Revue de micropaléontologie 54 (2011) 87–103 Original article Foraminifera in the diet of coral reef fish from the lagoon of New Caledonia: Predation, digestion, dispersion Foraminifères dans le régime alimentaire des poissons récifaux du lagon de Nouvelle-Calédonie : prédation, digestion, dispersion Jean-Pierre Debenay a,∗,b , Aude Sigura a , Jean-Lou Justine c,d a UR 055 paléotropique, institut de recherche pour le développement (IRD), BP A5, 98848 Nouméa cedex, New Caledonia b 430, chemin de Montplaisir, 34190 Laroque, France c UMR 7138 systématique, adaptation, évolution, Muséum national d’histoire naturelle, case postale 52, 57, rue Cuvier, 75231 Paris cedex 05, France d Aquarium des Lagons, BP 8185, 98807 Nouméa, New Caledonia Abstract Marine benthic Foraminifera are abundant and thus represent a potential food source for fish. Previous studies of Foraminifera in fish diets have examined only small samples, with significant input reported only for a single surface-feeding species of fish. The present study is the first based on a significant sample (247 fish belonging to 83 species, 291 species of Foraminifera identified from more than 20,000 specimens examined). It provides new information on the contribution of Foraminifera to fish diets, and on the impact of fish predation on Foraminifera. The planktonic Tretomphalus phases, selectively ingested by Pomacentrus amboinensis, were the only significant nutritional input from Foraminifera. Herbivorous fish accidentally ingested living epiphytic Foraminifera, which were still living after digestion, and were defecated, with a significant effect on their dispersion. Carnivorous fish ingested a small number of tests, which were generally altered by the acidic phase of digestion and had no impact on foraminiferal assemblages. Sediment feeders ingested large quantities of empty tests that were released elsewhere, suggesting a possible bias in paleontological interpretations by mixing the thanatocoenoses. Observations on gut contents showed that the fish sometimes fed on a wide range of food, changing with food availability and individual preferences of fish. © 2010 Elsevier Masson SAS. All rights reserved. Keywords: Gut contents; Feeding; Benthic Foraminifera; Epiphytic Foraminifera Résumé Les foraminifères benthiques marins sont abondants et représentent une source de nourriture potentielle pour les poissons. Les études précédentes des foraminifères dans le régime alimentaire des poissons se sont appuyées sur de petits nombres d’individus, avec une consommation significative rapportée pour un seul poisson se nourrissant en surface. La présente étude est la première qui se base sur un nombre important d’individus (247 poissons appartenant à 83 espèces, 291 espèces de foraminifères identifiées sur plus de 20 000 individus observés). Elle fournit des informations nouvelles sur la contribution des foraminifères à l’alimentation des poissons et sur l’impact de la prédation par les poissons sur les peuplements de foraminifères. Les phases planctoniques Tretomphalus, ingérées sélectivement par Pomacentrus amboinensis, constituent le seul apport nutritionnel significatif à partir des foraminifères. Les poissons herbivores ingèrent accidentellement des foraminifères épiphytes vivants, qui restent vivants pendant la digestion, et sont déféqués avec un effet significatif sur leur dispersion. Les poissons carnivores ingèrent un petit nombre de tests qui sont généralement altérés au cours de la phase acide de la digestion et n’ont pas d’impact sur les peuplements de foraminifères. Les poissons sédimentivores ingèrent de grandes quantités de tests vides qui sont rejetés ailleurs, suggérant un biais possible dans les interprétations paléoécologiques en raison du mélange des thanatocénoses. L’observation des contenus stomacaux a montré que les poissons consomment parfois une nourriture très variée, qui peut changer en fonction des disponibilités et des préférences individuelles. © 2010 Elsevier Masson SAS. Tous droits réservés. Mots clés : Contenu stomacal ; Nutrition ; Foraminifères benthiques ; Foraminifères épiphytes ∗ Corresponding author. E-mail address: debenay@wanadoo.fr (J.-P. Debenay). 0035-1598/$ – see front matter © 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.revmic.2010.04.001 88 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 1. Introduction The abundance of benthic Foraminifera in marine environments, where they are often major contributors to meiofaunal biomass (Murray, 2006), makes them a potential food source for many predators, including fish. However, little is known about their position in the trophic structure of marine communities since they have been studied mostly from the perspective of environmental monitoring and paleoenvironmental reconstruction. Some predators have been identified, including nematodes (Sliter, 1971), polychaetes (Lipps and Ronan, 1974), molluscs (Bilyard, 1974; Hickman and Lipps, 1983; Herbert, 1991; Chester, 1993; Berry, 1994; Langer et al., 1995; Glover et al., 2003), echinoderms (Mateu, 1968, 1969; Goldbeck et al., 2005), arthropods (Rainer, 1992; Wassenberg and Hill, 1993; Svavarsson et al., 1993), and fish (Todd, 1961; Hobson and Chess, 1973; Daniels and Lipps, 1978; Buzas and Carle, 1979; Palmer, 1988; Lipps, 1988, Culver and Lipps, 2003). Incidental predation is common, due to deposit feeders ingesting sedimentdwelling Foraminifera or herbivorous organisms that ingest epiphytic Foraminifera. Selective predation on Foraminifera is poorly studied and this topic is open to both field and laboratory analysis (Walker and Goldstein, 1999). The presence of Foraminifera in the diet of coral reef fish has been reported. For example, Randall (1985) mentioned Foraminifera in the diet of Sufflamen fraenatum, Parupeneus multifasciatus and P. pleurostigma from Hawaii, and Sano et al. (1984) mentioned Foraminifera in the diet of several fish from Ryukyu Island, including Parupeneus barberinus (2% of the gut content) and Acanthurus dussumieri (1%). However, these studies did not provide information about the nature and condition of the Foraminifera. Only two systematic studies have been carried out on the ingestion of benthic Foraminifera by coral reef fish (Todd, 1961; Lipps, 1988), based on the gut contents of 22 and 37 fish, respectively. They mostly detected incidental predation. The only noticeable contribution of Foraminifera in fish diets was reported for the