This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and

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2 Marine Micropaleontology 76 (2010) Contents lists available at ScienceDirect Marine Micropaleontology journal homepage: Research paper Benthic foraminiferal responses to absence of fresh phytodetritus: A two-year experiment Elisabeth Alve Department of Geosciences, University of Oslo, P.O. Box 1047 Blindern, 0316 Oslo, Norway article info abstract Article history: Received 3 February 2010 Received in revised form 26 May 2010 Accepted 31 May 2010 Keywords: Survival Benthic foraminifera Food quality Trophic strategy Refractory organic material Resilience Sediment and bottom water from 320 m water depth in the Skagerrak basin (NE North Sea) was maintained in the laboratory and kept unfed in the dark, at ambient temperature, for two years. Although the relative abundance of agglutinated taxa in the sediments increased at the expense of allogromiids and calcareous forms, the deprivation of fresh phytodetritus caused only a moderate change of the faunal composition of the bathyal, benthic foraminiferal assemblage (six of the seven most abundant species were the same before and after the treatment; overall similarity was 58%). Among the most common species, the halt in supply of fresh organic material promoted population growth in some (e.g., Textularia earlandi, Leptohalysis gracilis, Melonis barleeanum), some maintained their populations (e.g., Globobulimina auriculata, Liebusella goësi, Eggerelloides medius), while others (e.g., Nonionella iridea, Cassidulina laevigata, and some allogromiids, particularly Micrometula hyalostriata) nearly disappeared. The different responses probably reflect the species' relative dependence on fresh phytodetritus. Those species which could utilize food stored or produced in the sediments (e.g., bacteria and degradation products) increased or maintained their populations, whereas those dependent on fresh phytodetritus and/or associated early-decomposition products declined. In spite of these changes, the species diversity showed only a minor reduction. The overall moderate response to lack of fresh phytodetritus was probably due to the fact that the assemblage already was adapted to an environment dominated by poor quality food particles. The study illustrates that the quality of organic material has an important impact on the composition and maintenance of some benthic foraminiferal communities, that the faunal response to reduction, or even a halt, in the supply of fresh phytodetritus, is not necessarily immediate or dramatic, and that the response depends on the trophic conditions prevailing in the area when the halt occurs Elsevier B.V. All rights reserved. 1. Introduction An understanding of the dynamics and processes controlling the spatial distribution and microhabitats of benthic foraminifera is crucial for optimizing palaeoecological interpretations of both older and more recently deposited fossil assemblages. Due to an increased realization of the role they play in recycling of organic carbon and their usefulness as palaeoenvironmental and human impact indicators, the last decades have seen an increasing number of studies focusing on relationships between C org -fluxes and benthic foraminiferal ecology. Shirayama (1984) and Corliss and Emerson (1990) illustrated some of the fundamental relationships between the flux of C org to the sea floor, dissolved [O 2 ] of the benthic habitat and meiofauna/benthic foraminiferal microhabitats. Their thoughts and suggestions were synthesised into the TROX model (Jorissen et al., 1995). Since then, numerous studies have extended our knowledge on aspects of microhabitats, Tel.: ; fax: address: ealve@geo.uio.no. trophic status, and associated environmental parameters. It is now well established that benthic foraminifera in oligotrophic environments, such as the deep sea, respond to phytoplankton blooms and subsequent arrival of phytodetritus at the sea floor by increased abundance of opportunistic species (e.g., Gooday, 2003). Responses are also seen in shelf (e.g., Duchemin et al., 2008) and coastal/fjordic (e.g., Gustafsson and Nordberg, 2001) environments where food is a limiting factor. Phytodetritus deposition in the oceans is highly variable spatially and temporally. For example, some regions may not have phytodetritus accumulation on the sea floor each year (Beaulieu, 2002). Recently, environmental remediation in areas previously impacted by cultural eutrophication experience reduced primary production and hence less food to the benthos (e.g., Alve et al., 2009). It would be useful to understand the impact this variability has on benthic foraminiferal faunas. How does a decrease or even a cease in phytoplankton production, and thereby a depletion in the flux of freshly produced organic material to the sea floor, affect the benthic fauna? Answers to this question can throw light on how dependent certain species are on regular supplies of fresh organic material. The /$ see front matter 2010 Elsevier B.V. All rights reserved. doi: /j.marmicro

