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Revue de micropaléontologie 54 (2011) 87–103

Original article

Foraminifera in the diet of coral reef fish from the lagoonof New Caledonia: Predation, digestion, dispersion

Foraminifères dans le régime alimentaire des poissons récifaux du lagonde 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 Caledoniab 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, Franced Aquarium des Lagons, BP 8185, 98807 Nouméa, New Caledonia

bstract

Marine benthic Foraminifera are abundant and thus represent a potential food source for fish. Previous studies of Foraminifera in fish diets havexamined only small samples, with significant input reported only for a single surface-feeding species of fish. The present study is the first basedn a significant sample (247 fish belonging to 83 species, 291 species of Foraminifera identified from more than 20,000 specimens examined). Itrovides new information on the contribution of Foraminifera to fish diets, and on the impact of fish predation on Foraminifera. The planktonicretomphalus phases, selectively ingested by Pomacentrus amboinensis, were the only significant nutritional input from Foraminifera. Herbivoroussh accidentally ingested living epiphytic Foraminifera, which were still living after digestion, and were defecated, with a significant effect on theirispersion. Carnivorous fish ingested a small number of tests, which were generally altered by the acidic phase of digestion and had no impact onoraminiferal assemblages. Sediment feeders ingested large quantities of empty tests that were released elsewhere, suggesting a possible bias inaleontological interpretations by mixing the thanatocoenoses. Observations on gut contents showed that the fish sometimes fed on a wide rangef food, changing with food availability and individual preferences of fish.

2010 Elsevier Masson SAS. All rights reserved.

eywords: Gut contents; Feeding; Benthic Foraminifera; Epiphytic Foraminifera

ésumé

Les foraminifères benthiques marins sont abondants et représentent une source de nourriture potentielle pour les poissons. Les études précédenteses foraminifères dans le régime alimentaire des poissons se sont appuyées sur de petits nombres d’individus, avec une consommation significativeapportée pour un seul poisson se nourrissant en surface. La présente étude est la première qui se base sur un nombre important d’individus (247

oissons appartenant à 83 espèces, 291 espèces de foraminifères identifiéesouvelles sur la contribution des foraminifères à l’alimentation des poissone foraminifères. Les phases planctoniques Tretomphalus, ingérées sélectivionnel significatif à partir des foraminifères. Les poissons herbivores ingèivants pendant la digestion, et sont déféqués avec un effet significatif surests qui sont généralement altérés au cours de la phase acide de la digestoissons sédimentivores ingèrent de grandes quantités de tests vides qui soaléoécologiques en raison du mélange des thanatocénoses. L’observation dne nourriture très variée, qui peut changer en fonction des disponibilités et

2010 Elsevier Masson SAS. Tous droits réservés.

ots clés : Contenu stomacal ; Nutrition ; Foraminifères benthiques ; Foraminifères

∗ Corresponding author.E-mail address: debenay@wanadoo.fr (J.-P. Debenay).

035-1598/$ – see front matter © 2010 Elsevier Masson SAS. All rights reserved.oi:10.1016/j.revmic.2010.04.001

sur plus de 20 000 individus observés). Elle fournit des informationss et sur l’impact de la prédation par les poissons sur les peuplementsement par Pomacentrus amboinensis, constituent le seul apport nutri-rent accidentellement des foraminifères épiphytes vivants, qui restentleur dispersion. Les poissons carnivores ingèrent un petit nombre deion et n’ont pas d’impact sur les peuplements de foraminifères. Lesnt rejetés ailleurs, suggérant un biais possible dans les interprétationses contenus stomacaux a montré que les poissons consomment parfoisdes préférences individuelles.

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. Introduction

The abundance of benthic Foraminifera in marine environ-ents, where they are often major contributors to meiofaunal

iomass (Murray, 2006), makes them a potential food source forany predators, including fish. However, little is known about

heir position in the trophic structure of marine communitiesince they have been studied mostly from the perspective ofnvironmental monitoring and paleoenvironmental reconstruc-ion.

