Wood-based diet and gut microflora of a galatheid crab associated with Pacific deep-sea wood falls

Mar Biol (2009) 1562421ndash2439

DOI 101007s00227-009-1266-2

ORIGINAL PAPER

Wood-based diet and gut microXora of a galatheid crab associated with PaciWc deep-sea wood falls

Caroline Hoyoux middot Magali Zbinden middot Sarah Samadi middot Franccediloise Gaill middot Philippe Compegravere

Received 18 August 2008 Accepted 19 July 2009 Published online 16 September 2009copy Springer-Verlag 2009

Abstract Wood falls in the deep sea have recentlybecome the focus of studies showing their importance asnutrients on the deep-sea Xoor In such environments Crus-taceans constitute numerically the second-largest groupafter Mollusks Many questions have arisen regarding theirtrophic role therein A careful examination of the feedingappendages gut contents and gut lining of Munidopsisandamanica caught with wood falls revealed this species asa truly original detritivorous species using wood and thebioWlm covering it as two main food sources Comparingindividuals from other geographic areas from substrates notreported highlights the galatheid crab as specialist of refrac-tory substrates especially vegetal remains M andamanicaalso exhibits a resident gut microXora consisting of bacteriaand fungi possibly involved in the digestion of wood frag-ments The results suggest that Crustaceans could be full-Xedged actors in the food chains of sunken-wood ecosys-tems and that feeding habits of some squat lobsters could bediVerent than scavenging

Introduction

Today wood falls are the focus of much research and manyoceanographic cruises They are regarded as sulWde-richreducing environments (H2S gt 50 M Smith et al 2003)along with whale falls hydrothermal vents and cold seepsWood falls are also seen as huge unexpected food sourceson the deep-sea Xoor possibly having fundamental impor-tance in the nutritional ecology of deep oceans (Cayreacute andRicher de Forges 2002 Smith et al 2003 Palacios et al2006) Twenty-Wve years after publishing the Wrst detailedlists of species associated to deep-sea wood falls by Turner(1977) and WolV (1979) the BOA1 cruise report (Samadiet al 2005) showed that sunken wood ecosystems support arichly diversiWed fauna of macroinvertebrates Mollusksform the Wrst group in terms of both diversity and number ofindividuals represented mainly by wood-borer teredinidbivalves as well as by mytilids and limpets Wrmly attachedto the wood The group has received a careful attention sincethe 1980s in the description of the animal communities (egMarshall 1985 1988 Kiel and Goedert 2006a b Pailleretet al 2006) as well as in the study of the impressive taxo-nomic diversity of mussels (Samadi et al 2007 Lorion et al2009) Moreover the phylogenetic relationships amongwood- bone- vent- and seep-associated mussels led to pro-pose the ldquostepping stonesrdquo hypothesis for the colonization ofthe deep-sea reducing environments (see Smith et al 1989Distel et al 2000) Crustaceans constitute the second-largestzoological group in deep-sea wood falls with many speciesof decapods as galatheid squat lobsters pagurid hermit crabsand thalassinid shrimps as well as with species of amphi-pods and isopods Apart from their taxonomies almost noth-ing else is known about these crustaceans

Among the decapods the squat lobster Munidopsisandamanica MacGilchrist 1905 is numerically one of the

Communicated by S A Poulet

C Hoyoux (amp) middot P CompegravereLaboratoire de Morphologie fonctionnelle et eacutevolutive Uniteacute de Morphologie Ultrastructurale Universiteacute de Liegravege Alleacutee de la Chimie 3 4000 Liegravege Belgiume-mail CarolineHoyouxulgacbe

M Zbinden middot F GaillUMR 7138 CNRS Universiteacute Pierre et Marie Curie 72252 Paris Cedex 05 France

S SamadiUMR 7138 UPMC-IRD-MNHN-CNRS CP 26 57 Rue Cuvier Museacuteum National drsquoHistoire Naturelle 75231 Paris cedex 05 France

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2422 Mar Biol (2009) 1562421ndash2439

most represented species Several recent cruises (BOA1-2005 SantoBOA-2006 SalomonBOA3-2007) have con-Wrmed its regular association to deep-sea wood fallsIndividuals are commonly found on the surface of thesunken wood pieces However nothing is known about itsdiet and trophic dependency to wood or to the wood fallecosystem Does it feed directly on wood or does it scavengeor practice predation on other organisms associated to itIn addition since sunken woods are not only refractorysubstrates (ie containing cellulose lignin) but alsoreducing chemosynthetic-based ecosystems does M and-amanica realize symbiotic associations with microorgan-isms either to digest wood or to exploit reducingcompounds as energy sources Is it speciWcally associatedto sunken wood or not Indeed M andamanica were pre-viously collected in other locations and perhaps on othersubstrates (not reported) in the Andaman Sea along thewest coast of Sumatra and in the waters of the Moluccasthe Philippines the South China Sea (Baba 1988) Taiwan(Wu et al 1998) Indonesia the Solomon Islands NewCaledonia and the Vanuatu and Fiji Islands at depths of333ndash1598 m (Macpherson 2007)

On the other hand the genus Munidopsis Whiteaves1874 is distributed worldwide in all deep-sea habitats andcommonly found living deeper than 500 m and down to2000 m on continental slopes and abyssal plains (Baba1988 2005 Macpherson and Segonzac 2005) Interest-ingly their presence is also reported in vent- and cold-seep communities (Williams 1988 Hashimoto et al 1995Chevaldonneacute and Olu 1996) as well as on whale andwood falls (Bennett et al 1994 GoVredi et al 2004Samadi et al 2005) Although few studies focused ontheir diet they are commonly thought to be scavengerswhile their feeding habits are much diversiWed and notclearly established Some species from hydrothermalvents such as M marionis M acutispina and anotherMunidopsis sp (complete name is not mentioned) wouldbe predators or scavengers (Chevaldonneacute and Olu 1996Macavoy et al 2008a) while M alvisca M subsquamosaM geyeri and another Munidopsis sp appeared to have amixed diet composed of organic debris of the sedimentpolychaetes limpets crab larvae and would also grazethe bacteria of the bioWlms (Van Dover and Lichtwardt1986 Escobar-Briones et al 2002 Micheli et al 2002Phleger et al 2005) Nothing is reported about the diet ofM cascadia M yaquiensis M verrilli and M quadratathat are found associated to whale carcasses (Williamset al 2000) However experimental studies showed thatM crassa and another Munidopsis sp would be scaveng-ers of bone remnants (Janszligen et al 2000 Kemp et al2006 Macavoy et al 2008b) In addition other species(M serricornis M sarissa) were found in gorgonians orsponges and would perhaps feed on the organic matter or

even on the tissues of these organisms (Macpherson andSegonzac 2005)

The aim of the present study was to describe and specifythe diet of the M andamanica specimens associated towood falls from Vanuatu in order to have a better under-standing about the role they play in these particular ecosys-tems In addition comparisons with specimens from Wveother geographic areas were carried out to determinewhether M andamanica is a specialist of sunken woods oran opportunistic generalist with various food sources ascommonly admitted for squat lobsters

We also looked for microorganisms in the digestivetract in order to determine whether the specimens ofM andamanica have developed digestive andor chemo-synthetic microbial symbioses Indeed previous studieshave highlighted chemosynthetic bacterial symbioses inthe branchial tissues of bivalves from wood falls (Disteland Roberts 1997 Gros and Gaill 2007 Duperron et al2008) and the digestion of vegetal cells often implies aheterotrophic gut microXora providing the host with exo-enzymes for metabolizing constituents of plant cell wallssuch associations are well known in xylophagous insects(Foglesong et al 1975 Potrikus and Breznak 1977Bayon 1980 Bignell 1984 Margulis et al 1990 Zurekand Keddie 1998 Dolan 2001)

Materials and methods

Biological material

Specimens of M andamanica associated to wood fallswere collected oV Vanuatu Islands during the BOA1cruise (September 2005 Vanuatu) and during the Santo-BOA cruise (October 2006) on the RV Alis Duringthese cruises the large bay (Big Bay) located at the northof Espiritu Santo Island in Vanuatu was thoroughlyexplored by trawling Over the two cruises 55 stationswere explored in this bay at depth ranging from 150 to1000 m Most of the time trawl brought back sunkenwoods and other plant debris The sunken plant materialwas always associated to a speciWc fauna Among otherorganisms wood-boring bivalves of the genus Xyloph-aga wood-eating limpets of the genus Pectinodonta andwood or reed housing hermit crabs of the genus Xylopag-urus were very abundant During these cruises M and-amanica were repeatedly caught in relatively greatnumber together with woods other plant debris and thetypical associated fauna We here examined six speci-mens from the wood falls of Vanuatu four from thestation CP2432 (14deg597S 166deg550E 630ndash705 m 08Sep 2005 BOA1) one from the station CP2421(14deg571S 166deg551E 677ndash771 m 06 Sep 2005

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Mar Biol (2009) 1562421ndash2439 2423

BOA1) and one from the station AT90 (15deg015S166deg541E 503ndash553 m 13 Oct 2006 SantoBOA) Wecompare these specimens with three individuals associ-ated to wood falls from Solomon Islands (stationCP2846 10deg280S 161deg224E 533ndash612 m 23 Sep2007 SalomonBOA3) and with four specimens fromfour diVerent geographic areas and possibly recoveredon other substrates because the later were not reportedThese specimens come from New Caledonia (stationCP741 22deg36S 166deg26E 700ndash950 m 1993 Bathus2)from the Philippines (station CP123 12deg11N 121deg45E648ndash649 m 1985 Musorstom3) from Indonesia (stationCC21 05deg14S 133deg00E 688ndash694 m 1991 Karubar)and from the Fiji Islands (station CP1342 16deg460S177deg397E 650ndash701 m 1998 Musorstom10) Almostall specimens were Wxed and conserved on board in 75degand used in light microscopy scanning andor transmis-sion electron microscopy (LM SEM and TEM) The gutof some specimens from Solomon Islands were dis-sected removed and Wxed in 4 paraformaldehyderinsed and kept in ethanol 99 at 4degC One of them wasused in this study for staining with 46-diamidino-2-phenylindole (DAPI)