3 68 E. Alve / Marine Micropaleontology 76 (2010) Table 1 Number of live (stained) foraminifera counted in the freshly collected and the stored 2004-sediments. The two size fractions and their sums are shown separately for each data set. Data-set Size fraction counted μm N125 μm N63 μm μm N125 μm N63 μm Allogromia crystallifera Cylindrogullmia alba Gloiogullmia sp Micrometula hyalostriata Nemogullmia longevariabilis Tinogullmia hyalina Allogromiid sp N Allogromiid oval Allogromiid neck Adercotryma wrighti Astrammina sp. (fragile) Bathysiphon argenteus Bathysiphon sp Cribrostomoides crassimargo Cribrostomoides jeffreysii Cribrostomoides subglobosa Eggerella europeum Eggerelloides medius Haplophragmoides bradyi H. cf. membranaceum Hippocrepinella alba Hippocrepinella remanei Leptohalysis catenata Leptohalysis gracilis Leptohalysis scottii Leptohalysis sp Liebusella goësi Morulaeplecta bulbosa Paratrochammina sp Phainogullmia spp Portatrochammina murrayi Recurvoides trochamminiforme Reophax dentaliniformis Reophax fusiformis Reophax rostrata Reophax subfusiformis Saccammina (white, fine grained) silver saccaminid Technitella sp Textularia kattegatensis Textularia earlandi Trochammina skrumpa Trochamminopsis quadriloba trochamminid trochamminid Bolivinellina pseudopunctata Brizalina spathulata Bulimina marginata Cassidulina laevigata Elphidium albiumbilicatum Elphidium excavatum Epistominella vitrea Fissurina sp Gavelinopsis praegeri Globobulimina auriculata Hopkinsina pacifica Hyalinea balthica Lenticulina sp Melonis barleeanum Nonionella turgida Nonionella auricula Nonionella iridea Oolina hexagona Pullenia osloensis Quinqueloculina sp Stainforthia concava Stainforthia fusiformis Uvigerina peregrina No. counted foraminifera No. spp Allogromiid taxa (%) Agglutinated taxa (%) Calcareous taxa (%) Fisher alpha index 9,6 6,5 11,4 7,4 4,7 7,6 ES(100)

4 E. Alve / Marine Micropaleontology 76 (2010) Table 1 (continued) Data-set Size fraction counted μm N125 μm N63 μm μm N125 μm N63 μm H (log e ) 2,7 1,6 2,8 2,4 1,7 2,6 H (log 2 ) 3,8 2,3 4,0 3,5 2,5 3,8 No. of Gromia pr counted foraminifera No. Gromia/No. foraminifera 0,01 0,10 0,048 0,00 0,07 0,02 results may have important implications for 1) understanding the processes (including the time aspect) associated with environmental remediation and faunal recovery following human impacts on benthic ecosystems (e.g., reduced nutrient discharges), 2) interpretations of what consequences e.g., extraterrestrial impacts with subsequent loss of primary production, may have on an important part of the benthic community, and 3) understanding variations in benthic foraminiferal δ 13 C. This study addresses the effect of phytoplankton deposition variability by maintaining benthic foraminifera in the laboratory without the introduction of new food over a two-year period. A comparison of the living fauna after two years with living fauna analysed at the time of sediment collection provides insight into the impact of phytodetritus and the resilience of benthic foraminifera to food availability. The same sediment was also used in an experiment focussing on survival and dispersal potential of benthic foraminiferal propagules (Alve and Goldstein, 2010) , and temperature C (data from sta. H1 H3 in Ståhl et al., 2004). On 21st August, 2002, sediment from three of the six containers was combined and sieved with ambient sea water through 32, 63, and 125 μm sieves, and the b32 μm-fraction was used in a propagule experiment (Alve and Goldstein, 2010). The coarser fractions were fixed in 4% buffered formalin in sea water, later re-sieved, and preserved in 70% ethanol with rose Bengal (1 g/l). Parts of the and N125 μm-fractions were examined for the propagule study. The sediment in the remaining three containers (sediment height about 1.5 cm in each) was stored untouched (sealed at all times) in a dark cold-room (7 C) for two years. On 27th August, 2004, the stored sediment was sieved through the same set of sieves, the fine fraction (b32 μm) was used in the propagule experiment (Alve and Goldstein, 2010), and the coarse fractions fixed and treated as described above. In the present study, the rose Bengal-stained and N125 μmfractions were combined and subsamples of the N63-μm fraction of the and 2004-sediments were sieved through 63- and 125-μm sieves. 2. Material and methods Sediment used in this study was collected with a box corer on 12th August, 2002, from a 320-m site in the Skagerrak basin (North Sea), midway between Norway, Sweden and Denmark ( N; E). Immediately upon arrival on deck of the RV Arne Tisselius, 9 L of seawater just above the sediment water interface in the box corer were transferred to a plastic container, and 29 cm 26 cm of the surface sediment (top 2 cm) was randomly transferred to 6 transparent 1000 ml (Joni DK, no ) plastic containers (sediment height cm in each), ambient sea water was added and the containers were sealed. The containers were kept in dark cold-rooms at ambient temperatures, first on the ship (5 C) and later at Oslo University (7 C). Bottom water characteristics of the present sampling site include bottom water [O 2 ] N85% saturation, salinity Fig. 1. Relative abundance of the most common species (N63-μm fraction) at a 320-m site in the middle part of the Skagerrak at the time of collection in 2002 (left) and from the same site and collection after having been kept in the original sediments for two years in the dark, in closed containers with ambient seawater and at ambient temperature (right). Fig. 2. Relative abundance of the most common species (N63-μm fraction) at a 320-m site in the middle part of the Skagerrak at the time of collection in 2002 and from the same site and collection after having been kept in the original sediments for two years in the dark, in closed containers with ambient seawater and at ambient temperature. Solid line (lower diagram) shows the 1:1 relationship between the two datasets.