Some predators have been identified, including nematodesSliter, 1971), polychaetes (Lipps and Ronan, 1974), mol-uscs (Bilyard, 1974; Hickman and Lipps, 1983; Herbert, 1991;hester, 1993; Berry, 1994; Langer et al., 1995; Glover etl., 2003), echinoderms (Mateu, 1968, 1969; Goldbeck et al.,005), arthropods (Rainer, 1992; Wassenberg and Hill, 1993;vavarsson et al., 1993), and fish (Todd, 1961; Hobson andhess, 1973; Daniels and Lipps, 1978; Buzas and Carle, 1979;almer, 1988; Lipps, 1988, Culver and Lipps, 2003). Incidentalredation is common, due to deposit feeders ingesting sediment-welling Foraminifera or herbivorous organisms that ingestpiphytic Foraminifera. Selective predation on Foraminifera isoorly studied and this topic is open to both field and laboratorynalysis (Walker and Goldstein, 1999).

The presence of Foraminifera in the diet of coral reef fishas been reported. For example, Randall (1985) mentionedoraminifera in the diet of Sufflamen fraenatum, Parupeneusultifasciatus and P. pleurostigma from Hawaii, and Sano

t al. (1984) mentioned Foraminifera in the diet of severalsh from Ryukyu Island, including Parupeneus barberinus2% of the gut content) and Acanthurus dussumieri (1%).owever, these studies did not provide information about theature and condition of the Foraminifera. Only two system-tic studies have been carried out on the ingestion of benthicoraminifera by coral reef fish (Todd, 1961; Lipps, 1988),ased on the gut contents of 22 and 37 fish, respectively.hey mostly detected incidental predation. The only notice-ble contribution of Foraminifera in fish diets was reported forhe planktonivorous fish Pranesus pinguis (Hobson and Chess,973).

More research on predation of Foraminifera may improve ournderstanding of trophic structures, but may also provide addi-ional perspective for using Foraminifera in ecological studiesnd paleoenvironmental reconstructions. Ingested Foraminiferaay be transported by fish that move from one area to another

n feeding and defecating, which may bias paleoenvironmentalecords (Langer and Lipps, 2006). During their transit throughhe digestive tract of fish, the calcareous tests of Foraminifera

ay be damaged by the acidic phase of digestion (Hobson andhess, 1973), but gut pH varies between fish with thin-walled

tomachs (mean pH 3.4), fish with thick-walled stomachs (meanH 7.0) (Lobel, 1981) and stomachless fish (around 8.0) (Hornt al., 2006). Moreover, herbivores produce less protease thanarnivores (e.g., Smith, 1980; Chan et al., 2004; Horn et al.,

006), which may lead to the preservation of the foraminiferalytoplasm inside the test, and the dispersion of still livingoraminifera.

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aléontologie 54 (2011) 87–103

On the other hand, predation may have a negative effect onoraminiferal assemblages. For example, the ingestion of about800 Foraminifera m−2 d−1 by the opisthobranch gastropodetusa obtusa may reduce the foraminiferal population (Berry,994). Significant predation pressure on benthic Foraminiferaas also demonstrated in deep-sea scaphopods (Langer et al.,995). Predation by fish has also been considered to have anmpact on Foraminifera (e.g., Palmer, 1988).

This study is based on the gut contents of 247 fish, belong-ng to 83 species. It is the first systematic investigation oforaminifera in such a number and variety of fish. The aimsf this study are:

To provide information on the ingestion and digestion ofForaminifera by fish;To determine the impact of predation on foraminiferal assem-blages;To determine if some fish species could be considered to beselective consumer of Foraminifera;To determine if the consumption of Foraminifera can providesignificant biomass to fish.

In addition to the study of Foraminifera as potential prey ofsh, qualitative observations carried out on the gut content wille presented and briefly discussed.

. Material and methods

Fish were collected over one year (2007–2008) inside andutside the lagoon of New Caledonia near Nouméa (Fig. 1),ither by hook and line or by spear fishing. Fine spears shot withrubber band were used for small species in order to preserve

heir digestive tract. For comparison with Foraminifera from theut contents, the foraminiferal assemblage was investigated inne sample of bottom sediment from Snark reef, where about0 fish were collected.

Two hundred and forty-seven fish belonging to 83 speciesere collected. Since the goal of the paper was primarily to

nvestigate the ingestion of Foraminifera by a number of speciesiving in various environments, we collected only a few individ-als of most species, which provided a low level of replication.n adequate level of replication, however, would be difficult

o reach due to the variation of the diet of the same species inelation to its environment (e.g., Horn et al., 2006) or with foodvailability (e.g., Hobson and Chess, 1978). Choat et al. (2002)oncluded that dietary groupings do not reflect taxonomic rela-ionships. Some authors even consider that meaningful statisticalests cannot be applied within species because of habitat andehavioural variation (Hobson, 1975; Lipps, 1988). Emphasisas made on the common fish Lethrinus genivittatus: 51 indi-iduals were collected for investigating differences in feedingattern among individuals of the same species.