Macroscopic observations and dissection

Before preparation for microscopy the specimens wereexamined and photographed During dissection the posi-tion of the digestive system in relation to the body wasdrawn in broad outline (Fig 1a) with the help of a cameraLucida on a Leica M10 stereomicroscope For microscopythe following dissections were performed with Xame-steril-ized instruments Mouthparts were removed and separatedin order to have complete details of their external morphol-ogy Digestive tracts were dissected and divided into threeparts the foregut the anterior intestinal region and the pos-terior intestinal region This division was arbitrary as noparticular external morphology enabled us to distinguishthe midgut from the hindgut Because ethanol Wxation tendsto weaken tissues the midgut often broke oV during dissec-tion It appeared very short just behind the stomach

SEM and X-ray microanalysis

Scanning electron microscopy (SEM) was used to observethe digestive tracts of Wve specimens from Vanuatu (4 fromthe BOA1 cruise and 1 from the SantoBOA cruise) and the

Fig 1 Munidopsis andama-nica Ethanol-preserved speci-men from a deep-sea sunken wood (BOA1 cruise Vanuatu) a Diagram of the digestive tract The midgut is supposed to be very short or lost because never observed Anterior and posterior parts of the hindgut are not externally diVerent and were dis-sected arbitrary b Dorsal view of the specimen c Spoon-shaped depression formed by a closed-up claw d SEM view of the tip of the cheliped Wnger serrated edge and clumps of large smooth setae

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2424 Mar Biol (2009) 1562421ndash2439

digestive tract of specimens from the Solomon IslandsPhilippines New Caledonia Fiji Islands and IndonesiaThe hindgut of the SantoBOA-cruise specimen was dividedinto four parts two for observation in SEM and two forobservation in TEM and LM (see below) Mouthparts andgut samples of a specimen from Vanuatu were dehydratedthrough a graded ethanol series critical-point dried withCO2 as the transitional Xuid and mounted on aluminumstubs During mounting the diVerent parts of the gut weresplit longitudinally to reveal the gut lining morphologyThe gut contents were gently removed and put next to thedigestive structure that initially contained them When theywere recognizable beneath the stereomicroscope constitu-ents of the gut contents were roughly identiWed The sam-ples were Wnally platinum-coated in a Balzers SCD-030sputter-unit prior to observation with a scanning micro-scope (JEOL JSM-840A) operating at 20 kV

Elemental energy-dispersive X-ray microanalyses(EDX) were performed on the platinum-coated bulk sam-ples prepared for SEM observation to determine the ele-mental composition of hard mineral pieces in the gutcontent X-ray microanalyses and elemental spectra wereperformed with a scanning electron microscope Wttedwith a Link Pentafet detector and a Link eXl-10 ana-lyzer

LM and TEM

Fixed on board in 70deg ethanol during the BOA1 andSantoBOA cruises the gut of one BOA1-cruise specimenand the two other parts of the hindgut of the SantoBOA-cruise specimen were utilized for light microscopy (LM)and transmission electron microscopy (TEM) For betterpreservation of the tissue during processing they werere-hydrated in the laboratory and Wxed in 25 glutaral-dehyde in seawater diluted 710 Then the gut sampleswere rinsed Wxed in 1 OsO4 dehydrated through anethanol and propylene oxide series and embedded inepoxy resin (SPI-PON 812) Semi-thin and ultra-thin sec-tions were obtained with a Reichert-Jung Ultramicro-tome (Ultracut E) using a diamond knife Semi-thinsections were stained with toluidine blue (1 pH 90)for observation by light microscopy (with an OlympusPROVIS AX70) and photographed with an OlympusDP50-CU camera Ultra-thin sections were contrastedwith uranium acetate and lead citrate and observed with aJeol (JEM 100-SX) transmission electron microscopeoperating at 80 kV

DAPI staining

The gut of one specimen from Solomon Islands was Wxedin 4 PFA kept in 100 ethanol and embedded in

Steedmanrsquos wax [polyethylene glycol distearate (PEG)1-hexadecanol 91] Sections of 8 m were obtained witha Reichert-Austria Microtome on Superfrost Ultra Plusslides and conserved at iexcl20degC The slides were passedthrough three successive 100 ethanol baths to removethe wax and dried then passed through 75 ethanol andre-dried and Wnally passed in methanol acetic acid (13)to permeabilize the bacteria before to be dried again TheDAPI solution (05 gml) was applied on the sections for15 min in the dark and then the slides were rinsed indistilled water and observed with an epiXuorescencemicroscope

Results

Morphological features of feeding appendages and claws

As shown on the specimen in Fig 1b M andamanica hassymmetrical long (twice the length of the carapace) andthin spindly but robust chelipeds As a reminder the pere-iopods of crustaceans classically consist of seven segmentscoxa basis ischium merus carpus propodus and dacty-lus The claws are formed by articulation of the dactyluswith an outgrowth of the propodus

In resting position the chelipeds of M andamanica areoutstretched forward with the claws laid in such a way thatthey can pinch laterally and are dorsoventrally XattenedThe mediodorsal rims of the Wngers bear a row of sharpteeth that grow serrated toward the distal part of each Wngerand become a smooth edge in the ventral rim When theWngers are closed the mediodorsal rims meet each otherthe serrated edges show imbricated teeth and the ventralside of each claw forms a spoon-shaped depression (Fig 1c)The chelipeds are covered with many clumps of largesmooth setae without epibiotic microorganisms (Fig 1d)The joints between the propodus and carpus and betweenthe carpus and merus enable movements of the clawstoward the mouth appendages

As in other decapods the mouthparts consist of six pairsof appendages From oral to aboral these are the mandi-bles the Wrst and second maxillae and the Wrst second andthird maxillipeds A general view of the mouthparts of Mandamanica is shown in Fig 2a All mouthparts wereobserved but we present here only the results pertaining tothe third maxillipeds the Wrst maxillae and the mandiblesbecause several previous studies on decapods have shownthat the third maxillipeds are often the Wrst parts to makecontact with the food (accumulating sediment collectingparticles in suspension or grasping preys) and that thecrista dentata a raw of strong teeth on the ischiopodite ofthe third maxilliped can sometimes play a role in claspinglarge food items The food is generally transferred from the

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Mar Biol (2009) 1562421ndash2439 2425

third maxillipeds up to the mandibles transported by theother oral appendages (the second and Wrst maxillipedsthen the second and Wrst maxillae) The mandibles are usu-ally involved in pummeling (ie cutting tearing crushingor grinding) the food before ingestion

For the same reasons the morphology of the setae cover-ing these mouthparts is also presented Setal types were dis-tinguished according to the classiWcation system found inGarm (2004) in which setae are divided into pappose plu-mose serrulate serrate papposerrate simple and cuspidatetypes An attempt is made here to link the morphology ofthe setae covering the mouthparts to the function theymight have (eg creating water current for respirationcleaning or brushing the antennae mechanoreception orchemoreception grasping and sticking the food etc)

Third maxillipeds

Each third maxilliped of M andamanica (Fig 2b) consistsof a basis bearing a segmented pediform endopodite and along slender segmented exopodite with few setae Theendopodite is composed of an ischiopodite with an aboralrow of ten large serrate setae (Fig 2c) a meropodite withseven strong simple setae a carpopodite with Wne long pap-poserrate setae (Fig 2d) a propodite with short papposesetae on the aboral side and long Wne serrate setae on theoral side (Fig 2e) and a small dactylopodite with bundlesof long serrate setae The medio-oral side of the ischiopo-dite has a well-developed crista dentata (Fig 2f) with arow of 18 strong teeth 70ndash80-m height with tip-to-tip dis-tances of sect60 m

Fig 2 Munidopsis andamanica from Vanuatu Mouthparts a Ventralview of the mouthparts bndashf general view and details of the left thirdmaxilliped c serrate setae on the ischiopodite d papposerrate setaecarpopodite e serrate setae on the propodite f strong crista dentata onthe ischiopodite g h left Wrst maxilla with (h) spines and teeth-like

cuspidate setae on the basipodite i j left mandible with (j) thick serratesetae with scale-like setules on the pedipalp Bas basipodite Cox cox-opodite Endo endopodite Exo exopodite Inc incisor process Mdmandible Mdp mandible pedipalp Mx1 Wrst maxilla Mxp3 thirdmaxilliped

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2426 Mar Biol (2009) 1562421ndash2439

First maxillae

Each Wrst maxilla of M andamanica (Fig 2g) consists of apaddle-shaped basipodite a coxopodite and a spike-heel-like endopodite Only the basipodite has large spines andlarge teeth-like cuspidate setae on the medial side (Fig 2h)

Mandibles

Each mandible of M andamanica (Fig 2i) consists of along basis bearing a gnathal lobe and a palp The gnathallobe is strongly curved and has two processes a largeXattened molar process orally and a large cutting inci-sor process aborally The palp is three-segmented andoriginates anteriorly at the base of the gnathal lobe Itcrooks to the median and the terminal segment is locatedorally in relation to the incisor process The end of theterminal segment bears a bundle of long large setae oftwo types on the one hand papposerrate setae withsparse Wne setules on the distal portion giving way tomore densely arranged distal setules and on the other

hand setae with thick densely arranged scale-like setules(Fig 2j)

Ultrastructure of the digestive lining

Gastric mill

The following descriptions concern the grinding pieces ofthe gastric mill in the foregut ie the dorsal (or median)tooth and lateral teeth For a description of the anatomy andphysiology of the decapod foregut see Ceccaldi (2006)

The dorsal tooth of M andamanica (Fig 3a) is smoothand pyramid-shaped with a rectangular base and triangularlateral surfaces The anterior face is rather concave and hasa dorso-ventral Xattened keel The ventral surface of theurocardiac ossicle leading to the tooth is slightly curved andbears dorso-ventral grooves Both of the lateral sides of theurocardiac ossicle are girded with setae and the areas fromwhich the tooth arises widen in a small Xange bearingspines Both of the lateral teeth are elongate and oval inshape (Fig 3b) tapering posteriorly with nine denticles

Fig 3 Munidopsis andama-nica from Vanuatu andashd Gastric mill a dorsal robust median tooth b oval-shaped lateral tooth with (c) projections of short thick spines in its grooves d lateral accessory tooth with strong spines e f Hindgut e spiny villous plates separated by deep grooves f cuticular spines on the villous plates and arranged in semi-circles toward the anus Ant anterior part arrows resident bacteria