planktonivorous fish Pranesus pinguis (Hobson and Chess, 1973). More research on predation of Foraminifera may improve our understanding of trophic structures, but may also provide additional perspective for using Foraminifera in ecological studies and paleoenvironmental reconstructions. Ingested Foraminifera may be transported by fish that move from one area to another in feeding and defecating, which may bias paleoenvironmental records (Langer and Lipps, 2006). During their transit through the digestive tract of fish, the calcareous tests of Foraminifera may be damaged by the acidic phase of digestion (Hobson and Chess, 1973), but gut pH varies between fish with thin-walled stomachs (mean pH 3.4), fish with thick-walled stomachs (mean pH 7.0) (Lobel, 1981) and stomachless fish (around 8.0) (Horn et al., 2006). Moreover, herbivores produce less protease than carnivores (e.g., Smith, 1980; Chan et al., 2004; Horn et al., 2006), which may lead to the preservation of the foraminiferal cytoplasm inside the test, and the dispersion of still living Foraminifera. On the other hand, predation may have a negative effect on foraminiferal assemblages. For example, the ingestion of about 4800 Foraminifera m−2 d−1 by the opisthobranch gastropod Retusa obtusa may reduce the foraminiferal population (Berry, 1994). Significant predation pressure on benthic Foraminifera was also demonstrated in deep-sea scaphopods (Langer et al., 1995). Predation by fish has also been considered to have an impact on Foraminifera (e.g., Palmer, 1988). This study is based on the gut contents of 247 fish, belonging to 83 species. It is the first systematic investigation of Foraminifera in such a number and variety of fish. The aims of this study are: • To provide information on the ingestion and digestion of Foraminifera by fish; • To determine the impact of predation on foraminiferal assemblages; • To determine if some fish species could be considered to be selective consumer of Foraminifera; • To determine if the consumption of Foraminifera can provide significant biomass to fish. In addition to the study of Foraminifera as potential prey of fish, qualitative observations carried out on the gut content will be presented and briefly discussed. 2. Material and methods Fish were collected over one year (2007–2008) inside and outside the lagoon of New Caledonia near Nouméa (Fig. 1), either by hook and line or by spear fishing. Fine spears shot with a rubber band were used for small species in order to preserve their digestive tract. For comparison with Foraminifera from the gut contents, the foraminiferal assemblage was investigated in one sample of bottom sediment from Snark reef, where about 50 fish were collected. Two hundred and forty-seven fish belonging to 83 species were collected. Since the goal of the paper was primarily to investigate the ingestion of Foraminifera by a number of species living in various environments, we collected only a few individuals of most species, which provided a low level of replication. An adequate level of replication, however, would be difficult to reach due to the variation of the diet of the same species in relation to its environment (e.g., Horn et al., 2006) or with food availability (e.g., Hobson and Chess, 1978). Choat et al. (2002) concluded that dietary groupings do not reflect taxonomic relationships. Some authors even consider that meaningful statistical tests cannot be applied within species because of habitat and behavioural variation (Hobson, 1975; Lipps, 1988). Emphasis was made on the common fish Lethrinus genivittatus: 51 individuals were collected for investigating differences in feeding pattern among individuals of the same species. The fish were collected in the morning, placed in a cool box and immediately brought back to the laboratory. They were identified using the standard works of Randall (2005) and Laboute and Grandperrin (2000). The entire digestive tract was removed, opened longitudinally and vigorously shaken in saline (1/4 sea J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 89 Fig. 1. Location of the main areas of collection. Localisation des principales zones de récolte. water, 3/4 tap water). The supernatant was replaced several times until all soluble elements were eliminated and the remaining liquid was clear. This method is generally used to collect the parasites from the digestive tract (Cribb and Bray, 2010). The entire contents were then observed and the constituents qualitatively listed with general indication on their abundance. Foraminifera were counted at the same time. Lipps (1988) reported that rose Bengal staining to determine living Foraminifera (Walton, 1952) was impossible within the digestive tract of fish owing to the foreign organic matter often introduced in the test. Consequently, rose Bengal staining was used only to obtain additional information. Whether or not the Foraminifera were alive when eaten was estimated mainly from the test. In one case, Foraminifera were extracted from the digestive tract and placed in seawater in order to verify if they still emitted pseudopodia. Generally, the guts contained a small number of Foraminifera and all the tests were counted. When fish had ingested a great quantity of sediment, Foraminifera were separated by flotation on trichloroethylene, and samples with rich assemblages were split into equal aliquots to avoid over-counting. Aliquots were examined to obtain at least 100 specimens, which are significant for studying the main species present (Fatela and Taborda, 2002). After counting was completed, the remaining sediment was checked for rare species not found during the counts. The total number of tests was evaluated and the relative abundance of each species was calculated. An attempt was made to estimate the biomass provided to the fish by the most abundant species of Foraminifera ingested. The biomass was estimated by measuring the volume of the test and estimating the proportion of cytoplasm in this volume. Foraminifera were approximated at simple geometrical shapes: e.g., a cone for Cymbaloporetta, a cylinder for Floresina or a cone plus a sphere for Tretomphalus. The dimensions were measured under a stereoscopic microscope provided with a micrometer eyepiece and the total volume of the test, including walls and chambers, was calculated. The proportion of cytoplasm in trochospiral tests was estimated by the calculation of the relative surfaces of the wall sections