5 70 E. Alve / Marine Micropaleontology 76 (2010) and 2004-sediment yielded abundant populations of several species with individuals N63 μm in size after being exposed to simulated shallow-water conditions (Alve and Goldstein, 2010). Because figures for the exact volume of the original 2002-sediment and of the stored 2004-sediment were not needed for the propagule dispersal experiment, absolute abundance data (foraminifera/cm 3 ) were not possible to determine for the present study. Species diversity was expressed using the Fisher alpha (Fisher et al., 1943), Shannon Wiener (Shannon and Weaver, 1963) withh (log e )andh (log 2 ), and Hurlbert's (Hurlbert, 1971) ES n = 100 indices. The similarity between pairs of samples was calculated according to Walton (1964) by summarizing the lowest common percentage values for each species. 3. Results Fig. 3. Relative abundance of the most common species (top: μm- and bottom: N125-μm fractions) at a 320-m site in the middle part of the Skagerrak at the time of collection in 2002 (left) and from the same site and collection after having been kept in the original sediments for two years in the dark, in closed containers with ambient seawater and at ambient temperature (right). For relative abundance of the same species in the complete N63-μm fractions,seefig. 1. The complete content of live (stained) foraminifera in the and N 125-μm fractions was wet-counted. Only individuals with brightly stained cytoplasm in most chambers were considered as being live at the time of collection. The presence of live populations was confirmed through the propagule experiment as the b32 μm-fraction of both the Table 2 Categories of bathyal (320 m) species according to how their relative abundance changed during two years of isolation (unfed) in the dark (i.e., deprived of fresh phytodetritus) in their native sediment with ambient water and at ambient temperature. %-values refer to the N63 μm-fractions. Category 1 Category 2 Category 3 Common taxa which nearly disappeared Allogromiids Nonionella iridea Cassidulina laevigata Taxa increasing from rare (b0.5%) to common (2 9%) Leptohalysis gracilis Eggerella europeum Hippocrepinella alba Trochammina skrumpa Technitella sp. Melonis barleeanum Adercotryma wrighti Haplophragmoides bradyi Reophax rostrata Abundant taxa showing some change Textularia earlandi (++) Globobulimina auriculata ( ) Liebusella goësi ( ) Stainforthia fusiformis ( ) Eggerelloides medius ( ) Pullenia osloensis (+) Reophax fusiformis ( ) The 2002 sub-sample yielded 2011 live (stained) individuals; 1132 in the μm- and 879 in the N125-μm fraction (Table 1). The most abundant taxa in the complete N63-μm fraction of the assemblage were Globobulimina auriculata (18%), Liebusella goësi (16%), allogromiids (13% including 6% Micrometula hyalostriata), Textularia earlandi (13%), and Stainforthia fusiformis (12%), with Eggerelloides medius, Pullenia osloensis, Reophax fusiformis, Nonionella iridea, and Cassidulina laevigata as common (8 2%) species (Figs. 1 and 2). When considering the two size fraction separately, G. auriculata and L. goësi strongly dominated the larger (N125 μm), whereas allogromiids, T. earlandi, and S. fusiformis dominated the smaller (b63 μm) fraction (Fig. 3). After two years, the stored 2004-sediment had a light gray colour (i.e., no sign of sulphides), and two of the three containers had polychaete tubes protruding up into the overlying water. Live (moving) polychaetes and bivalves were present. The foraminiferal sub-sample had 1275 live (stained) individuals of which 959 occurred in the μm fraction and 316 occurred in the N125-μm fraction. The most common taxa (N2%) either in the or in the assemblage, or in both, are grouped into three categories according to relative abundance (Table 2). Category 1 includes allogromiids, N. iridea, and C. laevigata which nearly had disappeared by 2004 (Table 1). Category 3 includes all other taxa which were abundant both in the and the 2004 assemblage. T. earlandi made up 27% of the complete N63-μm fraction and 36% of the μm fraction in the 2004 data-set. For G. auriculata, the abundance in the complete N63-μm fraction was 10%. Its abundance in the N125-μm fraction was the same as in the 2002-data-set (40%). Category 2 includes Leptohalysis gracilis, Eggerella europeum, Hippocrepinella alba, Trochammina skrumpa, Technitella sp., Melonis barleeanum, Adercotryma wrighti, and Haplophragmoides bradyi, all of which were only recorded with a few individuals in the 2002-assemblage but were common (2 9%) in The seven commonest species made up 76% of the complete (N63 μm) assemblage in both the and in the 2004 data-set. Of these seven, they had six in common whereas the 7th was M. hyalostriata in 2002 and L. gracilis in The similarity in species composition between the complete (N63 μm) and assemblages was 58%. For the sub-fractions, the similarity between the two smaller ( μm) was 56%, whereas that for the larger (N125 μm) was 85%. In the 2002-assemblage, the smaller fraction made up 56% of the assemblage whereas in 2004, the figure had increased to 75%. The 2002 assemblage had 59 species of which 31 were recorded in the stored 2004-assemblage. An additional 8 species were recorded in the latter. Both the and assemblages were dominated by agglutinated taxa but with a higher relative abundance in the latter. Allogromiids made up 13% and 1% of the complete (N63 μm) assemblages respectively. The species diversity indices showed a minor reduction from 2002 to 2004, irrespective of which index was considered, whereas the relative abundance of agglutinated forms increased by about 20% (Table 1).