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Mar Biol (2009) 1562421ndash2439 2427

the Wrst anterior denticle being the largest The Wrst threedenticles are smooth and crest-shaped the fourth beingcurved The medial surface of the teeth is concave from thispoint and Wve grooves traverse the teeth posteriorly Theyextend to the ventral side of the teeth and are continued ontheir dorsal side by the last Wve denticles of the teeth Thethree anterior-most grooves have an anterior edge bearingprojections of short thick spines (Fig 3c) Both of the lat-eral accessory teeth (Fig 3d) bear 14ndash15 strong compactventral spines arranged in a circle and directed posteriorly

Midgut and digestive gland

The midgut and the digestive gland of M andamanica wereunfortunately not observed Due to ethanol Wxation thedigestive gland was liqueWed and the junction betweenforegut and hindgut always broke during dissection Never-theless this junction appears very thin suggesting that themidgut is very short maybe limited to a simple ringbetween the pyloric stomach and the anterior hindgut

Hindgut

The hindgut of M andamanica has characteristic ellipticalvillous plates (100ndash150-m large 200ndash300-m length and10-m height Fig 3e) except on the ventral zone Cuticleprojections were observed arranged in acute semi-circlesof spines directed toward the anus (Fig 3f) each semi-cir-cle being formed by one epidermal cell The anterior-mostpart of the hindgut has simpler arrangements (3 or 5spines) but the number of spines increases rapidly towardthe posterior part The major part of the hindgut thus bearssemi-circles with 12ndash25 spines 3-m length at their exter-nal border and 8ndash14 spines 500-nm length at their internalborder Between convolutions however the number of

spines is very low and sometimes nil The hindgut liningharbors a nanorelief (Figs 3f 6c) made of tiny entwinedrod-shaped paddings (sect15-m length) and depressions

Gut content morphology and X-ray microanalysis

The analyses of the gut contents of all the specimensincluding those from the diVerent geographic areas aresummarized in the Table 1 and illustrated by the Figs 4andashf5andashg and 6andashd Most of the pictures were taken on individ-uals from wood falls of Vanuatu but some of them illus-trate peculiar structures found in specimens from otherlocations The content of the gut always includes bothorganic and mineral fractions

In all the specimens associated to the Vanuatu woodfalls LM photographs reveal an organic fraction consistingof large blue-stained wood fragments (up to 500 m)mixed with a coarse purple-stained organic material notreadily recognizable (Fig 4a) The plant fragments exhibitthick secondary walls and empty cell lumens conWrmingthat they consist of ligneous hard tissue and most probablyxylem (Fig 4b e) The peripheral broken cells are gener-ally Wlled with exogenous material (Figs 4b e 5c) andtheir walls appear considerably decomposed by microor-ganisms (ie bacteria and fungi) (Fig 4b f) Bacteria andfungi are observed by SEM on the plant cell walls (Fig 5ab) By TEM these walls appear perforated by tunnelingbacteria (Fig 4f) Low-magniWcation SEM pictures showthat the wood fragments look like shavings rolled up onthemselves (Fig 5c) Almost all specimens from other loca-tions have terrestrial vegetal fragments in their gut contentsexcept the one from Fiji Islands (Table 1) The specimenassociated to wood falls from Solomon Islands has gut con-tent very similar to that of the specimens from Vanuatuwood falls with high quantities of vegetal fragments of

Table 1 Comparative analysis of the resident hindgut microXora and the gut contents of 14 M andamanica specimens from six diVerentgeographic areas Vanuatu Solomon Islands New Caledonia Fiji Islands Indonesia and Philippines

Approximate proportion of items observed + rare (15) ++ more than sparse (15ndash30) +++ abundant (50ndash60) ++++ very abundant (70 andmore) An empty case means that the item was not observed

n number of specimens examined

Munidopsis andamanica

n Resident hindgut microXora

Gut contents

Mineral fraction Organic fraction

Bacteria Fungi Clay Skeletons and spicules

Tests of protists

Organic matter

Plant remains

Algae Fungi Gorgonin Bacteria

Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

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2428 Mar Biol (2009) 1562421ndash2439

leaves and wood The diVerence with the other specimens(from New Caledonia Indonesia and Philippines) isobserved in the lower proportion of vegetal cells and in thepresence of other organic fragments as branching Wlamentsof algae (50ndash100-m width Fig 6a) in the gut of the Indo-nesian specimen or fungi Wlaments (5ndash40-m widthFig 6b) in the gut of the Fijian specimen Both algae andfungi are found in great amounts in the gut of the specimenfrom New Caledonia In contrast to terrestrial plants frag-ments algae Wlaments do not show cells with strong brokenwalls angular disposition and open punctuations betweenthem They rather appear as ribbon-like structures with sev-eral cells abreast in width thin intercellular walls that areoften folded and a smooth external surface giving a hint ofthe cells beneath The fungus hyphae appear as single Wlesof cells and exhibit a thick wrinkled surface such as resi-dent gut fungi (see below) Other organic fragments in thegut of specimens from Solomon Islands New Caledoniaand Philippines are identiWed as gorgonin (Fig 6c) ieorganic matrix of the corneous skeleton in gorgonianswhose elemental microanalysis shows a major peak of sul-fur (eg see Block and Bolling 1938) These gorgonin frag-

ments are sometimes associated with mineral debris ofgorgonian skeleton (Ca-phosphate see below) The gutcontent of all specimens recovered or not with wood fallsincludes rod-shaped bacteria (1 m pound 025 m) either iso-lated or compacted into pellets that can be very large (up to180 m in diameter Fig 5d e) The DAPI-staining of thegut cross-sections of the Solomon Islandsrsquo specimen givesevidence of a lot of bacterial rods inside the digestive con-tent (Fig 7) Finally in all individuals SEM (Fig 5f) aswell as LM (Fig 4a) and TEM (Fig 5g) reveal coarse tornorganic matter between the larger recognizable organicand mineral fragments This matter is often mixed withscaly clay particles (3ndash5 m) described below Among theunidentiWed organic material in the gut content of Vanuatuspecimens recognizable constituents are membraneremains or vesicles bacterial cell ghosts small debris ofplant cell walls and secretions left in wood cell walls bytunneling bacteria (compare Figs 4f 5g) Thus the organicfraction in the gut content of M andamanica appears toconsist mostly of highly degraded vegetal debris (terrestrialplants algae) and other refractory materials as gorgoninfragments and mycelium Wlaments and also in a large

Fig 4 Munidopsis andama-nica from Vanuatu a Semi-thin cross-section of the anterior hindgut Wood fragments (arrowheads) in the contents are blue-stained organic matter is purple-stained and the mineral fraction appears as dark parti-cles (arrows) b Detail of a frag-ment of wood (xylem tissue) with empty cell lumens and thick secondary walls At the periph-ery the cell walls are degraded by microorganisms and the cells are Wlled with exogenous mate-rial c d Semi-thin section of the posterior hindgut with (d) fungal mycelium Wlaments (dotted ar-row) located between the gut content and the cuticle e Ultra-thin section of a wood fragment with peripheral cells Wlled with exogenous organic material and minerals (thin arrows) f Traces (t) left by tunnelling bacteria having perforated secondary walls (w) of a wood fragment in the gut Cont gut content Cut cuticle lining Epi epiderm t traces of bacteria w secondary walls of wood fragments arrow-head wood fragment arrow minerals dotted arrow fungal mycelia

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Mar Biol (2009) 1562421ndash2439 2429

Fig 5 Munidopsis andama-nica from Vanuatu a Bacteria and b fungi at the surface of wood fragments in the gut c Shaving-shaped wood fragment observed by SEM d e Pellet of rod-shaped bacteria f Organic matter mixed with clay particles (arrows) and X-ray spectrum of clay particles showing Al Si Ca and Fe major peaks g Organic remains in the gut content as viewed by TEM m membrane remains or bacte-rial ghost t traces of tunnelling bacteria arrows clay particles

Fig 6 Munidopsis andama-nica gut contents a Branching algae and b fungi Wlaments in the specimen from New Caledonia c Gorgonin in the specimen from Fiji Islands d mineralized Ca-phosphate skeleton of a gorgonian coral in the specimen from the Philippines

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2430 Mar Biol (2009) 1562421ndash2439

proportion of bacteria either from surface bioWlms or fromthe inside of decaying substrates No cuticle fragments areseen however suggesting that M andamanica does notfeed on crustacean preys or cadavers Animal tissueremains cannot be excluded but if present they must comefrom animals other than crustaceans

In all specimens the minerals and mineralized structuresof the gut content consist of clay particles intact or brokenperforated globular foraminifer tests straight and spiny spic-ules as well as other mineral fragments (Table 1) The clayparticles appear scaly by SEM as darkly stained particles byLM (Fig 4a) and as stacks of parallel electron-dense sheetsby TEM (Fig 5g) Their nature was conWrmed by X-rayspectra showing major Al (K 148 keV) Si (K 173 keV)Ca and Fe (K 64 keV) peaks (Fig 5f) The calcareouscomposition of foraminifer tests was conWrmed by spectradominated by Ca peaks (K 369 keV K 401 keV) Themicroanalysis revealed the siliceous nature of some spiculeswhich might thus be sponge spines In the specimen fromFiji structures looking like mineral fragments of gorgoniancoral skeletons are identiWed on the basis of the crossed dis-position of the crystals (Fig 6d) and their X-ray spectradominated by signiWcant Ca et P (K 2013 keV) peaksCalcium phosphate particles found in the bolus of the speci-mens from Fiji Islands Solomon Islands and Indonesiacould also originate from gorgonian skeletons Finally thespectra obtained with wood fragments displayed minor Siand Ca peaks compatible with the mineral content of wood

Gut microorganisms

No microXora was found on the foregut lining of M and-amanica but microbial colonization (ie bacteria and fun-gal mycelia) was obvious in the hindgut of all specimens

The pictures show that in all specimens from wood fallsof Vanuatu rod-shaped bacteria (15 m pound 025 m) aredistributed all along the hindgut (Fig 8a) Often attached tothe cuticle spines of the villous plates these bacteria aremostly found at higher density in the depressions betweenplates (Fig 8b c) In the median dorsal zone of the hindgutthey are generally stuck together whereas they are moreseparated from each other in the ventral zone In someplaces they are glued in mucous secretions probably ofbacterial origin (Fig 8d) Bacteria are also observed onultra-thin sections (Fig 8e) Although ill-deWned the cellenvelope displays two membranes as classically found inGram-negative bacteria (eg Costerton et al 1974) Table 1shows that such resident rod-shaped bacteria are found inthe hindgut of the specimens from others locations exceptin the Indonesian specimen Yet it was noticed that thebacterial colonization was less extended and patchier in theindividuals from New Caledonia Fiji Islands Indonesiaand Philippines than in the specimens from wood falls ofVanuatu and Solomon Islands