The fish were collected in the morning, placed in a cool box

nd immediately brought back to the laboratory. They were iden-ified using the standard works of Randall (2005) and Laboutend Grandperrin (2000). The entire digestive tract was removed,pened longitudinally and vigorously shaken in saline (1/4 sea

J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 89

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ig. 1. Location of the main areas of collection.ocalisation des principales zones de récolte.

ater, 3/4 tap water). The supernatant was replaced several timesntil all soluble elements were eliminated and the remainingiquid was clear. This method is generally used to collect the par-sites from the digestive tract (Cribb and Bray, 2010). The entireontents were then observed and the constituents qualitativelyisted with general indication on their abundance. Foraminiferaere counted at the same time.Lipps (1988) reported that rose Bengal staining to determine

iving Foraminifera (Walton, 1952) was impossible within theigestive tract of fish owing to the foreign organic matter oftenntroduced in the test. Consequently, rose Bengal staining wassed only to obtain additional information. Whether or not theoraminifera were alive when eaten was estimated mainly from

he test. In one case, Foraminifera were extracted from the diges-ive tract and placed in seawater in order to verify if they stillmitted pseudopodia.

Generally, the guts contained a small number of Foraminiferand all the tests were counted. When fish had ingested a greatuantity of sediment, Foraminifera were separated by flotationn trichloroethylene, and samples with rich assemblages were

plit into equal aliquots to avoid over-counting. Aliquots werexamined to obtain at least 100 specimens, which are signifi-ant for studying the main species present (Fatela and Taborda,002). After counting was completed, the remaining sediment

mmrs

as checked for rare species not found during the counts. Theotal number of tests was evaluated and the relative abundancef each species was calculated.

An attempt was made to estimate the biomass provided tohe fish by the most abundant species of Foraminifera ingested.he biomass was estimated by measuring the volume of the

est and estimating the proportion of cytoplasm in this vol-me. Foraminifera were approximated at simple geometricalhapes: e.g., a cone for Cymbaloporetta, a cylinder for Flo-esina or a cone plus a sphere for Tretomphalus. The dimensionsere measured under a stereoscopic microscope provided with aicrometer eyepiece and the total volume of the test, includingalls and chambers, was calculated. The proportion of cyto-lasm in trochospiral tests was estimated by the calculationf the relative surfaces of the wall sections and chamber sec-ions on serial sections of “Ammonia” provided by Muller-Merz1980), and on both the cross and axial sections of “Ammo-ia” provided by Billman et al. (1980). ImageJ for Macintoshas used (Rasband, 1997–2007). Chambers occupied an aver-

ge of 56.5% of the total surface in the first set of data (n = 3,

in = 50.9, max = 61.5), and 55.5% in the second one (n = 6,in = 46.0, max = 64.5). We thus estimated a chambers/wall

atio of 60% for trochospiral tests. When the benthic phase ofome 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 somefragments) 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) (quelquesfragments) à abondant (***) (constituant l’essentiel du contenu digestif).

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aining a spherical gas-filled float is added to the ventral sidef the test, which converts it into a planktonic Tretomphalushase, often considered as a discrete genus (Myers, 1938). Directeasures on broken spherical chambers of Tretomphalus spp.

llowed us to estimate that the cytoplasm represented 20% ofhe volume of the chamber. Following Korsun et al. (1998), weonsidered that the density of foraminiferal cytoplasm was aboutne. The volume of flattened planispiral tests, such as those oflphidium, was calculated using the formula of Korsun et al.:olume = (diameter)3 × 0.1.

The relative abundance of each taxon comprising at least 4%f the assemblage in one gut content and present in at least fivesh was treated in a Q-mode hierarchical analysis. Fish withewer than 10 Foraminifera in their digestive tract were removedrom the analysis. This analysis was based on Euclidean distanceorrelation coefficients using Ward’s merging criterion, carriedut with Statlab for Macintosh (SLP infoware).