and chamber sections on serial sections of “Ammonia” provided by Muller-Merz (1980), and on both the cross and axial sections of “Ammonia” provided by Billman et al. (1980). ImageJ for Macintosh was used (Rasband, 1997–2007). Chambers occupied an average of 56.5% of the total surface in the first set of data (n = 3, min = 50.9, max = 61.5), and 55.5% in the second one (n = 6, min = 46.0, max = 64.5). We thus estimated a chambers/wall ratio of 60% for trochospiral tests. When the benthic phase of some rotaliid species reaches maturity, a float chamber con- 90 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Fig. 2. Gut contents of the fish species collected in the lagoon of New Caledonia. The symbols indicate the abundance of the components from rare (o) (only some fragments) to abundant (***) (making up the bulk of the gut content). Contenu digestif des espèces de poissons récoltées dans le lagon de Nouvelle-Calédonie. Les symboles indiquent l’abondance des composants de rare (o) (quelques fragments) à abondant (***) (constituant l’essentiel du contenu digestif). J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 taining a spherical gas-filled float is added to the ventral side of the test, which converts it into a planktonic Tretomphalus phase, often considered as a discrete genus (Myers, 1938). Direct measures on broken spherical chambers of Tretomphalus spp. allowed us to estimate that the cytoplasm represented 20% of the volume of the chamber. Following Korsun et al. (1998), we considered that the density of foraminiferal cytoplasm was about one. The volume of flattened planispiral tests, such as those of Elphidium, was calculated using the formula of Korsun et al.: volume = (diameter)3 × 0.1. The relative abundance of each taxon comprising at least 4% of the assemblage in one gut content and present in at least five fish was treated in a Q-mode hierarchical analysis. Fish with fewer than 10 Foraminifera in their digestive tract were removed from the analysis. This analysis was based on Euclidean distance correlation coefficients using Ward’s merging criterion, carried out with Statlab for Macintosh (SLP infoware). 3. Results 3.1. Food sources The main food sources identified by direct observation are summarized semi-quantitatively in Fig. 2. Algal feeders such as Naso unicornis had their digestive tract full of algal fragments with some epiphytic organisms, including micro-gastropods and small Foraminifera. A great variety of algae are ingested (Fig. 3), and fish of the same species may select different algae. Four individuals of Siganus fuscescens, from Snark reef, fed mostly on Sargassum spp., Dictyota spp. and Lobophora spp., while an individual from Crouy reef consumed Jania spp. and Dichtyopteris spp. The availability of these algae was attested to by their presence in the guts of other herbivorous fish. Comparisons between foraminiferal assemblages found in the gut contents of algal feeders and the foraminiferal assemblages living on the 91 algae they feed on (Debenay and Payri, 2010) did not show significant similarity. The diet of Lethrinus genivittatus changed with the location and/or the season. At Îlot Canard, the fish preyed on worms (polychaetes) and echinoderms whilst worms were not consumed elsewhere, and echinoderms were only occasional prey items. The prey also changed from one individual to another (Fig. 4). At Maa Bay, one individual fish clearly selected bryozoans, another one preyed mostly on echinoderms, and others ingested significant quantities of sediment. Three individual fish had ingested Foraminifera large enough to suggest that they could be seen and selected by the fish; each individual had ingested a different species of Foraminifera. 3.2. Relationships between fish and foraminiferal assemblages A total of 291 foraminiferal species was recorded in the digestive tracts. Most of them were very rare, sometimes represented by only one specimen. Results shown in Fig. 5 consider only the 82 species making up at least 4% of the assemblage and present in at least five fish. The other species are listed separately (Appendix A). Fish with fewer than 10 Foraminifera in their digestive tract were also removed from Fig. 5, leaving 85 individual fish belonging to 31 species. The hierarchical clustering carried out on the basis of Fig. 5 resulted in the definition of two major clusters, one fish (one individual of Lethrinus genivittatus) remaining isolated (Fig. 6). The first cluster (A) groups the greatest number of fish. The sediment sample collected for comparison is in this cluster. The second cluster (B) is subdivided into three subclusters. The characteristics of the fish grouped into subcluster B1 are not clear, but the presence of Pararotalia calcar in the digestive tract of most of them indicates that they probably feed on algal turfs. The second subcluster (B2) groups fish that had eaten a great number Fig. 3. Algae collected in the gut content of some herbivorous fish from rare (o) (only some fragments) to abundant (***) (making up the bulk of the gut content). Algues récoltées dans le tube digestif de quelques poissons herbivores de rare (o) (quelques fragments) à abondant (***) (constituant l’essentiel du contenu digestif). 92 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Fig. 4. Gut contents of Lethrinus genivittatus. The symbols indicate the abundance of the components from rare (o) (only some fragments) to abundant (***) (making up the bulk of the gut content). Contenu digestif de Lethrinus genivittatus. Les symboles indiquent l’abondance des composants de rare (o) (quelques fragments) à abondant (***) (constituant l’essentiel du contenu digestif). of Rosalina and/or Cymbaloporetta, mostly at their Tretomphalus planktonic reproductive phase; it includes Pomacentrus amboinensis. The third subcluster (B3) groups individuals of Gymnocranius euanus and Sufflamen fraenatus that had ingested Amphistegina spp., showing that these fish mainly feed on the reefs, in deeper areas for Gymnocranius euanus that feeds on the deep species Amphistegina radiata. Most of the fish species have individuals in two subclusters or more. 3.3. Importance of Foraminifera in the fish diet Foraminifera were absent from carnivorous species feeding mostly on fish, rare and generally badly preserved in species feeding mostly on crustaceans and/or polychaetes, more abundant and generally well preserved in omnivorous and herbivorous species. Foraminifera may be ingested by accident, along with crustaceans and polychaetes, which feed on them, J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 93 Fig. 5. Counts of Foraminifera collected in the gut contents of fish. The 82 species making up at least 4% of the assemblage and present in at least five fish are included in the figure. The 85 fish selected belonging to 31 species contained more than 10 Foraminifera in their digestive tract. Assemblages de foraminifères récoltés dans le contenu digestif des poissons. Les 82 espèces de foraminifères constituant au minimum 4 % de l’assemblage et présents dans au moins cinq poissons sont notés dans cette figure. Les 85 poissons sélectionnés, appartenant à 31 espèces, contenaient plus de 10 foraminifères dans leur appareil digestif. 