In all specimens from wood falls of Vanuatu except theone from the SantoBOA cruise large Wlaments resemblingfungal hyphae in shape and size (sect 23 mm pound 8 m) areobserved in the posterior hindgut Their surface is deli-cately and longitudinally wrinkled They cover an averageof 20 of the hindgut surface according to measurementstaken on SEM objects SEM (Fig 9a b) and LM (Fig 4d)pictures show that these Wlaments surround the gut contentlike a cylindrical cover between the cuticle and the ingestedfood Some of the hyphae clearly appear to be attached tothe hindgut cuticle (Fig 9c d) with a pot-bellied base(12-m width) upstream and a Wlament extending towardthe anus Others are attached downstream with the Wlamentextending up the digestive tract Their eukaryotic fungalnature is conWrmed by the observation of cell nuclei andthick cell walls by TEM (Fig 8e) In their distal part theWlaments exhibit round-shaped or ovoid fructiWcationsappearing to vary in number from 7 to 35 ldquocellsrdquo at least(Fig 9f) Rod-shaped bacteria are found at some locationson the stems of the fungal Wlaments Fungi attached to thehindgut lining are also found in specimens from NewCaledonia Indonesia and Philippines but neither in thosefrom Solomon nor in those from Fiji Islands (Table 1) Thehyphae roughly correspond to the above description The onlydiVerences consist in the length of the Wlaments that aremuch shorter (from 10 to 40 m) in the specimen fromNew Caledonia and in attach of the Wlament to the cuticlesurface Instead of a pot-bellied base the Wlaments have acylindrical narrow foot of 5 m in length in the specimensfrom New Caledonia and Indonesia Only the resident fungifound in the specimens from Vanuatu exhibits distal fruc-tiWcations Fungal colonizations were also less expanded inindividuals from New Caledonia and Philippines

Fig 7 Munidopsis andamanica from Solomon Islands DAPI-stain-ing of the bacteria Xuorescing in blue inside the gut content Theirshape of small rods enables us to diVerentiate them from someelements that have a natural auto-Xuorescence like the minerals or thelignin of the wood fragments

123

Mar Biol (2009) 1562421ndash2439 2431

Discussion

In the absence of any possible in situ observations on Mandamanica the morphological approach has been mosthelpful in supplying information on its feeding ecologyWhile some morphological features may be constantwithin families it has been shown that the mouthpartsand digestive tract morphology can vary according to thetype of mastication (Powell 1974 Kunze and Anderson1979 Icely and Nott 1984 Ngoc-Ho 1984 Felgenhauerand Abele 1985 Skilleter and Anderson 1986 Wolfeand Felgenhauer 1991 Pinn et al 1999 Ceccaldi 2006)We have also been able to relate the diet of the host tothe presence of microbial symbionts of several types thatcan play a role in the digestion especially in detritivo-rous and herbivorous species (Harris 1993 Pinn et al1999)

On what does it feed

Our results clearly show that M andamanica associated towood falls (from Vanuatu and Solomon Islands) is at leastpartially xylophagous Yet observations particularly ofothers specimens (from New Caledonia PhilippinesIndonesia and Fiji Islands) suggest that M andamanica isnot exclusively xylophagous but rather a specialist ofrefractory substrates Moreover bacteria associated to theingested substrates (ie the bioWlm) should highly contrib-ute to its diet

Munidopsis andamanica associated to sunken woodsfeeds directly on them as attested by the quantity of woodfragments found in its gut contents Other indications thatthe squat lobster feeds on the deposit substrate are the pres-ence of clay spangles and the shaving-like wood fragmentsin the gut suggesting that M andamanica grazes silty

Fig 8 Munidopsis andamanica from Vanuatu hindgut a Rod-shapedbacteria (15 pound 025 m) widely distributed over the hindgut lining bc higher density of bacteria in the grooves between the villous plates

(p) d bacteria attached to the cuticular spines and glued in mucoussecretions and e TEM view of a bacterium showing its Gram-negativecell envelope p villous plates

123

2432 Mar Biol (2009) 1562421ndash2439

sunken wood The clay spangles as the calcareous and sili-ceous fragments from various organisms (ie tests of pro-tists mineralized gorgonian skeletons sponge spicules)certainly have a sedimentary origin On the other handorganic matter other than wood of unknown origin consti-tutes a considerable proportion of the gut contents and thusseems to be an important food source for M andamanicaon sunken woods The large bacterial pellets found in thegut of some specimens suggest that M andamanica may beable to feed on the bioWlm covering the substrate Althoughunrecognizable with the exception of traces of tunnelingbacteria and some membrane vesicles or bacteria ghoststhis organic matter might be degraded microorganisms andor highly decomposed wood components The comparisonbetween specimens from wood falls and those from othersubstrates (not reported) strongly suggest that the speciesM andamanica is rather specialized in eating refractorysubstrates including wood algae fungi and the corneous

skeletons of gorgonian corals It seems however to have aclear preference for terrestrial vegetal remains Indeed atleast one of these refractory substrates occurs in all thespecimens (Table 1) and can reach high quantities espe-cially when it consists of wood Even if soft animalsrsquo tis-sues cannot be excluded from the diet a predatory behaviorshould be ruled out Indeed the morphology of the spindlyclaws strongly reduces this hypothesis Instead the scav-enging of worms or mollusks from sunken wood whichrepresent a large part of the macrofauna associated to woodfalls ecosystems (Samadi et al 2005) remains possible butis not defended by any evidence A much more probablesource of nutrients other than wood would be bacteriaingested with the substrate Even if there is no directevidence of bacterial digestion by M andamanica manybacteria were found in the gut contents especially with theDAPI-staining and in SEM showing bacteria clustered intolarge pellets Traces of bacteria viewed in TEM notably

Fig 9 Munidopsis andamanica from Vanuatu posterior hindguta b Fungal mycelia (sect23 mm pound 8 m) surrounding the gut contentc d fungal mycelia attached (large arrows c) to the cuticle lininge cross-section of a fungal Wlament showing the cell nucleus (n) and

wall (w) f vegetative fructiWcations of the fungal hyphae (thin arrow)n cell nucleus of fungal mycelium w wall of fungal mycelium largearrow base of the fungal mycelia thin arrow fructiWcations of fungalmycelium

123

Mar Biol (2009) 1562421ndash2439 2433

inside the vegetal cell walls support the view that bacteriawere degrading the substrate and most probably alivebefore being ingested The squat lobster ingesting deeplydegraded wood could Wrst beneWt from the action of free-living wood bacteria that release degradation products andnutritive compounds The presence of numerous bacterialghosts on the TEM sections suggests that a great proportionof the free-living wood bacteria die during the transit Thisdoes not exclude that some of them survive and developinto a transitional microXora in the digestive tract and couldprovide cellulose-degrading enzymes as it is proposed forthe resident microXora (see below)

How does it feed

The claws mouthparts and foregut morphology of M and-amanica are in good agreement with the diet of the speciesas determined by analysis of the gut contents The feedingappendages appear similar to those of detritivorous deca-pods while the gastric mill is suggestive of deposit-feed-ing On these bases a processing sequence for food itemsespecially wood pieces is proposed

Feeding appendages morphology

The spindly chelipeds of M andamanica are not those of apredator The use of the chelipeds for feeding is oftenreported for both crabs and galatheid squat lobsters (egMunida sarsi according to Hudson and Wigham 2003) Itwas also observed directly on board during the Salomon-BOA3 cruise with freshly collected live galatheid speci-mens other than M andamanica (C Hoyoux personalobservation) The Wngers of M andamanica forming aspoon not gaping and with prehensile edges crenulatedmight hold a piece of decayed wood by clasping (eg asplinter at the surface of a log) tear the piece oV by crush-ing its teeth Wngers against each other and then Wnallybring the freshly cut fragment to the third maxillipedsusing the spoon-shaped depression to retain it Bacteriafound in the gut contents could be highly likely be ingestedwith the wood fragment but this depression could alsoscrape the bioWlm covering the substrate producing the pel-lets of bacteria Among the 224 species of Munidopsis sppdiscovered up to now (see Baba et al 2008) at least 49 spe-cies have this type of chelipeds Interestingly although thediet of very few of them was described it appears that spe-cies feeding at least partially on bacteria have often thisspoon-shaped structure (eg M alvisca M subsquamosaM crassa Maries) in contrast to some others that wouldbe predators or scavengers (eg M acutispina M mario-nis M serricornis) Such spoon-shaped chelipeds are alsoreported in herbivorous crab species (Wolcott and OrsquoConnor1992) for collecting plants (Coen 1987) and in two

specimens of Munidopsis spp that had plant fragments intheir foregut (Gore 1983)

The mouthparts of M andamanica exhibit features sug-gesting that they are adapted to manipulating large fooditems It is commonly accepted that teeth-like structuresie a well-developed crista dentata on the third maxilli-peds spiny Wrst maxillae and well-developed mandiblesenable clasping as well as shredding of larger food items(Caine 1974 Kunze and Anderson 1979 Stamhuis et al1998 Martin et al 1998 Garm and Hoslasheg 2001 Salindehoand Johnston 2003) Although these morphologies are oftenreported to a carnivorous feeding (eg Kunze and Anderson1979) these are also found in deposit-feeders (Salindehoand Johnston 2003 Garm and Hoslasheg 2001 Nickell andAtkinson 1995 Stamhuis et al 1998) Yet Nickell et al(1998) and Coelho and Rodrigues (2001) consider that themorphology of the crista dentata is linked to phylogenyrather than to the type of feeding but they do not excludethe possibility that this structure might be used in situ tocatch food since the specimens they studied were fed incaptivity We can thus suggest that these features maysimply indicate an aptitude to process large food itemsfor carnivorous as well as for detritivorous species InM andamanica from wood falls the crista dentata couldbe used in feeding to hold wood pieces Wrmly and to pushthem toward the mandibles Furthermore the symmetry ofthe mandibles of M andamanica is not typical of a carnivo-rous species as this feeding type often implies asymmetri-cal mandibles (Kunze and Anderson 1979 Skilleter andAnderson 1986 Salindeho and Johnston 2003)