6 E. Alve / Marine Micropaleontology 76 (2010) The organic-walled rhizarian protist Gromia which is related to the foraminifera was present in both size fractions of both data sets but its abundance relative to the number of foraminifera was more than halved during the two years storage in the dark (Table 1). 4. Discussion 4.1. The culture conditions During two years storage at ambient temperature, no nutrients were added to the cultures and the sediment was exposed to indoor light only for a few minutes per month when items were placed in or collected from the cold-room. This was probably not enough to trigger growth or maintenance of algae (Bente Edvardsen and Wenche Eikrem, pers. com., 2009). A methodological weakness was that no environmental parameters (except temperature) were measured or analysed during the two year period. However, it is likely that the salinity remained constant as the cultures were sealed at all times and the following suggests stable geochemical conditions during the course of the experiment. During the two year storage, bioturbation within the thin sediment-layer (e.g., Hemleben and Kitazato, 1995; Gross, 2002) and oxygen penetration through the culture walls probably prevented the cm thin sediment layers from turning anoxic. Macrofauna was present and there were no signs of sulphide. Lack of deep infaunal space cannot have served as a serious limiting factor as species of Globobulimina (abundant in the present study) are commonly among the deepest recorded infaunal foraminiferal species (e.g., Corliss and Van Weering, 1993; Fontanier et al., 2002) Species responses to absence of freshly produced algae The only food available for the foraminifera during the two years in isolation was food particles already present in the sediment at the time of collection and associated bacteria and degradation products. Still, of the 59 species recorded in the original 2002 assemblage, at least 31 survived and most taxa which were abundant in 2002 were still abundant in 2004 (Fig. 1). Also, the fact that six of the seven most abundant species in 2002 were still the most abundant two years later, show that no dramatic faunal restructuring occurred. Similarity indices and changes in relative abundance of the smaller vs the larger size fraction (Fig. 3) indicate that the faunal response primarily occurred in the smaller species. This moderate response is in contrast to the dramatic faunal change that occurred with the assemblage in the same sediment when the fine fractions containing juveniles only were exposed to simulated shallow-water conditions (Alve and Goldstein, 2010). The most pronounced negative faunal change was seen in the Category 1-species (Table 2) with a strongly reduced relative abundance of the organic-walled allogromiids and a near disappearance of the calcareous N. iridea and C. laevigata (Figs. 2 and 3). The present results are in accordance with the view that these two calcareous species and at least some allogromiids are shallow infaunal taxa, linked to the presence of phytodetritus (possibly different kinds) on the sea floor (e.g., Corliss and van Weering, 1993; Gooday and Hughes, 2002; Gross, 2002; Duchemin et al., 2008). For allogromiids, their relative abundance in the 2002-assemblage is within the range reported for deep-sea assemblages (e.g., Gooday, 1986; Gooday and Hughes, 2002). It seems, in general, that they are less responsive to inputs of fresh organic material than calcareous foraminifera (Gooday, 2002). On the other hand, a species of Tinogullmia (T. riemanni) is a phytoplankton-dwelling form but also occurs in the sediment below (Cornelius and Gooday, 2004). Further, while some hard-shelled species were recorded living down to 30 cm below a marsh surface, allogromiids lived exclusively at the surface (Goldstein et al., 1995). Fatty acid biomarker analyses have shown that another Cassidulina species, C. crassa, feeds selectively on the high quality part of freshly deposited organic matter from phytoplankton bloom events (Suhr and Pond, 2006) and N. iridea seems able to withstand relatively low background organic flux but needs pulsed arrivals of phytodetritus in order to dominate the assemblage (Duchemin et al., 2005, p. 213). The present results show that most Category 1 taxa, although reduced in abundance, can survive for a longer time (here, two years) than the months normally needed between phytoplankton