94 Fig. 5. (Continued ) J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Fig. 5. (Continued ). 95 96 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Fig. 6. Dendrogram classification of fish produced by Q-mode hierarchical clustering applied on foraminiferal assemblages. Dendrogramme de classification des poissons obtenus par une classification hiérarchique ascendante réalisée sur les assemblages de foraminifères. by fish, which ingest these invertebrates, and may be released alive from the digestive tract of the prey after digestion. Some bottom feeding fish such as Acanthurus xanthopterus ingested a great quantity of sediment, including empty foraminiferal tests. The highest quantity of living Foraminifera (≈4000), mostly epiphytic species, was found in the gut of a specimen of Acanthurus dussumieri. The other species that ingested a noticeable number of living Foraminifera were Pomacentrus amboinen- J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 97 Fig. 7. Left: dissection of the digestive tract of one specimen of Pomacentrus amboinensis. F indicates an accumulation of Foraminifera and W an accumulation of worm remains. Right: the Foraminifera (Tretomphalus squammosus) have been extracted from the digestive tract. À gauche : dissection du tube digestif d’un spécimen de Pomacentrus amboinensis. F indique une accumulation de foraminifères et W une accumulation de restes de vers. À droite : les foraminifères (Tretomphalus squammosus) ont été extraits du tube digestif. sis, Siganus fuscescens, and Ctenochaetus striatus. Foraminifera from the guts of Acanthurus dussumieri, Ctenochaetus striatus and Siganus fuscescens were well preserved, and still contained cytoplasm recognizable by its own colour, and by intense rose Bengal staining. The small omnivorous species Pomacentrus amboinensis fed largely and selectively on Foraminifera, but also on polychaete worms, and its intestinal tract contained alter- nating accumulations of Foraminifera (mostly Tretomphalus squammosus) and worms (Fig. 7). The transparency and colour of the tests of T. squammosus indicated that the Foraminifera were certainly living when ingested, but the floating chambers were broken, the wall was partially destroyed (Fig. 7), and the tests were generally devoid of cytoplasm, thus suggesting an active digestion by the fish. The individual biomass provided by Foraminifera is very small (Fig. 8) and a great number of individuals are necessary to provide a significant nutritional input. For example, the three individuals of Pomacentrus amboinensis, which seem to select Tretomphalus squammosus as a noticeable part of their diet, had an average of 1600 tests in their digestive tract, which represents about 0.025 g of biomass. 4. Discussion 4.1. Food sources Fig. 8. Biomass available in a single specimen of selected species of Foraminifera. The mention of Korsun et al. indicates that the cytoplasmic volume was calculated using Korsun et al. formula. Biomasse fournie par un seul spécimen de foraminifère d’espèces sélectionnées. La mention de Korsun et al. indique que le volume cytoplasmique a été calculé en utilisant la formule de Korsun et al. The fish diet observed in this study was sometimes different from what is reported in the literature. For example, Ctenochaetus striatus and Siganus doliatus, reported as herbivorous or detritivorous (Woodland, 1997; Choat et al., 2004; Carassou et al., 2008), were omnivorous, ingesting numerous micro-gastropods or nudibranchs, respectively. Lethrinus genivittatus reported as a “high-speed stalking or lie-in-wait predator that mostly feed on mobile prey such as fish and crustaceans” (Lo Galbo et al., 2002) fed on a wide range of prey, including molluscs and worms (Sano et al., 1984; Masuda and Allen, 1993; Kulbicki et al., 2005), but also echinoderms and bryozoans. The noticeable spatial (or spatiotemporal) variation in the diet of L. genivittatus is consistent with the plasticity in the diet 98 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 of fish, which are generally opportunistic feeders (e.g., Walker, 1978; Harmelin-Vivien, 1981; Froese and Pauly, 1990–2008; Salini et al., 1994; Kulbicki et al., 2005). However, the ingestion of different prey by specimens of L. genivittatus collected in the same area suggests individual feeding selectivity. It is consistent with the selectivity of carnivorous fish that do not necessarily feed on the most abundant items (Beukers-Stewart and Jones, 2004; Kulbicki et al., 2005), but may also be an adaptation to the competition for food in areas of dense population. No relationship was observed between the size of L. genivittatus and its diet, which does not switch from crustaceans to nekton as size increases, as reported for other carnivorous species (e.g., Cardinale, 2000; Hanson and Chouinard, 2002; Kulbicki et al., 2005). This may be due to the relative homogeneity of the size of the fish collected. The differences in algae consumed by Siganus fuscescens collected in different areas (Jania spp. and Dichtyopteris spp. at Récif Crouy compared with Dictyota spp. and Lobophora spp. at Récif Snark; Fig. 3) show that plasticity also exists in the diet of algal feeders, which may change with the availability of algae. Algal feeders may also select different parts of the thalli. Naso unicornis fed on fresh, non-encrusted thalli while an individual of S. fuscescens preferentially ingested old, encrusted thalli of Sargassum spp. This selectivity, together with the high complexity and heterogeneity in the distribution of epiphytic Foraminifera (Debenay and Payri, 2010), may explain the dissimilarity between Foraminifera found