. Results

.1. Food sources

The main food sources identified by direct observation areummarized semi-quantitatively in Fig. 2. Algal feeders such asaso unicornis had their digestive tract full of algal fragmentsith some epiphytic organisms, including micro-gastropods and

mall Foraminifera. A great variety of algae are ingested (Fig. 3),nd fish of the same species may select different algae. Four indi-iduals of Siganus fuscescens, from Snark reef, fed mostly onargassum spp., Dictyota spp. and Lobophora spp., while anndividual from Crouy reef consumed Jania spp. and Dichty-

pteris spp. The availability of these algae was attested to byheir presence in the guts of other herbivorous fish. Comparisonsetween foraminiferal assemblages found in the gut contents oflgal feeders and the foraminiferal assemblages living on the

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ig. 3. Algae collected in the gut content of some herbivorous fish from rare (o) (onllgues récoltées dans le tube digestif de quelques poissons herbivores de rare (o) (que

aléontologie 54 (2011) 87–103 91

lgae they feed on (Debenay and Payri, 2010) did not showignificant similarity.

The diet of Lethrinus genivittatus changed with the locationnd/or the season. At Îlot Canard, the fish preyed on wormspolychaetes) and echinoderms whilst worms were not con-umed elsewhere, and echinoderms were only occasional preytems. The prey also changed from one individual to anotherFig. 4). At Maa Bay, one individual fish clearly selected bry-zoans, another one preyed mostly on echinoderms, and othersngested significant quantities of sediment. Three individual fishad ingested Foraminifera large enough to suggest that theyould be seen and selected by the fish; each individual hadngested a different species of Foraminifera.

.2. Relationships between fish and foraminiferalssemblages

A total of 291 foraminiferal species was recorded in the diges-ive tracts. Most of them were very rare, sometimes representedy only one specimen. Results shown in Fig. 5 consider onlyhe 82 species making up at least 4% of the assemblage andresent in at least five fish. The other species are listed sepa-ately (Appendix A). Fish with fewer than 10 Foraminifera inheir digestive tract were also removed from Fig. 5, leaving 85ndividual fish belonging to 31 species.

The hierarchical clustering carried out on the basis of Fig. 5esulted in the definition of two major clusters, one fish (one indi-idual of Lethrinus genivittatus) remaining isolated (Fig. 6). Therst cluster (A) groups the greatest number of fish. The sedimentample collected for comparison is in this cluster. The secondluster (B) is subdivided into three subclusters. The characteris-

ics of the fish grouped into subcluster B1 are not clear, but theresence of Pararotalia calcar in the digestive tract of most ofhem indicates that they probably feed on algal turfs. The sec-nd subcluster (B2) groups fish that had eaten a great number

y some fragments) to abundant (***) (making up the bulk of the gut content).lques 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 (***) (makingup the bulk of the gut content).C ce desl

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ontenu digestif de Lethrinus genivittatus. Les symboles indiquent l’abondan’essentiel du contenu digestif).

f Rosalina and/or Cymbaloporetta, mostly at their Tretom-halus planktonic reproductive phase; it includes Pomacentrusmboinensis. The third subcluster (B3) groups individuals ofymnocranius euanus and Sufflamen fraenatus that had ingestedmphistegina spp., showing that these fish mainly feed on the

eefs, in deeper areas for Gymnocranius euanus that feeds onhe deep species Amphistegina radiata. Most of the fish speciesave individuals in two subclusters or more.

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composants de rare (o) (quelques fragments) à abondant (***) (constituant

.3. Importance of Foraminifera in the fish diet

Foraminifera were absent from carnivorous species feed-ng mostly on fish, rare and generally badly preserved inpecies feeding mostly on crustaceans and/or polychaetes, more

bundant and generally well preserved in omnivorous and her-ivorous species. Foraminifera may be ingested by accident,long 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 areincluded 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 présentsdans au moins cinq poissons sont notés dans cette figure. Les 85 poissons sélectionnés, appartenant à 31 espèces, contenaient plus de 10 foraminifères dans leurappareil digestif.

94 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103

Fig. 5. (Continued )

J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103 95

Fig. 5. (Continued ).

96 J.-P. Debenay et al. / Revue de micropaléontologie 54 (2011) 87–103

F teringD rarch

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ig. 6. Dendrogram classification of fish produced by Q-mode hierarchical clusendrogramme de classification des poissons obtenus par une classification hié

y fish, which ingest these invertebrates, and may be released

live from the digestive tract of the prey after digestion. Someottom feeding fish such as Acanthurus xanthopterus ingested areat quantity of sediment, including empty foraminiferal tests.