Construing the function of the setae covering the mouth-parts is quite diYcult Some authors have tried to linkfunction to setal morphology but sometimes similar mor-phologies fulWll several possible functions (Factor 1978Schembri 1982 Felgenhauer and Abele 1985 Crain 1999Stamhuis et al 1998 Coelho and Rodrigues 2001 Garm andHoslasheg 2001) The literature suggests that serrate setae canplay a role in chemosensitivity cleaning or food adhesioncuspidate setae can play a role in grasping food plumosesetae are often involved in creating water currents importantin respiration or suspension-feeding and pappose setae donot participate in food handling but usually create setal barri-ers M andamanica has very few plumose setae on itsmouthparts conWrming that it is clearly not a suspension-feeder The majority of setae on the third maxillipeds are ser-rate chemoreceptive setae and pappose setae that can retainWne food particles stuck in the setules The cuspidate setae onthe basipodite of the Wrst maxillae could help to grasp food

Gastric mill morphology

The gastric mill of M andamanica exhibits morphologicalcharacteristics generally found in deposit-feeders (Kunze

123

2434 Mar Biol (2009) 1562421ndash2439

and Anderson 1979 Pinn et al 1999 Salindeho andJohnston 2003) few setae a simple strong dorsal tooth andlarge oval-shaped lateral teeth with deep transversal ridgesfew Xexible spines and a large anterior denticle This isclearly diVerent from suspension-feeders the gastric mill ofwhich usually has many setae a complex dorsal tooth andrhomboidal lateral teeth with many stout spines having acomb-like appearance (Pinn et al 1999) In M andama-nica the simple strongly calciWed and robust teeth mightbe adapted to processing hard substrates and specialized forcrushing and grinding wood fragments Interestingly simi-lar morphological features of the gastric teeth are found inherbivorous crabs where they are used to crush Wbrousplant materials (Coen 1987 Warner 1977 Giddins et al1986) This is especially true for the mangrove crab Neos-armatium smithi which feeds on mangrove litter that hasdecayed for several weeks This crab has robust smoothgastric teeth with deep grooves (ie molar-shaped teeth)Large spines encircling the accessory lateral tooth are alsofound in M andamanica in addition to lateral teethTogether these spines and teeth might like the lateral teethof deposit-feeders help to maintain food particles such aswood shavings while the dorsal tooth would grind the foodparticles like a pestle on a mortar

Munidopsis andamanica thus possesses the feedingappendages and gastric mill of a detritivorous deposit-feeder that seems fairly well adapted to feeding on woodUp to the foregut the treatment sequence of food espe-cially wood pieces in M andamanica might be describedin three steps as follows (1) use of the chelipeds to tear oVa partially degraded wood fragment and bring it betweenthe crista dentata of the third maxillipeds (2) production ofshavings from the wood fragment maintained by the maxil-lipeds and spiny maxillae by grating with the incisor cut-ting edge of the mandibles and (3) crushing of the woodshavings between the lateral and dorsal teeth of the gastricmill This scenario suggests that M andamanica would notdirectly bore the wood surface and does not form a part ofthe Wrst colonizers of the sunken wood this agrees with thebehavior of some species of the genus (eg M crassa andanother Munidopsis sp) which come later in the coloniza-tion of a bait (eg thuna or seal cadaver) compared to otherscavengers as Wshes and amphipods (Janszligen et al 2000Kemp et al 2006)

Role of the resident gut microorganisms

It is generally recognized that the gut microXora of marinedetritivores provide the host with a complementary enzy-matic arsenal for the degradation of refractory ingestedorganic substrates (Dempsey and Kitting 1987 Plante et al1990 Erasmus et al 1997) Harris (1993) further suggeststhat the degree and type of colonization of the decapod

digestive tract is related to the diet Thus carnivorous spe-cies show little evidence of bacterial colonization in thegut while the hindgut of detritivorous decapods is exten-sively colonized In contrast to the symbionts harbored bymollusk and annelid tissues which are generally intracellu-lar (ie endosymbionts) crustacean symbionts are oftenextracellular (ie ectosymbionts) and located on the cuticlelining of the hindgut as in the digestive symbiosesdescribed in detritivorous isopods (Zimmer and Bartholmeacute2003 Lindquist et al 2005) thalassinid shrimps (Pinn et al1999 Lau et al 2002 Harris 1993) prawns (Zbinden andCambon-Bonavita 2003 Oxley et al 2002) and crayWshes(Growns and Richardson 1988) which feed on leafs litter(Guan and Wiles 1998 Reynolds and OrsquoKeeVe 2005)

The present results reveal a considerable microXora ofresident bacteria andor fungi in all specimens examinedMoreover it is likely that some bacteria from the gut con-tents form a living transitional microXora

Based on both the literature (Smith and Douglas 1987Margulis et al 1990 Douglas 1994 Zook 1998 Bricage1998 2000 Werner et al 2002) and our own observationsof the bacteria covering the hindgut lining of M andama-nica we here propose four morphological criteria thatcould deWne a resident possibly symbiotic association (1)the association occurs in all examined specimens (2) themicroorganisms are consistently located on the gut lining(3) the supporting tissues appear healthy and (4) the diet ofthe host suggests a requirement for digestive symbiontsThe xylophagous detritivorous diet of M andamanicaassociated to wood falls strongly suggests a need for thissymbiotic digestive microXora The colonization lessextended or patchier in the case of specimens from sub-strates not reported would be linked either to their moltstage or to their diet less rich in vegetal fragments Forexample in the specimen from Indonesia contrarily to theoccurrence of resident fungi no bacterial colonization wasfound (Table 1) During transit through the hindgut diges-tion of wood might be assisted by the activity of residentbacteria surviving transitory bacteria or both The prolifer-ation and activity of these bacteria could enrich the fecesin nutrients As suggested for mangrove grapsid crabs(Webster and BenWeld 1986) M andamanica should bothaccelerate wood decay by tearing oV pieces and enrich themedium in nutrients by producing feces containing woodfragments partially degraded by the microorganisms of itsdigestive tract The role of such detritivores is recognizedas very important in the biodeterioration of deep-seaorganic substrates (Schwarz et al 1976 Palacios et al2006)

In M andamanica interestingly the bacteria are notattached only to the microspines of the hindgut lining butappear massed in the folds between the spiny villous platesThis suggests that the cuticular spines might not really be

123

Mar Biol (2009) 1562421ndash2439 2435

necessary for bacterial attachment as proposed by Breckoand Strus (1992) and Pinn et al (1999) They might ratherplay a mechanical role facilitating the transit of the fecalpellets through the hindgut (Pillai 1960 Dall 1967 Bignell1984 Felgenhauer 1992) According to our observations onM andamanica attachment of the bacteria should befavored by the nanorelief of the cuticle surface which pro-vides small depressions precisely in the size range of theobserved rod-shaped bacteria This contributes to thedebate on the role of the cuticle microdentition

The presence of resident bacteria in the hindgut ofM andamanica further suggests that most of the digestionmight occur in the hindgut like in the terrestrial isopodPorcellio scaber which feeds on leaf litter and harborscellulolytic bacterial endosymbionts in its digestive gland(Zimmer and Topp 1998) Two ways could be consideredfor M andamanica to gain nutrients they are eitherobtained through the very thin cuticle of the hindgut or bythe ingestion of feces The part of nutrients that are notassimilated then would be deWnitively lost and wouldenrich the environment Moreover this important role ofthe hindgut is likely related to the reduced size of themidgut which although not observed here because of itstendency to break oV appears very short in M andamanica

The fungal mycelia detected in M andamanica meetonly three of the four criteria of a symbiotic associationThey are frequently found and always located in the poster-ior hindgut They are oriented and anchored to the cuticlelining They reproduce outside the gut contents and they donot seem to be parasitic given the apparent good health ofthe tissue Their anchorage to the cuticle suggests that theyare not environmental fungi ingested with wood fragmentsMorphologically the fungal microXora of M andamanicaalso appears very diVerent from the fungi found in thesunken wood itself (Dupont et al 2005) The vegetativefructiWcation of the hyphae in Vanuatu specimens and theirlocation at the end of the hindgut might be due to the highnutrient content of the posterior feces enriched by theupstream bacterial proliferation Yet their absence in somespecimens might indicate that these fungi are not obligatesymbionts Although resident fungi are generally consid-ered pathogens in marine invertebrates (Loacutepez Lastra 1990Lichtwardt 1996 Alencar et al 2003) complex digestivesymbioses have been described between cellulase-produc-ing fungi and arthropods (Martin 1992 Kimura et al2002) An example of digestive symbiosis is found in thesquat lobster Munidopsis subsquamosa from hydrothermalvents which hosts a trichomycete in the foregut It thusseems likely that the hindgut fungi of M andamanica con-tinue the digestion of wood perhaps by degrading ligninwhich should be present in the xylem of ingested woodfragments and is known to be attacked by fungi (egHammel 1997) Fungal microorganisms might considerably

assist digestion of the ligneous wood plant andor algaethat M andamanica ingests

Herbivorous specialist or generalist scavenger

Squat lobsters are generally thought to be scavengers andfew studies have focused on the diet of species of the genusMunidopsis Even rare these studies give nevertheless evi-dence of diVerences of diet within the genus (Van Doverand Lichtwardt 1986 Chevaldonneacute and Olu 1996 Janszligenet al 2000 Escobar-Briones et al 2002 Micheli et al2002 Phleger et al 2005 Kemp et al 2006 Macavoy et al2008a b) The diet of M andamanica from deep-sea woodfalls shown here to ingest ligneous wood in large propor-tion appears quite original or exceptional Indeed variousplant materials eg phytoplankton micro- and macroalgaefoliage seeds fruits and leaf litter have been reported asfood sources for diVerent crab species wood being theexception not listed by Wolcott and OrsquoConnor (1992)However Gore (1983) examined two specimens belongingto the species M aries and M bermudezi and reported thatthey had plant fragments in their stomach Thus it could beproposed that among the genus Munidopsis some speciesare actually scavengers but others as M andamanicacould have evolved and become specialized in feeding ondiVerent hard substrates The similarity shared by therefractory substrates considered here ie wood plantdebris algae and fungi cell walls as well as hard animaltissues as corneous gorgonians skeletons and vertebratebones is a Wbrous texture and macromolecules stabilizedby hardy breakable covalent links Generally animals donot dispose of the endogenous enzymes to degrade suchorganic substrates Feeding on them should thus be consid-ered as a specialization diVerent from usual scavenging thatdoes not require any peculiar adaptation when restricted tothe feeding on soft tissues from dead animals As showedby Kiel et al (2008) some species (eg Xylophaga)appears to be specialized in a wood-based diet at least sincethe late Cretaceous