blooms (for survival of deep-sea cultures, see also Hemleben and Kitazato, 1995). There are two potential explanations: 1) that they can survive for at least two years by reducing their metabolism. The quality of settling organic particles is a key factor in understanding temporal variability in benthic metabolic rates (Ståhl et al., 2004); 2) that they can survive on degraded organic material or on bacteria associated with phytodetritus (rather than on the phytodetritus itself) as suggested for Cassidulina teretis (Gooday and Lambshead, 1989), i.e., they have a potentially varied diet. The latter is supported by the fact that the cytoplasm of live C. laevigata may have bright green, orange, shades of brown, or cream colours (Alve unpubl. observations) indicating that it ingests other food items as well as chloroplasts. Species of Allogromia used their pseudopodial networks to harvest bacterial biofilm parcels (Bernhard and Bowser, 1992). A positive response pattern was seen in the Category 2-species (Table 2) for most of which the trophic strategies are not well known. T. earlandi stands out as it became the predominant species (Figs. 1 and 2) following the two years isolation treatment. In addition to the present findings, there are several indications that T. earlandi is an omnivorous opportunist able to feed on and reproduce in response to a wide spectrum of food resources: 1) it grew and reproduced in high numbers when exposed to simulated shallow-water conditions (probably in response to algae and/or bacteria growing when exposed to sun light) following two years of dark isolation (Alve and Goldstein, 2010), 2) it suddenly occurred in large numbers in an oil-treated mesocosm experiment (Ernst et al., 2006), 3) it was one of the predominant species in terrestrial dominated (C:N ratios N30) sediments deposited from turbid melt water in an Alaskan fjord (Ullrich et al., 2009), and 4) it (as Spiroplectinella earlandi) suddenly became the dominant species in an unfed culture (Heinz et al., 2002). Leptohalysis is recorded in organic rich, oxygen-limited sediments influenced by terrestrial plant debris (e.g., Blais-Stevens and Patterson, 1998; discussion in Murray et al., 2003) and Gooday (1996) suggested that Leptohalysis benefitted from degraded phytodetritus or from the associated bacterial populations. Both deep-sea and shallow-water species have been shown to feed on bacteria by deposit feeding and ingestion of bacterial cells (Goldstein and Corliss, 1994). Haplophragmoides bradyi is described as an infaunal species (Gooday 1986), probably implying that it can feed on degradation products as also indicated by the present study. In the Adriatic Sea, Adercotryma wrighti (as A. glomeratum) showed a well-defined subsurface microhabitat as well as a more surficial one (destigter et al., 1998). Adercotryma glomeratum has been described as a species responding positively to phytodetritus (e.g., Gooday, 1988; Heinz et al., 2002; Koho et al., 2008). However, in the deep sea, although a few individuals of A. glomeratum occurred in the phytodetritus, most were recorded in the sediment below (Cornelius and Gooday, 2004). Whether A. wrighti and A. glomeratum have similar feeding strategies is not known. As for Technitella, it seems that Technitella melo was the first benthic foraminifer to colonize a turbidite deposited in the Bay of Biscay, France, in 1999 and that it took advantage of the foodimpoverished conditions in the days following a turbidite deposition (Anschutz et al., 2002). Melonis barleeanum was the only calcareous species in Category 2. A feeding strategy not dependent on regular supply of fresh organic material, as suggested by this finding, also fits with the characterization of this species as a typical infaunal species which does not move up towards the sediment surface following phytodetritus deposition (Koho et al., 2008). The fact that all Category 2-species, except one, are agglutinated support Koho et al.'s (2008) suggestions that calcareous foraminifera

7 72 E. Alve / Marine Micropaleontology 76 (2010) are more sensitive (i.e., respond positively) than agglutinated forms to labile organic matter input, that calcareous taxa require a high quality food source to survive (in the present case some calcareous forms survived for two years), and that agglutinated species in general appear to be less influenced by the lability of phytodetritus, and may have developed other feeding strategies. The Category 3-species were abundant during two years of unfed treatment. Among the most abundant ones, G. auriculata and L. goësi commonly occupy deep infaunal microhabitats in meso-eutrophic environments (e.g., Corliss and van Weering, 1993; destigter et al., 1998; Fontanier et al., 2003; Bubenschikova et al., 2008; Hess and Jorissen, 2009) and species of Globobulimina seem to be able to feed on low quality organic matter (Rathburn and Corliss, 1994; Licari and Mackensen, 2005) as well as fresh phytodetritus (see discussion in Nomaki et al., 2006). Accordingly, Koho