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applied on foraminiferal assemblages.ique ascendante réalisée sur les assemblages de foraminifères.

he highest quantity of living Foraminifera (≈4000), mostly

piphytic species, was found in the gut of a specimen of Acan-hurus dussumieri. The other species that ingested a noticeableumber 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 ofw extraÀ sis. Fv tube

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orm remains. Right: the Foraminifera (Tretomphalus squammosus) have beengauche : dissection du tube digestif d’un spécimen de Pomacentrus amboinen

ers. À droite : les foraminifères (Tretomphalus squammosus) ont été extraits du

is, Siganus fuscescens, and Ctenochaetus striatus. Foraminiferarom the guts of Acanthurus dussumieri, Ctenochaetus striatusnd Siganus fuscescens were well preserved, and still containedytoplasm recognizable by its own colour, and by intense rose

engal staining. The small omnivorous species Pomacentrusmboinensis fed largely and selectively on Foraminifera, butlso on polychaete worms, and its intestinal tract contained alter-

ig. 8. Biomass available in a single specimen of selected species oforaminifera. The mention of Korsun et al. indicates that the cytoplasmic volumeas calculated using Korsun et al. formula.iomasse fournie par un seul spécimen de foraminifère d’espèces sélectionnées.a mention de Korsun et al. indique que le volume cytoplasmique a été calculén utilisant la formule de Korsun et al.

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cted from the digestive tract.indique une accumulation de foraminifères et W une accumulation de restes dedigestif.

ating accumulations of Foraminifera (mostly Tretomphalusquammosus) and worms (Fig. 7). The transparency and colourf the tests of T. squammosus indicated that the Foraminiferaere certainly living when ingested, but the floating chambersere broken, the wall was partially destroyed (Fig. 7), and the

ests were generally devoid of cytoplasm, thus suggesting anctive digestion by the fish.

The individual biomass provided by Foraminifera is verymall (Fig. 8) and a great number of individuals are necessaryo provide a significant nutritional input. For example, the threendividuals of Pomacentrus amboinensis, which seem to selectretomphalus squammosus as a noticeable part of their diet, hadn average of 1600 tests in their digestive tract, which representsbout 0.025 g of biomass.

. Discussion

.1. Food sources

The fish diet observed in this study was sometimes dif-erent from what is reported in the literature. For example,tenochaetus striatus and Siganus doliatus, reported as her-ivorous or detritivorous (Woodland, 1997; Choat et al., 2004;arassou et al., 2008), were omnivorous, ingesting numer-us micro-gastropods or nudibranchs, respectively. Lethrinusenivittatus reported as a “high-speed stalking or lie-in-waitredator that mostly feed on mobile prey such as fish and crus-aceans” (Lo Galbo et al., 2002) fed on a wide range of prey,ncluding molluscs and worms (Sano et al., 1984; Masuda and

llen, 1993; Kulbicki et al., 2005), but also echinoderms andryozoans.

The noticeable spatial (or spatiotemporal) variation in theiet of L. genivittatus is consistent with the plasticity in the diet

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8 J.-P. Debenay et al. / Revue de m

f fish, which are generally opportunistic feeders (e.g., Walker,978; Harmelin-Vivien, 1981; Froese and Pauly, 1990–2008;alini et al., 1994; Kulbicki et al., 2005). However, the inges-

ion of different prey by specimens of L. genivittatus collectedn the same area suggests individual feeding selectivity. It isonsistent with the selectivity of carnivorous fish that do notecessarily feed on the most abundant items (Beukers-Stewartnd Jones, 2004; Kulbicki et al., 2005), but may also be an adap-ation to the competition for food in areas of dense population.o relationship was observed between the size of L. genivittatus

nd its diet, which does not switch from crustaceans to nektons size increases, as reported for other carnivorous species (e.g.,ardinale, 2000; Hanson and Chouinard, 2002; Kulbicki et al.,005). This may be due to the relative homogeneity of the sizef the fish collected.

The differences in algae consumed by Siganus fuscescensollected in different areas (Jania spp. and Dichtyopteris spp.t Récif Crouy compared with Dictyota spp. and Lobophorapp. at Récif Snark; Fig. 3) show that plasticity also exists inhe diet of algal feeders, which may change with the avail-bility of algae. Algal feeders may also select different partsf the thalli. Naso unicornis fed on fresh, non-encrusted thallihile an individual of S. fuscescens preferentially ingested old,

ncrusted thalli of Sargassum spp. This selectivity, together withhe high complexity and heterogeneity in the distribution of epi-hytic Foraminifera (Debenay and Payri, 2010), may explainhe dissimilarity between Foraminifera found in the guts of algaleeders and the assemblages living on the algae.