in the guts of algal feeders and the assemblages living on the algae. The hierarchical clustering based on Foraminifera from the digestive tract of fish shows the distinction between fish with different feeding behaviours. The presence of fish from the same species in different subclusters indicates intraspecific differences in feeding behaviour. not digest their cytoplasm and do not derive any benefit from them, even if they are abundant as in Acanthurus dussumieri. The preservation of the calcareous test and cytoplasm may result from the absence of acidic phase of digestion, and from a limited production of proteases (Smith, 1980). The fact that different fish feed on a large number of different taxa of Foraminifera and sometimes ingest substantial quantities of foraminiferal individuals suggests the absence of toxicity of Foraminifera against fish (Langer and Bell, 1995). However, owing to the small amount of biomass ingested by most of the fish, it is impossible to conclude on the presence or not of toxins in Foraminifera. 4.3. The role of fish in the dispersion of Foraminifera Living Foraminifera that pass through the digestive tract of predators have already been reported. For example, they may pass through the complete digestive tract of the sediment-feeding holothurians without being harmed (Goldbeck et al., 2005). This may affect microdistributional processes, ultimately resulting in an allochthonous dispersion of living Foraminifera within the environment. Owing to the higher mobility of fish, they are able to disperse Foraminifera over larger areas, which should play a major role during the seasonal periods of growth of algae or seagrass, and the subsequent colonization by epiphytic communities. When it occurs, this process of dispersion by fish may supplement recolonization by species from the sediment (Lobegeier, 2001). The dispersion of empty tests ingested by fish that feed, at least partly, on the sediment has no impact on the foraminiferal population, but may introduce changes in the thanatocoenoses, and this must be taken into account to avoid bias in paleoenvironmental interpretations (Lipps, 1988). 4.2. Importance of Foraminifera in the fish diet 4.4. The case of Tretomphalus Our results are consistent with the findings of Lipps (1988) that omnivorous and herbivorous fish take in a large number of Foraminifera, whereas carnivores take few Foraminifera. However, calcareous tests can be destroyed in the digestive tract of fish that have an acidic phase of digestion (Hobson and Chess, 1973), thus producing a bias. Pomacentrus amboinensis fed largely and selectively on Foraminifera and these occupied a significant part of their digestive tract (Fig. 7). The fact that all the tests were fresh but empty indicates that the cytoplasm of the Foraminifera was actively digested. The ingestion of about 0.025 g of foraminiferal biomass is not negligible when compared to the average weight of the fish (about 15 g), and this fish species receives significant nutritional value from the Foraminifera. Conversely, the biomass provided by Foraminifera can be considered as negligible for most of the other fish. Moreover, Foraminifera may be significantly selected against by fish, as it is the case for the darter goby, Gobionellus boleosoma (Carle and Hasting, 1982). The presence of well-preserved tests with cytoplasm in the whole digestive tract of herbivorous fish indicates that (i) the Foraminifera were living when ingested and (ii) the fish do Only species of Foraminifera with a planktonic Tretomphalus reproductive phase were selected by fish. At this stage, the test is full of thousands of biflagellate gametes, which provide significant biomass, and probably have a high nutritional value, with a small amount of residual protoplasm (Myers, 1938). Tretomphalus has already been reported to make a noticeable contribution to the diet of the nocturnal surface-feeding fish Pranesus pinguis from the Marshall Islands (Hobson and Chess, 1973). The proliferation of Tretomphalus sp. is reported to be seasonal, occurring mostly in summer (Myers, 1943; Alldredge and King, 1977; Renon, 1978). In New Caledonia, Pomacentrus amboinensis fed selectively on Tretomphalus during the period of collection, in autumn (May–June), which shows that a noticeable number of Tretomphalus may be produced and consumed at periods other than summer. Seasonal studies will be necessary to determine how Pomacentrus amboinensis adapts to the seasonal changes in its feeding resources, becoming herbivorous when the abundance of Foraminifera decreases as reported by Hobson and Chess (1978) for planktivorous damselfish. J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 99 Fig. 9. Left: accumulation of living Cymbaloporetta squammosa in the filamentous thallus of Chamaedoris sp. Right: Tretomphalus squammosus with its float chamber in the same thallus of Chamaedoris sp. À gauche : accumulation de Cymbaloporetta squammosa vivants dans le thalle filamenteux de Chamaedoris sp. À droite : Tretomphalus squammosus avec sa loge de flottaison dans le même thalle de Chamaedoris sp. The transformation from the bottom dwelling to the planktonic Tretomphalus phase requires about 18 hours (Myers, 1938). Most of the Tretomphalus emerge in the evening (Renon, 1978), and the greatest number is found at night (Alldredge and King, 1977). The planktonic phase is short-lived (Todd, 1971), all of the gametes being discharged within 6 hours from the time the test arrives at the surface (Myers, 1938). In New Caledonia, many Cymbaloporetta (benthic phase) grow in the algal turf made of Chamaedoris spp. where they transform into the free-floating Tretomphalus (Debenay and Payri, 2010) (Fig. 9). Pomacentrus amboinensis is a territorial fish that protects its territory against other fish, preventing them to feed on the algal turf. It feeds by combing the protected algal turf with its teeth, catching the numerous microorganisms (including Foraminifera) that live in the filamentous thalli (Payri, pers. comm.). As it feeds during the day, the Tretomphalus are collected while they live in the algal turf, before becoming planktonic (Fig. 9). Even if Tretomphalus spp. are selectively preyed on by both surface- and bottom-feeding fish, the populations of the epiphytic benthic phases (Rosalina and Cymbaloporetta) are still highly abundant (Debenay and Payri, 2010) and do not show any negative impact of predation. This observation is consistent with the statement of Coull (1999) that the predator makes little impact on meiofauna prey population (including Foraminifera). It is also consistent with the findings of Alve and Olsgard (1999), who concluded that there was no evidence that the macrofauna had a negative impact (e.g., through predation) on the foraminiferal colonization pattern. However, this is in contradiction with other studies that suggest that predation by macrofauna may significantly reduce the density of foraminiferal assemblages (Christiansen, 1958; Buzas, 1978, 1982; Berry, 1994; Murray and Bowser, 2000). Palmer (1988) showed that fish predation on Foraminifera reduced their numbers by 19–31% during experiments in a flume. 