et al. (2008) observed that L. goësi (as Bigenerina cylindrica) did not move up towards the sediment surface following phytodetritus deposition, whereas individuals of Globobulimina affinis are reported to migrate up to ingest algae (Nomaki et al., 2005). On the other hand, a simulated phytodetritus sedimentation event revealed almost no response in G. turgida (Sweetman et al., 2009). Feeding in Globobulimina pacifica includes small parcels of sediment and organic detritus and it does not seem to ingest diatoms (Goldstein and Corliss, 1994). The fact that G. auriculata and L. goësi predominated the N125-μm fraction in both data sets (Fig. 3) indicates that they are not dependent on the presence of fresh organic material for survival and that they probably maintained their populations by feeding on refractory and associated organic material already present in the sediment. However, they maintained their populations for two years but did not seem to reproduce (hardly any small individuals of these species were recorded). Of other Category 3 species, S. fusiformis is known to increase its population by a factor of 7 within a month, probably in response to a spring phytoplankton bloom (Gustafsson and Nordberg, 2001). In the present study, the fact that its relative abundance did not decline dramatically when deprived of fresh organic phytodetritus for two years, shows that it is highly capable of maintaining its population by utilizing other, more refractory food resources or degradation products and associated bacteria. A varied diet fits well with its opportunistic life strategy (Alve, 2003) and strongly variable microhabitat (e.g., Collison, 1980; Alve and Bernhard, 1995; Wollenburg and Mackensen, 1998). A varied diet is probably also characteristic of E. medius, P. osloensis, and R. fusiformis Community response and trophic structure It is now commonly realized that the flux of organic carbon to the sea floor is important for the structuring and abundance of benthic foraminiferal assemblages. In what form (i.e., composition and nutritional quality of the organic material) the C org reaches the benthos has often received less attention (discussion in Murray, 2006). Exceptions include controlled laboratory protocols, ultrastructural evidence etc (for review, see Goldstein, 1999) and in recent years, efforts using lipids and labelled food (e.g., Nomaki et al., 2006; Suhr and Pond, 2006; Suhr et al., 2008; Sweetman et al., 2009) have contributed new insight. This is important because environments with similar organic loading may contain organic matter with widely varying degradability and therefore different food value for benthic organisms (Dauwe and Middelburg, 1998). Along the same line, several studies have illustrated that sediment organic carbon content is a weak proxy for food availability (e.g., Alve and Murray, 1997; Levin and Gage, 1998) and we still have limited direct proofs for exactly what the different species eat. Fortunately, there is now a growing body of literature focusing specifically on foraminiferal diets. In the present study, depriving a bathyal Skagerrak slope assemblage of freshly produced algae for two years only caused a moderate change in the faunal composition. Why was the faunal response not more severe? The faunal composition of the original 2002 data-set agrees well with, and extends in an eastward direction, the distribution of the live (stained) G. auriculata-assemblage previously recorded at about 250 to N500 m water depth on parts of the Skagerrak basin slopes (Alve and Murray, 1995, 1997). Furthermore, it is well documented that the Skagerrak basin (max depth 700 m) is the major sink for particles produced and resuspended in the North Sea and that the particulate organic material deposited is highly refractory (e.g., van Weering et al., 1993; Dauwe and Middelburg, 1998; Dauwe et al., 1998; Kröncke et al., 2004). Bottom current- and turbidity measurements indicate a significant lateral transport of suspended particulate matter in the area (Ståhl et al., 2004). At a 280-m station just north of the present sampling site, high input of refractory organic matter yields sediments with 2% total organic carbon content but of low quality (Dauwe et al., 1998). The sediments support a rich, deeply penetrating macrofauna (down to 20 cm) consisting mainly of subsurface deposit feeding animals that are generally adapted to poor food sources. As discussed above, most species in the G. auriculata-assemblage also seem to be able to feed on refractory and associated organic material, illustrating that both the macrofauna and at least the foraminiferal part of the meiofauna reflect the low quality trophic conditions of the habitat. The initial (2002) low abundance of Category 1 species (Table 2, Fig. 3) probably reflects that the relative supply of labile, easily metabolisable organic material to the site is limited, whereas the relative abundance of Category 2 and 3 species reflects a dominance of the more refractory component. The