The hierarchical clustering based on Foraminifera from theigestive tract of fish shows the distinction between fish withifferent feeding behaviours. The presence of fish from theame species in different subclusters indicates intraspecific dif-erences in feeding behaviour.

.2. Importance of Foraminifera in the fish diet

Our results are consistent with the findings of Lipps (1988)hat omnivorous and herbivorous fish take in a large number oforaminifera, whereas carnivores take few Foraminifera. How-ver, calcareous tests can be destroyed in the digestive tract ofsh that have an acidic phase of digestion (Hobson and Chess,973), thus producing a bias.

Pomacentrus amboinensis fed largely and selectively onoraminifera and these occupied a significant part of their diges-

ive tract (Fig. 7). The fact that all the tests were fresh butmpty indicates that the cytoplasm of the Foraminifera wasctively digested. The ingestion of about 0.025 g of foraminiferaliomass is not negligible when compared to the average weightf the fish (about 15 g), and this fish species receives signif-cant nutritional value from the Foraminifera. Conversely, theiomass provided by Foraminifera can be considered as negli-ible for most of the other fish. Moreover, Foraminifera maye significantly selected against by fish, as it is the case for the

arter goby, Gobionellus boleosoma (Carle and Hasting, 1982).

The presence of well-preserved tests with cytoplasm in thehole digestive tract of herbivorous fish indicates that (i) theoraminifera were living when ingested and (ii) the fish do

dcta

aléontologie 54 (2011) 87–103

ot digest their cytoplasm and do not derive any benefit fromhem, even if they are abundant as in Acanthurus dussumieri.he preservation of the calcareous test and cytoplasm may result

rom the absence of acidic phase of digestion, and from a limitedroduction of proteases (Smith, 1980).

The fact that different fish feed on a large number of differentaxa of Foraminifera and sometimes ingest substantial quantitiesf foraminiferal individuals suggests the absence of toxicity oforaminifera against fish (Langer and Bell, 1995). However,wing to the small amount of biomass ingested by most of thesh, it is impossible to conclude on the presence or not of toxins

n Foraminifera.

.3. The role of fish in the dispersion of Foraminifera

Living Foraminifera that pass through the digestive tract ofredators have already been reported. For example, they mayass through the complete digestive tract of the sediment-feedingolothurians without being harmed (Goldbeck et al., 2005). Thisay affect microdistributional processes, ultimately resulting in

n allochthonous dispersion of living Foraminifera within thenvironment. Owing to the higher mobility of fish, they are ableo disperse Foraminifera over larger areas, which should playmajor role during the seasonal periods of growth of algae or

eagrass, and the subsequent colonization by epiphytic com-unities. When it occurs, this process of dispersion by fishay supplement recolonization by species from the sediment

Lobegeier, 2001).The dispersion of empty tests ingested by fish that feed, at

east partly, on the sediment has no impact on the foraminiferalopulation, but may introduce changes in the thanatocoenoses,nd this must be taken into account to avoid bias in paleoenvi-onmental interpretations (Lipps, 1988).

.4. The case of Tretomphalus

Only species of Foraminifera with a planktonic Tretomphaluseproductive phase were selected by fish. At this stage, the tests full of thousands of biflagellate gametes, which provide sig-ificant biomass, and probably have a high nutritional value,ith a small amount of residual protoplasm (Myers, 1938).retomphalus has already been reported to make a noticeableontribution to the diet of the nocturnal surface-feeding fishranesus pinguis from the Marshall Islands (Hobson and Chess,973).

The proliferation of Tretomphalus sp. is reported to be sea-onal, occurring mostly in summer (Myers, 1943; Alldredgend King, 1977; Renon, 1978). In New Caledonia, Pomacentrusmboinensis fed selectively on Tretomphalus during the periodf collection, in autumn (May–June), which shows that a notice-ble number of Tretomphalus may be produced and consumed ateriods other than summer. Seasonal studies will be necessary to

etermine how Pomacentrus amboinensis adapts to the seasonalhanges in its feeding resources, becoming herbivorous whenhe abundance of Foraminifera decreases as reported by Hobsonnd 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 floatchamber 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 loged

t11Katntf

iaiFccp

sphawiIwfft

mbMpd

5

oow4ienbrbfdpiaF

e flottaison dans le même thalle de Chamaedoris sp.