5. Conclusion This work is the first systematic investigation on the ingestion of benthic Foraminifera by a relatively large number and variety of coral reef fish. It confirms the importance of sediment feeders, which accidentally ingest great quantities of empty tests (up to 4000), in the dispersion of thanatocoenoses. New information is also given about incidental predators of living Foraminifera, either herbivorous, which do not digest the Foraminifera or carnivorous, which ingest and digest insignificant foraminiferal biomass. It is the first report of significant nutritional value received from the selective predation on Foraminifera at its benthic stage (Tretomphalus spp.) by a fish that protects his feeding territory (Pomacentrus amboinensis). This selective predation does not seem to significantly impact upon foraminiferal populations. The presence of epiphytic Foraminifera still alive in the digestive tract of herbivorous fish confirms the probable role of these incidental predators in the dispersion of Foraminifera. This study also shows that coral reef fish may feed on a wide range of food, changing their diet according to availability. Fish from the same population may have individual preferences in the selection of food, including Foraminifera. 100 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Acknowledgements Appendix A (Continued ) The authors are grateful to Napoléon Colombani, Samuel Tereua, Miguel Clarque, Gerard Mou Tham and John Butscher for assistance in the field, and to Angelo Di Matteo and Cyndie Dupoux for laboratory assistance. Dr Claude Payri (IRD, Nouméa) provided information about fish behaviour and identified the algae, and Dr John E. Randall (Bishop Museum, Hawaii) identified several fish from our photographs. Dominique Ponton (IRD, Nouméa) commented on an early version of the manuscript. Ian Beveridge kindly edited the English. Cribroelphidium excavatum Cribroelphidium sp. Cushmanina spiralis Cycloclypeus carpenteri Cycloforina quinquecarinata Dendritina striata Dentalina communis Discorbinella sp. Discorbinoides australis Dyocibicides biserialis Elphidium advenum dispar Elphidium jenseni Elphidium limbatum Elphidium sp. Epistomaroides polystomelloides Epistominella pulchra Fijiella aculeata Fissurina lucida Fissurina sp. Flintina bradyana Fursenkoina pauciloculata Gaudryina quadrangularis Gavelinopsis praegeri Glabratella sp. Glandulina laevigata Globigerina sp. Glomospira glomerata Guttulina regina Haplophragmoides cf. pusillus Hauerina bradyi Hauerina divaricata Hauerina pacifica Haynesina depressula Hemisphaerammina sp. Heterolepa praecincta Heterostegina curva Heterostegina depressa Heterostegina operculinoides Homotrema rubra Inaequalina affixa Labrospira jeffreysii Lachlanella bidentata Lachlanella parkeri Lagena striata strumosa Lagenammina pacifica Lagena sp. Lamarckina ventricosa Lenticulina cf. australis Lenticulina vortex Lobatula mayori Loxostomina costatapertusa Massilina inaequalis Miliola earlandi Miliolinella cf baragwanathi Miliolinella circularis Miliolinella quinquangulata Miliolinella suborbicularis Miliolinella webbiana Miliolinella sp Millettia limbata Mimosina echinata Miniacina miniacea Monalysidium acicularis Mychostomina revertens Neoconorbina spp. Appendix A. List of rare foraminiferal species collected in the digestive tracts. Affinetrina sp. Allogromiidae Alveolina quoyi Ammonia convexa Amphisorus sauronensis Amphistegina bicirculata Amphistegina lobifera Amphistegina papillosa Amphistegina quoyi Angulogerina angulosa Anomalinoides cf. globulosa Anomalinulla glabrata Articulina alticostata Articulina mucronata Articulina pacifica Asanonella tubulifera Asterigerinata mamilla ? Assilina ammonoides Baculogypsina sphaerulata Baggina australiensis Bolivina durrandii Bolivina pseudoplicata Bolivina spp. Bolivinella elegans Bolivinella folia ornata Bolivinella spinosa Brizalina spathulata Brizalina vadescens Brizalina sp. Bulimina elongata Bulimina marginata Bulimina sp. Buliminella elegantissima Buliminoides williamsonianius Cancris auriculus Caribeanella philippinensis Carterina spiculotesta Cassidulina laevigata Cassidulina sp. Cerebrina clathrata Cerebrina perforata Cibicides sp. Clavulina multicamerata Conicospirillinoides denticulatus Conicospirillinoides semidecoratus Conorbella pulvinata Cornuspira planorbis Cornuspiramia cf. antillarum J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Appendix A (Continued ) Appendix A (Continued ) Neouvigerina porecta Nodophthalmidium antillarum Nonion cf. fabum Nonion pauperatum Nonionella turgida Nubeculina divaricata advena Nubeculinella sp. Nubeculinopsis queenslandica Nummulites cumingii Oolina scalariformis Parasorites orbitolitoides Paratrochammina simplissima Parrina bradyi Patellina advena altiformis Placopsilina bradyi Planispirinella exigua Planoglabratella opercularis Planorbulina acervalis Plotnikovina transversaria Poroeponides lateralis Pseudohauerina occidentalis Pseudomasilina macilenta Pseudotriloculina eamesii Pseudotriloculina subgranulata Pyrgo denticulata Pyrgo cf elongata Pyrgo oblonga Pyrgo parvagluta Pyrgo striolata Pyrgo sp. Quinqueloculina bassensis Quinqueloculina bosciana Quinqueloculina cuvieriana Quinqueloculina debenayi Quinqueloculina delicatula Quinqueloculina distorqueata Quinqueloculina elongata Quinqueloculina exculpa Quinqueloculina lecalvezae Quinqueloculina oblonga Quinqueloculina parkeri Quinqueloculina poeyana Quinqueloculina polygona Quinqueloculina schlumbergeri Quinqueloculina seminula Quinqueloculina cf. semireticulosa Quinqueloculina transversestriata Quinqueloculina tropicalis Rectobolivina raphana Rosalina floridana Rotaliammina chitinosa Sagrinella convallaria Sagrinella spinea Sahulia barkeri