyclical assemblage changes recognized in the Amadeus Segment are, probably, a result of cyclical changes in both oxygen content and primary productivity induced by orbital forcing. In fact variations of these two parameters cause considerable changes in the trophic structure of the bottom environment and so in the benthonic communities (Jones & Charnock, 1985;Bernhard, 1986;Coccioni, 1990b;Koutsoukos & Hart, 1990;Premoli Silva & Erba, 1991, among others).
The influence of orbital forcing on benthonic foraminiferal assemblage pattern distribution has been reported previously from the Cenomanian and Turonian of southern England (Leary et al., 1989;Cottle, 1989) and from the Late Albian of Central Italy (Coccioni & Galeotti, 1991). Leary et al. (1989) showed that changes in the abundance of Lenticulina and Gavelinella were related to changes in amount of introduced carbonate sediment as a consequence of the precessional forcing of the climate. Detailed sampling of two sections of Turonian-aged Chalk from south-east England for foraminifera has revealed that cyclical abundance changes of Gyroidinoides nitidus and Gavelinella emscheriana were mediated by orbitally induced climatic cycles (Cottle, 1989). In particular, changes in abundance of G. nitidus were driven by the obliquity cycle. Instead, in the Amadeus Segment the cyclical changes in abundance of this species are correlatable to the precessional cycle. Evidently, a single species may show a different sensitivity to orbital forcing through time (probably under different climatic regimes) or at different paleolatitudes.

CONCLUSIONS
Abundance, taxonomic composition, morphology, and test size of benthonic foraminifera fluctuate greatly from layer to layer throughout the Amadeus Segment reflecting dynamic fluctuations of the sea floor environment.
With respect to lithology, three peculiar associations (MA, CMA, and BSA) have been identified which we suggest to be related to different degrees of primary productivity and oxygenation of the bottom water. This paper provides evidence that these changes are the result of orbitally induced productivity and redox cycles .
The influence of orbital forcing has been recognized in the distribution of some species, genera and morphogroups. Moreover, the orbital forcing drives cyclic changes in the trophic strategies. Our data demonstrate that a single species may show different sensitivity to orbital forcing through time (probably under different climatic regimes) or at different paleolatitudes.
The impoverishment of the benthonic foraminifera assemblages within the black shales, which were deposited under a low productivity regime, can be attributed to oxygen depletion under stratified water conditions. It coincides with predominance of the more specialized anaerobic forms within the infaunal assemblages, which are more sensitive indicators of oxygen content variations. In the more calcareous lithotypes, which were deposited under high productivity regimes, the impoverishment of the benthonic foraminiferal assemblages is interpreted as due to the rapid introduction of a large amount of sediment, mainly made up of nannoplankton, which tend to dilute the benthos.