The transformation from the bottom dwelling to the plank-onic Tretomphalus phase requires about 18 hours (Myers,938). Most of the Tretomphalus emerge in the evening (Renon,978), and the greatest number is found at night (Alldredge anding, 1977). The planktonic phase is short-lived (Todd, 1971),

ll of the gametes being discharged within 6 hours from the timehe test arrives at the surface (Myers, 1938). In New Caledo-ia, many Cymbaloporetta (benthic phase) grow in the algalurf made of Chamaedoris spp. where they transform into theree-floating Tretomphalus (Debenay and Payri, 2010) (Fig. 9).

Pomacentrus amboinensis is a territorial fish that protectsts territory against other fish, preventing them to feed on thelgal turf. It feeds by combing the protected algal turf withts teeth, catching the numerous microorganisms (includingoraminifera) that live in the filamentous thalli (Payri, pers.omm.). As it feeds during the day, the Tretomphalus areollected while they live in the algal turf, before becominglanktonic (Fig. 9).

Even if Tretomphalus spp. are selectively preyed on by bothurface- and bottom-feeding fish, the populations of the epi-hytic benthic phases (Rosalina and Cymbaloporetta) are stillighly abundant (Debenay and Payri, 2010) and do not showny negative impact of predation. This observation is consistentith the statement of Coull (1999) that the predator makes little

mpact on meiofauna prey population (including Foraminifera).t is also consistent with the findings of Alve and Olsgard (1999),ho concluded that there was no evidence that the macro-

auna had a negative impact (e.g., through predation) on theoraminiferal colonization pattern. However, this is in contradic-ion with other studies that suggest that predation by macrofauna

otiF

ay significantly reduce the density of foraminiferal assem-lages (Christiansen, 1958; Buzas, 1978, 1982; Berry, 1994;urray and Bowser, 2000). Palmer (1988) showed that fish

redation on Foraminifera reduced their numbers by 19–31%uring experiments in a flume.

. Conclusion

This work is the first systematic investigation on the ingestionf benthic Foraminifera by a relatively large number and varietyf coral reef fish. It confirms the importance of sediment feeders,hich accidentally ingest great quantities of empty tests (up to000), in the dispersion of thanatocoenoses. New informations also given about incidental predators of living Foraminifera,ither herbivorous, which do not digest the Foraminifera or car-ivorous, which ingest and digest insignificant foraminiferaliomass. It is the first report of significant nutritional valueeceived from the selective predation on Foraminifera at itsenthic stage (Tretomphalus spp.) by a fish that protects hiseeding territory (Pomacentrus amboinensis). This selective pre-ation does not seem to significantly impact upon foraminiferalopulations. The presence of epiphytic Foraminifera still aliven the digestive tract of herbivorous fish confirms the prob-ble role of these incidental predators in the dispersion oforaminifera.

This study also shows that coral reef fish may feed

n a wide range of food, changing their diet accordingo availability. Fish from the same population may havendividual preferences in the selection of food, includingoraminifera.

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cknowledgements

The authors are grateful to Napoléon Colombani, Samuelereua, Miguel Clarque, Gerard Mou Tham and John Butscheror assistance in the field, and to Angelo Di Matteo and Cyn-ie Dupoux for laboratory assistance. Dr Claude Payri (IRD,ouméa) provided information about fish behaviour and iden-

ified the algae, and Dr John E. Randall (Bishop Museum,awaii) identified several fish from our photographs. Dominiqueonton (IRD, Nouméa) commented on an early version of theanuscript. Ian Beveridge kindly edited the English.

ppendix A. List of rare foraminiferal species collectedn the digestive tracts.