Despite of the negative aspects and constraints in usingplants as food instead of animal tissues herbivory is a com-mon phenomenon in many decapod crustaceans especiallycrabs in both aquatic and terrestrial habitats (Wolcott andOrsquoConnor 1992) and even in species considered carnivo-rous (Warner 1977) Using plants as a food source doeshave many negative aspects and constraints such as thepresence of refractory components such as lignin cellulosetannins and phenolics that are diYcult to digest (Mattson1980) calciWcations causing excessive wear on the chelaemandibles and teeth of the gastric mill (Coen 1987) giventhe high CN ratio of plants the 30 lower nitrogen con-tent of a plant-based versus an animal-based diet (Wolcottand Wolcott 1984) and lower levels of essential amino

123

2436 Mar Biol (2009) 1562421ndash2439

acids vitamins sterols and polyunsaturated fatty acids ascompared to animal tissue (Phillips 1984) Thus plant-eating decapods are generally not exclusively herbivorousbeneWting from other food sources or using various meansto oVset the unfavorably high CN ratio The mangrove crabN meinerti which eats leaf litter is proposed to derive asigniWcant part of its diet by foraging sediment detritus aricher source of nitrogen (Skov and Hartnoll 2002) Fur-thermore these crabs fragment leaves during feeding(Malley 1978) with subsequent acceleration of microbialdecay (Webster and BenWeld 1986) and a decrease in theCN ratio (Cundell et al 1979)

Our results on M andamanica showed that this speciesdoes not break with the rule Even if almost all the speci-mens have vegetal debris in their gut contents they alsomanifestly feed on other organic matters The results of ourexamination of M andamanica gut contents strongly sug-gest that the CN-ratio-reducing secondary food source ofM andamanica is the bacteria found in high quantities inall gut contents likely originating from the bioWlm growingat the surface of decayed wood or other hard substratesThe large amount of fungi found in the bolus of two speci-mens (New Caledonia and Fiji) should play the same roleas ingested bacteria Such an alternative food is indeedrequired by most wood-eating species because the xylemconsists solely of thick ligniWed cell walls and is devoid ofeven remnants of cytoplasm Thus the bioWlm may be animportant supply of molecules and elements lacking inwood It is noteworthy in this context that M andamanicadoes not bore into intact sunken wood but rather ingestspartially degraded wood fragments that it tears oV or grazesat diVerent places The periphery of these fragments gener-ally shows alterations such as perforations by tunnelingbacteria which occurred in the environment prior to inges-tion of the fragments

In conclusion M andamanica is predominantly a detri-tivorous deposit-feeder and as such has robust mouthpartsand a robust gastric mill By its regular distribution with anumber of individuals on wood falls by the presence of ahigh proportion of wood or plant debris in the gut of numer-ous specimens by the morphology of its appendages andgastric mill as well as by the regular presence of two kindsof digestive symbionts (bacteria and fungi) M andamanicahas to be regarded as a specialist adapted to feed preferen-tially on terrestrial vegetal remains but also by extension onother hard refractory substrates of animal origin Althoughthe specimens associated with wood appear to feed mainlyon the wood itself ingesting large quantities of xylem tis-sues an important other food source should be the bacteriaand the fungi grazed from bioWlms Comparing the feedinghabits of M andamanica with the ones of other Munidopsisspecies let us think that this species and perhaps some of itscongeners have evolved diVerently from others among the

genus On the other hand M andamanica has developedlasting associations with fungal and bacterial resident gutmicroorganisms which most probably assist digestion ofthe refractory components especially in the case of a wood-based diet

Munidopsis andamanica is likely to be an importantactor in the food chains of deep-sea wood falls through itsability to mechanically degrade wood and to produce as isusual for herbivores feces enriched in nutrients and organicnitrogen (Wafar et al 1997 Skov and Hartnoll 2002) Thisconclusion breaks with the widespread idea that squat lob-sters are generalist scavengers

Acknowledgments The authors thank the chief scientists of theBOA1 and SantoBOA cruises S Samadi and B Richer de Forgesrespectively and also the captains and crews SantoBOA was includedin the Biodiversity expedition Santo MNHNPNIIRD (Co-PI P BouchetO Pascal and H Le Guyader) that was supported by grants from theTotal Foundation The authors also gratefully acknowledge the excel-lent technical assistance of N Decloux with transmission and scanningelectron microscopy Thanks are also due to E Macpherson for the tax-onomic determination of the specimens Thanks also go to the review-ers for providing constructive comments on the manuscript This workis included in the GDRE-DIWOOD research program (ldquoDiversityEstablishment and Function of Organisms Associated with MarineWood Fallsrdquo) directed by F Gaill and was supported by the BelgianFund for Joint Basic Research (FRFC Belgium conventionno 2459407F) Caroline Hoyoux is a PhD student fellow of theFRSndashFNRS (National Fund for ScientiWc Research Belgium)

References

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Baba K (1988) Chirostylid and Galatheid crustaceans (DecapodaAnomura) of the ldquoAlbatrossrdquo Philippine expedition 1907-1910Researches on Crustacea Special Number 2 v + 203 p

Baba K (2005) Deep-sea Chirostylid and Galatheid crustaceans (Deca-poda Anomura) from the Indo-PaciWc with a list of the speciesGalathea report 20 317 p

Baba K Macpherson E Poore GC Ahyong ST Bermudez A CabezasP Lin C-W Nizinski M Rodrigues C Schnabel K (2008) Cata-logue of squat lobsters of the world (Crustacea DecapodaAnomuramdashfamilies Chirostylidae Galatheidae and Kiwaidae)Zootaxa 19051ndash220

Bayon C (1980) Volatile fatty acids and methane production in relationto anaerobic carbohydrate fermentation in Oryctes nasicornislarvae (Coleoptera Scarabaeidae) J Insect Physiol doi1010160022-1910(80)90098-0

Bennett BA Smith CR Glaser B Maybaum HL (1994) Faunal com-munity structure of a chemoautotrophic assemblage on whalebones in the deep northeast PaciWc Ocean Mar Ecol Prog Ser108205ndash223

Bignell D (1984) The arthropod gut as an environment for microorgan-isms In Anderson J Rayner A Walton D (eds) Invertebrate-microbial interactions Cambridge University Press Cambridgepp 205ndash227

Block RJ Bolling D (1938) The amino acid composition of keratins-the composition of gorgonin spongin turtle scutes and otherkeratins J Biol Chem 127685ndash693

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Brecko D Strus J (1992) The morphology of the hindgut in semi-ter-restrial and terrestrial isopods In Proceedings of the 1st Euro-pean Crustacean conference Paris pp 17ndash18

Bricage P (1998) La Survie des Systegravemes Vivants In Atelier MCX20Prendre soin de lrsquohomme Programme Europeacuteen Modeacutelisation dela Complexiteacute MCX Pau 19 Oct 1998 3 p

Bricage P (2000) Systegravemes biologiques Le jeu de la croissance et dela survie Quelles regravegles Quelles deacutecisions Quels bilans In Ladeacutecision systeacutemique du biologique au social AFSCET Paris6 p

Caine EA (1974) Feeding of Ovalipes guadulpensis (Saussure) (Deca-poda Brachyura Portunidae) and morphological adaptations toa burrowing existence Biol Bull 147550ndash559

Cayreacute P Richer de Forges B (2002) Faune mysteacuterieuse des oceacuteansprofonds La Recherche 35559ndash62

Ceccaldi HJ (2006) The digestive tract anatomy physiology and bio-chemistry In Forest J von Vaupel Klein JC (eds) Treatise onzoologymdashanatomy taxonomy biologymdashthe crustacea vol 2Brill Leiden Boston pp 85ndash203

Chevaldonneacute P Olu K (1996) Occurrence of anomuran crabs (Crusta-cea Decapoda) in hydrothermal vent and cold-seep communitiesa review Proc Biol Soc Wash 109(2)286ndash298

Coelho VR Rodrigues SA (2001) Trophic behaviour and functionalmorphology of the feeding appendages of the laomediid shrimpAxianassa australis (Crustacea Decapoda Thalassinidea) J MarBiol Ass UK 81441ndash454

Coen LD (1987) Plant-Animal interactions ecology and functionalcomparative morphology of plant-grazing decapod (brachyuran)crustaceans PhD dissertation University of Maryland

Costerton JW Ingram JM Cheng K-J (1974) Structure and function ofthe cell envelope of gram-negative bacteria Bact Rev 38(1)87ndash110

Crain JA (1999) Functional morphology of prey ingestion byPlacetron wosnessenskii Schalfeew Zoeae (Crustacea AnomuraLithodidae) Biol Bull 197207ndash218

Cundell AM Brown MS Stanford R Mitchell R (1979) Microbialdegradation of Rhizophora mangle leaves immersed in the seaEast Coast Mar Sci 9281ndash286

Dall W (1967) The functional anatomy of the digestive tract of ashrimp Metapeneaus bennettae Racek and Dall (CrustaceaDecapoda Penaedae) Aust J Zool 15699ndash714

Dempsey AC Kitting CL (1987) Characteristics of bacteria isolatedfrom penaeid shrimp Crustaceana 52(1)90ndash94

Distel DL Roberts SJ (1997) Bacterial endosymbionts in the gills ofthe deep-sea wood-boring bivalves Xylophaga atlantica and Xyl-ophaga washingtona Biol Bull 192253ndash261

Distel DL Baco AR Chuang E Morrill W Cavanaugh C Smith CR(2000) Do mussels take wooden steps to deep-sea vents Naturedoi10103835001667

Dolan MF (2001) Speciation of termite gut protists the role of bacte-rial symbionts Int Microbiol 4203ndash208

Douglas AE (1994) Symbiotic interactions Oxford University PressOxford doi101017S0025315400047810

Duperron S Laurent MCZ Gaill F Gros O (2008) Sulphur-oxidizingextracellular bacteria in the gills of Mytilidae associated withwood falls FEMS Microbiol Ecol doi101111j1574-6941200800438x

Dupont J Rousseau F Zbinden M Freacutebourg G Samadi S Gaill F(2005) Systematics investigations on a deep sea Ascomyceterecovered from wood samples In 3rd international symposiumon hydrothermal vent and seep biology