moderate reduction in species diversity (Table 1) over the two years period probably also reflects that overall, sustainment of the Globobulimina-assemblage does not depend on seasonal supply of fresh phytodetritus. In other words, except for loss/reduction of phytodetritus - species, the food sources (including degradation products and bacteria) associated with the refractory material stored in the sediments, seemed able to maintain the overall community structure. Consequently, because the fauna already was adapted to a diet dominated by low quality refractory organic material, a halt in the supply of fresh organic material did not have a profound effect. Still, the number of species present indicates that the available diet is more diverse than we so far are able to prove. Predatory behaviour or symbiosis with chemoautotrophic bacteria may fulfill some nutritional needs in refractory sediment (Dauwe et al., 1998). Carnivory is rarely described in benthic foraminifera. One example is Floresina amphiphaga which is predatory on Amphistegina gibbosa (Hallock and Talge, 1994), and some other examples made Suhr et al. (2008) speculate that carnivory may be more prevalent among foraminifera than previously believed. Whether carnivory is a trophic strategy among some of the present species is left to be seen. Overall, the present study demonstrates how a sedimentary environment dominated by accumulation of refractory organic material (i.e., low quality food) supports a benthic foraminiferal assemblage with a trophic structure that can survive for at least two years without supply of fresh, high quality organic material from the surface waters. The results indicate that in areas dominated by refractory organic material, there is a time lag in the benthic response to reduced organic carbon fluxes. This delayed response probably occurs because it takes time (depending on sediment accumulation rates and biogeochemical pore-water conditions) for organic matter already incorporated in the sediments to degrade/mineralize, leaving the fauna with adequate food for some time (in the present case 2 years) after the supply has ceased. Although the experimental conditions represent an extreme situation which probably hardly occur in nature (perhaps in response to extra terrestrial impacts which may cause collapse of primary production), the approach aids the understanding of more general processes and responses. For example, the present findings have implications for our understanding of processes associated with environmental remediation and faunal recovery following periods of human impact on benthic

8 E. Alve / Marine Micropaleontology 76 (2010) ecosystems (e.g., reduced discharge of nutrients and thereby reduced eutrophication). Finally, the experimental approach (preferably including a better control of environmental parameters) seems to have the potential to further explore how dependant benthic foraminifera are on export production, and thereby the flux of fresh organic material to the sea floor, i.e., how they respond if the flux is strongly reduced or ceases for shorter or longer time periods than demonstrated here Palaeoecological implications In the fossil record, evidence for changes in oceanic primary production has been sought by considering changes in the relative abundance of epifaunal and infaunal forms. Epifaunal taxa are thought to be indicative of oligotrophic, well oxygenated conditions, and the dominance of infaunal taxa are considered indicative of increased primary production and sometimes oxygen depleted conditions. An example is the Cretaceous/Palaeogene boundary. Although no major extinctions of benthic foraminifera have been reported for this boundary, several studies have documented faunal restructuring of their assemblages across it. This has mainly been explained by a collapse of oceanic primary production or collapse of the biological pump transporting food to the benthos, whereas more recent studies argue that the food supply to the deep sea in the Pacific Ocean increased rather than decreased (discussions in Culver, 2003; Thomas, 2007; Alegret and Thomas, 2009, and references therein). The present results show that if a bathyal assemblage living in an environment dominated by refractory organic material experiences a reduction, or even a halt, in the supply of fresh phytodetritus, the faunal response is not necessarily immediate or dramatic. The response depends on the trophic conditions prevailing in the area when the halt occurs, i.e., how sensitive the fauna in focus is to the halt. Also, in the present case, the halt in export production did not reduce the relative abundance of typical deep infaunal species such as G. auriculata, whereas species commonly stimulated by fresh organic material (N. iridea, C. laevigata) nearly disappeared. In the years to come, one of our main challenges for improving the applicability of benthic foraminifera in both recent environmental monitoring and in palaeoecological interpretations studies will be to get a more detailed understanding of their trophic strategies. 