ffinetrina sp.llogromiidaelveolina quoyimmonia convexamphisorus sauronensismphistegina bicirculatamphistegina lobiferamphistegina papillosamphistegina quoyingulogerina angulosanomalinoides cf. globulosanomalinulla glabratarticulina alticostatarticulina mucronatarticulina pacificasanonella tubuliferasterigerinata mamilla ?ssilina ammonoidesaculogypsina sphaerulataaggina australiensisolivina durrandiiolivina pseudoplicataolivina spp.olivinella elegansolivinella folia ornataolivinella spinosarizalina spathulatarizalina vadescensrizalina sp.ulimina elongataulimina marginataulimina sp.uliminella elegantissimauliminoides williamsonianiusancris auriculusaribeanella philippinensisarterina spiculotestaassidulina laevigataassidulina sp.erebrina clathrataerebrina perforataibicides sp.lavulina multicamerataonicospirillinoides denticulatus

onicospirillinoides semidecoratusonorbella pulvinataornuspira planorbisornuspiramia cf. antillarum

MMMN

aléontologie 54 (2011) 87–103

ppendix A (Continued )

ribroelphidium excavatumribroelphidium sp.ushmanina spiralisycloclypeus carpenteriycloforina quinquecarinataendritina striataentalina communisiscorbinella sp.iscorbinoides australisyocibicides biserialislphidium advenum disparlphidium jensenilphidium limbatumlphidium sp.pistomaroides polystomelloidespistominella pulchraijiella aculeataissurina lucidaissurina sp.lintina bradyanaursenkoina pauciloculataaudryina quadrangularisavelinopsis praegerilabratella sp.landulina laevigatalobigerina sp.lomospira glomeratauttulina reginaaplophragmoides cf. pusillusauerina bradyiauerina divaricataauerina pacificaaynesina depressulaemisphaerammina sp.eterolepa praecinctaeterostegina curvaeterostegina depressaeterostegina operculinoidesomotrema rubra

naequalina affixaabrospira jeffreysiiachlanella bidentataachlanella parkeriagena striata strumosaagenammina pacificaagena sp.amarckina ventricosaenticulina cf. australisenticulina vortexobatula mayorioxostomina costatapertusaassilina inaequalisiliola earlandiiliolinella cf baragwanathiiliolinella circularisiliolinella quinquangulatailiolinella suborbicularisiliolinella webbianailiolinella spillettia limbataimosina echinata

iniacina miniaceaonalysidium acicularisychostomina revertenseoconorbina spp.

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ppendix A (Continued )

eouvigerina porectaodophthalmidium antillarumonion cf. fabumonion pauperatumonionella turgidaubeculina divaricata advenaubeculinella sp.ubeculinopsis queenslandicaummulites cumingiiolina scalariformisarasorites orbitolitoidesaratrochammina simplissimaarrina bradyiatellina advena altiformislacopsilina bradyilanispirinella exigualanoglabratella opercularislanorbulina acervalislotnikovina transversariaoroeponides lateralisseudohauerina occidentalisseudomasilina macilentaseudotriloculina eamesiiseudotriloculina subgranulatayrgo denticulatayrgo cf elongatayrgo oblongayrgo parvaglutayrgo striolatayrgo sp.uinqueloculina bassensisuinqueloculina boscianauinqueloculina cuvierianauinqueloculina debenayiuinqueloculina delicatulauinqueloculina distorqueatauinqueloculina elongatauinqueloculina exculpauinqueloculina lecalvezaeuinqueloculina oblongauinqueloculina parkeriuinqueloculina poeyanauinqueloculina polygonauinqueloculina schlumbergeriuinqueloculina seminulauinqueloculina cf. semireticulosauinqueloculina transversestriatauinqueloculina tropicalisectobolivina raphanaosalina floridanaotaliammina chitinosaagrinella convallariaagrinella spineaahulia barkeriaintclairoides toreutuschackoinella globosachlumbergerina alveoliniformiseptotextularia rugosaiphogenerina striatulaiphonaperta agglutinansiphonaperta anguina arenata

iphonaperta distorqueataiphonaperta horridaiphoniferoides siphoniferaiphonina tubulosa

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aléontologie 54 (2011) 87–103 101

ppendix A (Continued )

iphoninoides echinatusiphotextularia fistulosaorites marginalisphaerogypsina globulapirillina viviparapiroloculina clarapiroloculina communispiroloculina convexapiroloculina subimpressapiroloculina sp.pirosigmoilina bradyipirosigmoilina parripirosigmoilina sp.tomatorbina concentricavratkina australiensisextularia candeianaextularia foliacea occidentalisextularia orbicaextularia pseudogramenextularia rugosaortoplectella rhomboidalisretomphalus clararifarina bradyiriloculina barnardiriloculina earlandiriloculina marshallanariloculina quadratariloculina sp.rochammina hadaiertebralina insignisiesnerella auriculata

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