Erasmus JH Cook PA Coyne VE (1997) The role of bacteria in thedigestion of seaweed by the abalone Haliotis midae Aquaculturedoi101016S0044-8486(97)00112-9

Escobar-Briones E Morales P Cienfuegos E Gonzaacuteles M (2002)Carbon sources and trophic position of two abyssal species of

Anomura Munidopsis alvisca (Galatheidae) and Neolithodesdiomedeae (Lithodidae) In Hendrickx ME (ed) Contributions tothe study of East PaciWc crustaceans Instituto de Ciencias del Mary Limnologiacutea UNAM pp 37ndash43

Factor JR (1978) Morphology of the mouthparts of larval lobstersHomarus americanus (Decapoda Nephropidae) with specialemphasis on their setae Biol Bull doi1023071541067

Felgenhauer B (1992) Internal anatomy of the Decapoda an over-view In Harrison F Humes A (eds) Microscopic anatomy ofinvertebrates Decapod Crustacea vol 10 Wiley-Liss NewYork pp 44ndash75

Felgenhauer BE Abele LG (1985) Feeding structures of two atypidshrimps with comments on caridean phylogeny J Crust Biol5397ndash419

Foglesong MA Walker DH Jr PuVer JS Markovetz AJ (1975)Ultrastructural morphology of some prokaryotic microorganismsassociated with the hindgut of cockroaches J Bacteriol123(1)336ndash345

Garm A (2004) Revising the deWnition of the crustacean seta and setalclassiWcation systems based on examinations of the mouthpartsetae of seven species of decapods Zool J Linn Soc doi101111j1096-3642200400132x

Garm A Hoslasheg JT (2001) Function and functional groupings of thecomplex mouth apparatus of the squat lobsters Munida sarsi Huusand M tenuimana GO Sars (Crustacea Decapoda) Biol Bull200281ndash297

Giddins RL Lucas JS Neilson MJ Richards GN (1986) Feeding ecol-ogy of the mangrove crab Neosarmatium smithi (CrustaceaDecapoda Sesarmidae) Mar Ecol Prog Ser 33147ndash155

GoVredi SK Paull CK Fulton-Bennett K Hurtado LA Vrijenhoek RC(2004) Unusual benthic fauna associated with a whale fall inMonterey Canyon California Deep Sea Res I doi101016jdsr200405009

Gore RH (1983) Notes on rare species of Munidopsis (Anomura Gal-atheidae) and Ethusina (Brachyura Dorippidae) collected by theUSNS Bartlett in the Venezuela basin Caribbean Sea Proc AcadNat Sci Phila 135200ndash217

Gros O Gaill F (2007) Extracellular bacterial association in gills ofldquowood musselsrdquo Cah Biol Mar 48(1)103ndash109

Growns IO Richardson AMM (1988) Diet and burrowing habits of thefreshwater crayWsh Parastacoides tasmanicus tasmanicus Clark(Decapoda Parastacidae) Mar Freshw Res 39(4)525ndash534

Guan R-Z Wiles PR (1998) Feeding ecology of the signal crayWshPacifastacus leniusculus in a British lowland river Aquaculturedoi101016S0044-8486(98)00377-9

Hammel KE (1997) Fungal degradation of lignin In Cadisch G GillerKE (eds) Driven by nature plant litter quality and decompositionCAB International Caen pp 33ndash45

Harris JM (1993) The presence nature and role of gut microXora inaquatic invertebrates a synthesis Microb Ecol doi101007BF00171889

Hashimoto JK Ohta S Fujikura K Miura T (1995) Microdistributionpattern and biogeography of the hydrothermal vent communitiesof the Minami-Ensei Knoll in the Mid-Okinawa Trough WesternPaciWc Deep Sea Res doi1010160967-0637(94)00037-S

Hudson IR Wigham BD (2003) In situ observations of predatory feed-ing behaviour of the galatheid squat lobster Munida sarsi (Huus1935) using a remotely operated vehicle J Mar Biol Ass UK83(3)463ndash464

Icely JD Nott JA (1984) On the morphology and Wne structure of thealimentary canal of Corophium volutator (Pallas) (CrustaceaAmphipoda) Philos Trans R Soc Lond B doi101098rstb19840081

Janszligen F Treude T Witte U (2000) Scavenger assemblages underdiVering trophic conditions a case study in the deep Arabian SeaDeep Sea Res II 472999ndash3026

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Kemp KM Jamieson AJ Bagley PM McGrath H Bailey DM CollinsMA Priede IG (2006) Consumption of large bathyal food fall asiw month study in the NE Atlantic Mar Ecol Prog Serdoi103354meps310065

Kiel S Goedert JL (2006a) A wood-fall association from Late Eocenedeep-water sediments of Washington State USA Palaiosdoi102110palo2005p05-086r

Kiel S Goedert JL (2006b) Deep-sea food bonanzas Early Cenozoicwhale-fall communities resemble wood-fall rather than seep com-munities Proc R Soc B doi101098rspb20063620

Kiel S Amano K Hikida Y Jenkins RG (2008) Wood-fall associationsfrom Late Cretaceous deep-water sediments of Hokkaido JapanLethaia doi101111j1502-3931200800105x

Kimura H Harada K Hara K Tamaki A (2002) Enzymatic approachto fungal association with arthopod guts a case study for thecrustacean host Nihonotrypaea harmandi and its foregut fungusEnteromyces callianassae Mar Ecol doi101046j1439-0485200202778x

Kunze J Anderson T (1979) Functional morphology of the mouthpartsand gastric mill in the hermit crabs Clibanarius taeniatus (MilneEdwards) Clibanarius virescens (Krauss) Paguristes squamosusMcCulloch and Dardanus setifer (Milne Edwards) (AnomuraPaguridae) Aust J Mar Freshw Res doi101071MF9790683

Lau WWY Jumars PA Armbrust EV (2002) Genetic diversity ofattached bacteria in the hindgut of the deposit-feeding shrimpNeotrypaea (formerly Callianassa) californiensis (DecapodaThalassinidae) Microb Ecol 43455ndash466

Lichtwardt RW (1996) Trichomycetes and the arthropod gut In How-ard D Miller D (eds) The Mycota animal and human relationsSpringer New York pp 315ndash330

Lindquist N Barber PH Weisz JB (2005) Episymbiotic microbes asfood and defence for marine isopods unique symbioses in a hos-tile environment Proc Biol Sci doi101098rspb20053082

Loacutepez Lastra C (1990) Primera cita de Smittium morbosum var rioplat-ensis var nov (Trichomycetes Harpellales) patoacutegeno de cincoespecies de mosquitos (Diptera Culicidae) en la Repuacuteblica deArgentina Re Arg Mic 1314ndash18

Lorion J Duperron S Gros O Cruaud C Samadi S (2009) Severaldeep-sea mussels and their associated symbionts are able to liveboth on wood and on whale falls Proc Biol Sci doi101098rspb20081101

Macavoy SE Carney RS Morgan E Macko SA (2008a) Stable isotopevariation among the mussels Bathymodiolus childressi and asso-ciated heterotrophic fauna at four cold-seeps communities in theGulf of Mexico J ShellWsh Res doi1029830730-8000(2008)27[147SIVATM]20CO2

Macavoy SE Morgan E Carney RS Macko SA (2008b) Chemoauto-trophic production incorporated by heterotrophs in Gulf ofMexico hydrocarbon seeps an examination of mobile benthicpredators and seep residents J ShellWsh Res doi1029830730-8000(2008)27[153CPIBHI]20CO2

Macpherson E (2007) Species of the genus Munidopsis Whiteaves1784 from the Indian and PaciWc Oceans and reestablishment ofthe genus Galacantha A Milne-Edwards 1880 (Crustacea Deca-poda Galatheidae) Zootaxa 14171ndash135

Macpherson E Segonzac M (2005) Species of the genus Munidopsis(Crustacea Decapoda Galatheidae) from the deep AtlanticOcean including cold-seep and hydrothermal vent areas Zootaxa10951ndash60

Malley DF (1978) Degradation of mangrove leaf litter by the tropicalsesarmid crab Chiromanthes onychophorum Mar Bioldoi101007BF00455032

Margulis L Olendzenski L Afzelius B (1990) Endospore-forming Wl-amentous bacteria symbiotic in termites ultrastructure andgrowth in culture of Arthromitus Symbiosis 8(2)95ndash116

Marshall BA (1985) Recent and tertiary deep-sea limpets of the genusPectinodonta Dall (Mollusca Gastropoda) from New Zealandand New South Wales New Zeal J Zool 12273ndash282

Marshall BA (1988) Skeneidae Vitrinellidae and Orbitestellidae (Mol-lusca Gastropoda) associated with biogenic substrata from bathy-al depths oV New Zealand and New South Wales J Nat Hist22949ndash1004

Martin MM (1992) The evolution of insect-fungus associations fromcontact to stable symbiosis Am Zool doi101093icb324593

Martin JW Jourharzadeh P Fitterer PH (1998) Description and com-parison of major foregut ossicles in hydrothermal vent crabs MarBiol 131259ndash267

Mattson WJ (1980) Herbivory in relation to plant nitrogen contentAnn Rev Ecol Syst doi101146annureves11110180001003

Micheli F Peterson CH Mullineaux LS Fisher CR Mills SW SanchoG Johnson GA Lenihan HS (2002) Predation structure communi-ties at deep-sea hydrothermal vents Ecol Monogr 72(3)365ndash382

Ngoc-Ho N (1984) The functional anatomy of the foregut of Porcellanaplatycheles and a compatison with Galathea squamifera and Upog-ebia deltaura (Crustacea Decapoda) J Zool Lond 203511ndash535

Nickell LA Atkinson RJ (1995) Functional morphology of burrowsand trophic modes of three thalassinidean shrimp species and anew approach to the classiWcation of thalassinidean burrow mor-phology Mar Ecol Prog Ser doi103354rstb19840081

Nickell LA Atkinson RJA Pinn EH (1998) Morphology of thalassin-idean (Crustacea Decapoda) mouthparts and pereiopods in rela-tion to feeding ecology and grooming J Nat Hist doi10108000222939800770381

Oxley AP ShiptonW Owens L McKay D (2002) Bacterial Xora fromthe gut of the wild and cultured banana prawn Penaeus mergui-ensis J Appl Microbiol doi101046j1365-2672200201673x