5. Conclusions Bathyal (320 m) surface sediments and associated bottom water from the Skagerrak (North Sea) were maintained in closed containers, under dark, ambient temperature conditions for two years (2002 to 2004). No food or nutrients were added. In order to study their response to a halt in the supply of freshly produced phytodetritus, the living (stained) benthic foraminiferal content was examined before and after the two year period. Because no fresh organic material from primary production was available, the foraminifera were left to feed on the organic material present in the sediment at the time of collection, the associated bacteria, and on degradation products. In the original assemblage, the abundance of allogromiids relative to other taxa was comparable to that of the deep sea. Based on changes in relative abundance three species response-categories are defined. Category 1 includes taxa (allogromiids, Nonionella iridea, Cassidulina laevigata), which probably depend on seasonal supply of fresh phytodetritus to maintain their populations and therefore, nearly disappeared. Category 2 includes taxa (e.g., Leptohalysis gracilis, Melonis barleeanum, Adercotryma wrighti, Haplophragmoides bradyi) which increased their abundance from rare (b0.5%) to common (2 9%). They probably have a feeding strategy which is not dependent on regular supply of fresh organic material but utilize refractory organic material and degradation products. Category 3 includes taxa (e.g., Textularia earlandi, Globobulimina auriculata, Liebusella goësi, Stainforthia fusiformis, Eggerelloides medius) that are able to maintain their populations for two years without supply of fresh organic material. They are probably able to decrease their metabolism for a couple of years and, in the same way as the category 2-species, they seem to have a varied diet. Overall, the relative abundance of agglutinated forms increased at the expense of allogromiids and calcareous forms but the faunal response was not dramatic, as six of the seven most abundant species in the 2002 and 2004 assemblages were the same. The similarity in faunal composition between the two data sets was 56% for the smaller ( μm) size fraction and 85% for the larger (N125 μm) fraction showing that the main change occurred among the smaller taxa. Still, the reduction in species diversity was moderate. The results demonstrate that some foraminiferal species have a particular resilience and survival potential to withstand extended periods (here 2 years) without a supply of fresh organic material. In other words, assemblages already adapted to an environment dominated by supply of refractory, organic material stand a better chance to survive periods when oceanic primary production is reduced or ceases for a while, e.g., in response to extraterrestrial impacts. The present experimental approach (but with better control of environmental parameters) may prove useful to test trophic strategies in other foraminiferal taxa. Acknowledgements Without Bruce Corliss' kind gesture to deviate from the original schedule and stop the RV Arne Tisselius in the middle of the Skagerrak to allow sampling to take place, this paper would never have been written. I am also grateful to Lennart Bornmalm for logistical help with the research cruise and to John W. Murray, Bruce Corliss, and an anonymous reviewer for helpful suggestions and comments on the manuscript. The research cruise was supported by NSF Grant OCE Appendix A. Faunal reference list Generic classification follows Loeblich and Tappan (1987). The original descriptions can be found in the Ellis and Messina world catalogue of foraminiferal species on The taxa are listed alphabetically. Adercotryma wrighti Brönnimann and Whittaker, Bolivinellina pseudopunctata (Höglund) = Bolivina pseudopunctata Höglund, Cassidulina laevigata d'orbigny, Eggerella europeum (Christiansen) = Verneuilina europeum Christiansen, Eggerelloides medius (Höglund) = Verneuilina media Höglund, This is not a commonly reported species, probably misidentified as Eggerelloides scaber. Epistominella vitrea Parker, Globobulimina auriculata (Bailey) = Bulimina auriculata Bailey, In the present study, due to high degree of morphological similarity (particularly in smaller individuals), this form also comprises G. turgida (Bailey). The former has priority as it was described prior to the latter. Haplophragmoides bradyi (Robertson) = Trochammina bradyi Robertson, Hippocrepinella alba Heron-Allen and Earland, Leptohalysis gracilis (Kiaer) = Nodulina gracilis Kiaer, 1900 (part.). Liebusella goësi Höglund, Probably the same as Martinottiella sp.1 in destigter et al. (1998), as Bigenerina cylindrica in Koho et al. (2008), and as Clavulina cylindrica in Hess and Jorissen (2009). Melonis barleeanum (Williamson) = Nonionina barleeana Williamson, Micrometula hyalostriata Nyholm, Nonionella iridea Heron-Allen and Earland, 1932.

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