Saintclairoides toreutus Schackoinella globosa Schlumbergerina alveoliniformis Septotextularia rugosa Siphogenerina striatula Siphonaperta agglutinans Siphonaperta anguina arenata Siphonaperta distorqueata Siphonaperta horrida Siphoniferoides siphonifera Siphonina tubulosa Siphoninoides echinatus Siphotextularia fistulosa Sorites marginalis Sphaerogypsina globula Spirillina vivipara Spiroloculina clara Spiroloculina communis Spiroloculina convexa Spiroloculina subimpressa Spiroloculina sp. Spirosigmoilina bradyi Spirosigmoilina parri Spirosigmoilina sp. Stomatorbina concentrica Svratkina australiensis Textularia candeiana Textularia foliacea occidentalis Textularia orbica Textularia pseudogramen Textularia rugosa Tortoplectella rhomboidalis Tretomphalus clara Trifarina bradyi Triloculina barnardi Triloculina earlandi Triloculina marshallana Triloculina quadrata Triloculina sp. Trochammina hadai Vertebralina insignis Wiesnerella auriculata 101 References Alldredge, A.L., King, J.M., 1977. Distribution, abundance, and substrate preferences of demersal reef zooplankton at Lizard Island Lagoon, Great Barrier Reef. Marine Biology 41, 317–333. Alve, E., Olsgard, F., 1999. Benthic foraminiferal colonization in experiments with Cu-contaminated sediments. Journal of Foraminiferal Research 29, 186–195. Berry, A.J., 1994. Foraminiferal prey in the annual life-cycle of the predatory opistobranch gastropod Retusa obtusa (Montagu). Estuarine Coastal and Shelf Science 38, 603–612. Beukers-Stewart, B.D., Jones, G.P., 2004. The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish. Journal of Experimental Marine Biology and Ecology 299, 155–184. Billman, H., Hottinger, L., Oesterle, H., 1980. Neogene to recent rotaliid Foraminifera from the Indopacific Ocean; their canal system, their classification and their stratigraphic use. Schweizerische Paläontologische Abhandlungen 101, 71–113. Bilyard, G.R., 1974. The feeding habits and ecology of Dentalium entale stimpsoni Henderson (Mollusca; Scaphopoda). Veliger 17, 126–138. Buzas, M.A., 1978. Foraminifera as prey for benthic deposit feeders: results of predator exclusion experiments. Journal of Marine Research 36, 617–625. Buzas, M.A., 1982. Regulation of foraminiferal densities by predation in the Indian River, Florida. Journal of Foraminiferal Research 12, 66–71. Buzas, M.A., Carle, K.J., 1979. Predators of Foraminifera in the Indian River, Florida. Journal of Foraminiferal Research 9, 336–340. Carassou, L., Kulbicki, M., Nicola, T.J., Polunin, N.V., 2008. Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, southwest Pacific. Aquatic Living Resources 21, 1–12. 102 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 Cardinale, M., 2000. Ontogenetic diet shifts of bull-rout, Myoxocephalus scorpius (L.), in the south-western Baltic Sea. Journal of Applied Ichthyology 16, 231–239. Carle, K.J., Hasting, P.A., 1982. Selection of meiofaunal prey by the Darter Goby, Gobionellus boleosoma (Gobiidae). Estuaries 5, 316–318. Chan, A.S., Horn, M.H., Dickson, K.A., Gawlicka, A., 2004. Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat. Journal of Fish Biology 65, 848–858. Chester, C.M., 1993. Comparative feeding biology of Acteocina canaliculata (Say, 1826) and Haminoea solitaria (Say, 1822) (Opistobranchia, Cephalaspidea). American Malacological Bulletin 10, 93–101. Choat, J.H., Clements, K.D., Robbins, W.D., 2002. The trophic status of herbivorous fishes on coral reefs 1: Dietary analyses. Marine Biology 140, 613–623. Choat, J.H., Robbins, W.D., Clements, K.D., 2004. The trophic status of herbivorous fishes on coral reefs. II. Food processing modes and trophodynamics. Marine Biology 145, 445–454. Christiansen, B., 1958. The foraminiferal fauna in the Drobak sound in the Oslo fjord (Norway). Nytt Magasin Zoology 6, 5–91. Coull, B.C., 1999. Role of meiofauna in estuarine soft-bottom habitats. Australian Journal of Ecology 24, 327–343. Cribb, T. H., Bray, R. A., 2010. Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76, 1–7. Culver, S.J., Lipps, J.H., 2003. Predation on and by Foraminifera. In: Kelley, P., Kowalewski, M., Hansen, T. (Eds.), Predation in the Fossil Record. Kluwer Academic/Plenum Publishers, New York, pp. 7–32. Daniels, A.J., Lipps, J.H., 1978. Predation on Foraminifera by Antarctic fish. Journal of Foraminiferal Research 8, 110–113. Debenay, J.-P., Payri, C., 2010. Epiphytic foraminiferal assemblages on macroalgae from the lagoon of New Caledonia. Journal of Foraminiferal Research 40, 36–60. Fatela, F., Taborda, R., 2002. Confidence limits of species proportions in microfossil assemblages. Marine Micropaleontology 45, 169–174. Froese, R., Pauly, D. (Eds.), 1990–2008. FishBase. World Wide Web electronic publication. Available from: http://www.fishbase.org (accessed 20.10.08). Glover, E., Taylor, J., Whittaker, J., 2003. Distribution, abundance and foraminiferal diet of an intertidal scaphopod, Laevidentalium lubricatum, around the Burrup Peninsula, Dampier, Western Australia. In: Wells, F.E., Walker, D.I., Jones, D.S. (Eds.), The Marine Flora and Fauna of Dampier, Western Australia. Western Australian Museum, Perth, pp. 225–240. Goldbeck, E.J., Houben, C., Langer, M., 2005. Survival of Foraminifera in the gut of holothuroids from Elba Island (Mediterranean Sea). Revue de Micropaléontologie 48, 169–174. Hanson, J.M., Chouinard, G.A., 2002. Diet of Atlantic cod in the southern Gulf of St Lawrence as an index of ecosystem change, 1959–2000. Journal of Fish Biology 60, 902–992. Harmelin-Vivien, M.L., 1981. Trophic relationships of reef fishes in Tulear (Madagascar). Oceanologica Acta 4, 365–374. Herbert, D.G., 1991. Foraminiferivory in a Puncturella (Gastropoda: Fissurellidae). Journal of Molluscan Studies 57, pp. 137–129. Hickman, C., Lipps, J.H., 1983. Foraminiferivory: Selective ingestion of Foraminifera and test alterations produced by the neogastropod Olivella. Journal of Foraminiferal Research 13, 108–114. Hobson, E.S., 1975. Feeding patterns among tropical reef fishes. American Scientist 63, 382–392. Hobson, E.S., Chess, J.R., 1973. Feeding oriented movements of the atherinid fish Pranesus pinguis at Majuro atoll, Marshall Islands. Fishery Bulletin 71, 777–786. Hobson, E.S., Chess, J.R., 1978. Trophic relationships among fishes and plankton in the lagoon of Enewetak Atoll, Marshall Islands. Fishery Bulletin 76, 133–153. Horn, M.H., Gawlicka, A.K., German, D.P., Logothetis, E.A., Cavanagh, J.W., Boyle, K.S., 2006. Structure and function of the stomachless digestive system in three related species of New World silverside fishes (Atherinopsidae) representing herbivory, omnivory, and carnivory. Marine Biology 149, 1237–1245. Korsun, S., Hald, M., Panteleeva, N., Tarasov, G., 1998. Biomass of Foraminifera in the St. Anna Trough, Russian Arctic continental margin. Sarsia 83, 419–431. Kulbicki, M., Bozec, Y.-M., Labrosse, P., Letourneur, Y., Mou-Tham, G., Wantiez, L., 2005. Diet composition of carnivorous fishes from coral reef lagoons of New Caledonia. Aquatic Living Resources 18, 231–250. Laboute, P., Grandperrin, R., 2000. Poissons de Nouvelle-Calédonie. Éditions Catherine Ledru, Nouméa, pp. 519. Langer, M.R., Bell, C.J., 1995. Toxic Foraminifera: Innocent until proven guilty. Marine Micropaleontology 24, 205–214. Langer, M.R., Lipps, J.H., 2006. Assembly and persistence of Foraminifera in introduced mangroves on Moorea. French Polynesia. Micropaleontology 52, 343–355. Langer, M.R., Lipps, J.H., Moreno, G., 1995. Predation on Foraminifera by the dentaliid deep-sea scaphopod Fissidentalium megathyris. Deep-Sea Research 42, 849–857. Lipps, J.H., 1988. Predation on Foraminifera by coral reef fish: taphonomic and evolutionary implications. Palaios 3, 1–12. Lipps, J.H., Ronan Jr., T.E., 1974. Predation on Foraminifera by the polychaete worm Diopatra. Journal of Foraminiferal Research 4, 139–143. Lobegeier, M.K., 2001. Foraminiferal assemblages and their contribution to carbonate sediment, Green Island Reef, Great Barrier Reef Province. In: Collen, J., Rodda, P. (Eds.), SOPAC Miscellaneous Report 445, pp. 30–31. Lobel, P.S., 1981. Trophic biology of herbivorous reef fishes: alimentary pH and digestive capabilities. Journal of Fish Biology 19, 365–397. Lo Galbo, A.M., Carpenter, K.E., Reed, D.L., 2002. Evolution of trophic types in emperor fishes (Lethrinus, Lethrinidae, Percoidei) based on Cytochrome b gene sequence variation. Journal of Molecular Evolution 54, 754–762. Masuda, H., Allen, G.R., 1993. Meeresfische der Welt - Groß-Indopazifische Region. Tetra Verlag, Herrenteich, Melle, pp. 528. Mateu, G., 1968. Contribución al conocimiento de los foraminíferos que sirven de alimentos a las holoturias. Boletín de la Sociedad de Historia Natural de Baleares 14, 5–17. Mateu, G., 1969. Foraminíferos del contenido gástrico del Spatangus purpureus O.F. Muller y su degradación protoplasmática a travès del aparato digestivo de este equinido. Boletín de la Sociedad de Historia Natural de Baleares 15, 75–84. Myers, E.H., 1938. The present state of our knowledge concerning the life cycle of the Foraminifera. Zoology 24, 10–17. Myers, E.H., 1943. Biology, ecology and morphogenesis of a pelagic Foraminifera. Stanford University Publications, University Series, Biological Sciences 9, pp. 5–38. Müller-Merz, E., 1980. Structural analysis of selected rotaloiid Foraminifera. Schweizerische Paläontologische Abhandlungen 101, 5–70. Murray, J.W., 2006. Ecology and applications of benthic Foraminifera. Cambridge University Press, Cambridge, UK, pp. 426. Murray, J.W., Bowser, S.S., 2000. Mortality, protoplasm decay rate, and reliability of staining techniques to recognize ‘living’ Foraminifera: a review. Journal of Foraminiferal Research 30, 66–70. Palmer, M.A., 1988. Epibenthic predators and marine meiofauna: separating predation, disturbance, and hydrodynamic effects. Ecology 69, 1251–1259. Rainer, S.F., 1992. Diet of prawns from the continental slope of North-Western Australia. Bulletin of Marine Science 50, 258–274. Randall, J.E., 1985. Guide to Hawaiian reef fishes. Harrowood Books, Newtown Square, PA 19073, pp. 74. Randall, J.E., 2005. Reef and shore fishes of the South Pacific. New Caledonia to Tahiti and the Pitcairn Islands. University of Hawaii Press, Honolulu, pp. 707. Rasband, W.S., 1997–2007. ImageJ. U.S. National Institutes of Health, Bethesda, Maryland, USA. Available from: http://rsb.info.nih.gov/ij/ (accessed 15.05.08). Renon, J.-P., 1978. Un cycle annuel du zooplancton dans un lagon de Tahiti. Cahiers ORSTOM, série Océanographie 16, pp. 63–85. Salini, J.P., Blaber, S.J.M., Brewer, D.T., 1994. Diets of trawled predatory fish of the Gulf of Carpentaria, Australia, with particular reference to preda- J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 tion on prawns. Australian Journal of Marine and Freshwater Research 45, 397–411. Sano, M., Shimizu, M., Nose, Y., 1984. Food habits of teleostean reef fishes in Okinawa Island, southern Japan, 25. University of Tokyo Press, Tokyo, Bulletin, pp. 128. Sliter, W.V., 1971. Predation on benthic Foraminifera. Journal of Foraminiferal Research 1, 20–28. Smith, L.S., 1980. Digestion in Teleost Fishes. In: Chow, K.W. (Ed.), Fish feed technology: Lectures presented at the FAO/UNDP Training Course in Fish Feed Technology, College of Fisheries, University of Washington, Seattle, Washington, U.S.A., 9 October–15 December 1978. Aquaculture Development and Coordination Programme ADCP/REP/80/11. Available from: http://www.fao.org/docrep/X5738E/x5738e02.htm (accessed 6.10.08). Svavarsson, J., Gudmundsson, G., Brattegard, T., 1993. Feeding by Asellote isopods (Crustacea) on Foraminifers (Protozoa) in the deep sea. Deep-Sea Research, Part I-Oceanographic Research Papers 40, pp. 1225–1239. Todd, R., 1961. Foraminifera from Onotoa Atoll, Gilbert Islands. United States Geological Survey, Professional Paper P0354-H, pp. 171–191. 103 Todd, R., 1971. Tretomphalus (Foraminifera) from Midway. Journal of Foraminiferal Research 1, 162–169. Walker, M.H., 1978. Food and feeding habits of Lethrinus chrysostomus Richardson (Pisces: Perciformes) and other Lethrinidae on the Great Barrier Reef. Australian Journal of Marine and Freshwater Research 29, 623–630. Walker, S.E., Goldstein, S.T., 1999. Taphonomic tiering: experimental field taphonomy of molluscs and Foraminifera above and below the sedimentwater interface. Palaeogeography, Palaeoclimatology, Palaeoecology 149, 227–244. Walton, W.R., 1952. Techniques for recognition of living Foraminifera. Contribution from the Cushman Foundation 3, 56–60. Wassenberg, T., Hill, B., 1993. Diet and feeding behaviour of juvenile and adult banana prawns Penaeus meguiensis in the Gulf of Carpentaria, Australia. Marine Ecology Progress Series 94, 287–295. Woodland, D., 1997. Siganidae. Spinefoots. Rabbitfishes. In: Carpenter, K.E., Niem, V. (Eds.), FAO Identification Guide for Fishery Purposes. The Western Central Pacific, pp. 3627–3650.