Pailleret M Haga T Petit P Gill CP Saedlou N Gaill F Zbinden M(2006) Sunken wood from the Vanuatu Islands identiWcation ofwood substrates and preliminary description of associated faunaMar Ecol doi101111j1439-0485200600149x

Palacios C Zbinden M Baco AR Treude T Smith C Gaill F LebaronP Boetius A (2006) Microbial ecology of deep-sea sunkenwoods quantitative measurements of bacterial biomass and cellu-lolytic activities Cah Biol Mar 47415ndash420

Phillips NW (1984) Role of diVerent microbes and substrates as poten-tial suppliers of speciWc essential nutrients to marine detritivoresBull Mar Sci 35283ndash298

Phleger CF Nelson MM Groce AK Cary SC Coyne KJ Nichols PD(2005) Lipid composition of deep-sea hydrothermal vent tube-worm Riftia pachyptila crabs Munidopsis subsquamosa andBythograea thermydron mussels Bathymodiolus sp and limpetsLepetodrilus spp Comp Biochem Physiol B Biochem Mol Biol141196ndash210

Pillai SR (1960) Studies on the shrimp Caridina laevis Heller 1Digestive system J Mar Biol Assoc India 257ndash75

Pinn EH Nickell LA Rogerson A Atkinson RJA (1999) Comparisonof gut morphology and gut microXora of seven species of mudshrimp (Crustacea Decapoda Thalassinidea) Mar Bioldoi101007s002270050448

Plante C Jumars PA Baross JA (1990) Digestive associations betweenmarine detritivores and bacteria A Rev Ecol Syst 2193ndash127

Potrikus CJ Breznak JA (1977) Nitrogen-Wxing Enterobacter agglom-erans isolated from guts of wood-eating termites Appl EnvironMicrobiol 33(2)392ndash399

Powell RR (1974) The functional morphology of the fore-guts of thethallassinid crustaceans Callianassa californiensis and Upogebiapugettensis University of California Press Berkeley

Reynolds JD OrsquoKeeVe C (2005) Dietary patterns in stream- and lake-dwelling populations of Austropotamobius pallipes Bull FrPeche Piscicult 376ndash377715ndash730

123

Mar Biol (2009) 1562421ndash2439 2439

Salindeho IR Johnston DJ (2003) Functional morphology of themouthparts and proventriculus of the rock crab Nectocarcinustuberculosus (Decapoda Portunidae) J Mar Biol Assoc UK83821ndash834

Samadi S Dupont J Rousseau F Haga T Amos G Richer de ForgesB (2005) Campagne BOA1 du NO laquoAlisraquo au Vanuatu du 2 au 18septembre 2005 10 p

Samadi S Queacutemeacutereacute E Lorion J Tillier A Cosel R Lopez P CruaudC Couloux A Boisselier M-C (2007) Phylogenetic position ofsunken woods mytilids C R Biol 330(5)446ndash456

Schembri PJ (1982) Functional morphology of the mouthparts andassociated structures of Pagurus rubricatus (Crustacea Deca-poda Anomura) with special reference to feeding and groomingZoomorphology 10117ndash38

Schwarz JR Yayanos AA Colwell RR (1976) Metabolic activity ofthe intestinal microXora of a deep-sea invertebrate Appl EnvironMicrobiol 3146ndash48

Skilleter GA Anderson DT (1986) Functional morphology of thechelipeds mouthparts and gastric mill of Ozius truncates (MilneEdwards) (Xanthidae) and Leptograpsus variegatus (Fabricius)(Grapsidae) (Brachyura) Aust J Mar Freshw Res 3767ndash79

Skov MW Hartnoll RG (2002) Paradoxical selective feeding on a low-nutrient diet why do mangrove crabs eat leaves Oecologia1311ndash7

Smith DC Douglas AE (1987) The biology of symbiosis EdwardArnold Ltd London

Smith CR Kukert H Wheatcroft RA Jumars PA Deming JW (1989)Vent fauna on whale remains Nature 34127ndash28

Smith CR Baco AR Hannides A Ruplinger D (2003) Chemosynthetichabitats on the California slope whale- wood- and kelp-fallscompared to vents and seeps Biogeography and Biodiversity ofChemosynthetic Ecosystems Planning for the Future Southamp-ton Oceanography Centre Southampton UK

Stamhuis EJ Dauwe B Videler JJ (1998) How to bite the dust mor-phology motion pattern and function of the feeding appendagesof the deposit-feeding thalassinid shrimp Callianassa subterra-nea Mar Biol 13243ndash58

Turner RD (1977) Wood mollusks and deep-sea food chains Bull AmMalacol Union 21313ndash19

Van Dover CL Lichtwardt RW (1986) A new trichomycete commen-sal with a galatheid squat lobster from deep-sea hydrothermalvents Biol Bull 171(2)461ndash468

Wafar S Untwale AG Wafar M (1997) Litter fall and energy Xux in amangrove ecosystem East Coast Shelf Sci doi101006ecss19960152

Warner GF (1977) The biology of crabs Elek Science London UKWebster JR BenWeld EF (1986) Vascular plant breakdown in freshwa-

ter ecosystems Annu Rev Ecol Syst 17567ndash594Werner D Barea JM Brewin NJ Cooper JE Katinakis P Lindstrom

K OrsquoGara F Spaink HP Truchet G Muller P (2002) Symbiosisand defence in the interaction of plants with microorganismsSymbiosis 3283ndash104

Williams AB (1988) New marine decapod crustaceans from watersinXuenced by hydrothermal discharge brine and hydrocarboneseepage Fish Bull 86(2)263ndash287

Williams AB Smith CR Baco AR (2000) New species of Paralomis(Decapoda Anomura Lithodidae) from a sunken whale carcassin the San Clemente basin oV southern California J Crust Biol20(special number 2)281ndash285

Wolcott DL OrsquoConnor NJ (1992) Herbivory in crabs adaptations andecological considerations Am Zool doi101093icb323370

Wolcott DL Wolcott TG (1984) Food quality and cannibalism in thered crab Gecarcinus lateralis Physiol Zool 57318ndash324

Wolfe SH Felgenhauer BE (1991) Mouthpart and foregut ontogeny inlarval postlarval and juvenile spiny lobster Panulirus argusLatreille (Decapoda Palinuridae) Zool Scripta doi101111j1463-64091991tb00274x

WolV T (1979) Macrofaunal utilization of plant remains in the deepsea Sarsia 64117ndash136

Wu MF Chan TY Yu HP (1998) On the Chirostylidae and Galathei-dae (Crustacea Decapoda Galatheidea) of Taiwan Annu TaiwanMus 4075ndash153

Zbinden M Cambon-Bonavita M (2003) Occurrence of Deferribacte-rales and Entomoplasmatales in the deep-sea Alvinocarid shrimpRimicaris exoculata gut FEMS Microbiol Ecol doi101016S0168-6496(03)00176-4

Zimmer M Bartholmeacute S (2003) Bacterial endosymbionts in Asellusaquaticus (Isopoda) and Gammarus pulex (Amphipoda) and theircontribution to digestion Limnol Oceanogr 48(6)2208ndash2213

Zimmer M Topp W (1998) Microorganisms and cellulose digestion inthe gut of the woodlouse Porcellio scaber J Chem Ecol24(8)1397ndash1408

Zook D (1998) A new symbiosis language ISS Symbiosis News1(3)1ndash3

Zurek L Keddie BA (1998) SigniWcance of methanogenic symbiontsfor development of the American cockroach Periplaneta ameri-cana J Insect Physiol doi101016S0022-1910(98)00024-9

123

2422 Mar Biol (2009) 1562421ndash2439

most represented species Several recent cruises (BOA1-2005 SantoBOA-2006 SalomonBOA3-2007) have con-Wrmed its regular association to deep-sea wood fallsIndividuals are commonly found on the surface of thesunken wood pieces However nothing is known about itsdiet and trophic dependency to wood or to the wood fallecosystem Does it feed directly on wood or does it scavengeor practice predation on other organisms associated to itIn addition since sunken woods are not only refractorysubstrates (ie containing cellulose lignin) but alsoreducing chemosynthetic-based ecosystems does M and-amanica realize symbiotic associations with microorgan-isms either to digest wood or to exploit reducingcompounds as energy sources Is it speciWcally associatedto sunken wood or not Indeed M andamanica were pre-viously collected in other locations and perhaps on othersubstrates (not reported) in the Andaman Sea along thewest coast of Sumatra and in the waters of the Moluccasthe Philippines the South China Sea (Baba 1988) Taiwan(Wu et al 1998) Indonesia the Solomon Islands NewCaledonia and the Vanuatu and Fiji Islands at depths of333ndash1598 m (Macpherson 2007)

On the other hand the genus Munidopsis Whiteaves1874 is distributed worldwide in all deep-sea habitats andcommonly found living deeper than 500 m and down to2000 m on continental slopes and abyssal plains (Baba1988 2005 Macpherson and Segonzac 2005) Interest-ingly their presence is also reported in vent- and cold-seep communities (Williams 1988 Hashimoto et al 1995Chevaldonneacute and Olu 1996) as well as on whale andwood falls (Bennett et al 1994 GoVredi et al 2004Samadi et al 2005) Although few studies focused ontheir diet they are commonly thought to be scavengerswhile their feeding habits are much diversiWed and notclearly established Some species from hydrothermalvents such as M marionis M acutispina and anotherMunidopsis sp (complete name is not mentioned) wouldbe predators or scavengers (Chevaldonneacute and Olu 1996Macavoy et al 2008a) while M alvisca M subsquamosaM geyeri and another Munidopsis sp appeared to have amixed diet composed of organic debris of the sedimentpolychaetes limpets crab larvae and would also grazethe bacteria of the bioWlms (Van Dover and Lichtwardt1986 Escobar-Briones et al 2002 Micheli et al 2002Phleger et al 2005) Nothing is reported about the diet ofM cascadia M yaquiensis M verrilli and M quadratathat are found associated to whale carcasses (Williamset al 2000) However experimental studies showed thatM crassa and another Munidopsis sp would be scaveng-ers of bone remnants (Janszligen et al 2000 Kemp et al2006 Macavoy et al 2008b) In addition other species(M serricornis M sarissa) were found in gorgonians orsponges and would perhaps feed on the organic matter or

even on the tissues of these organisms (Macpherson andSegonzac 2005)

The aim of the present study was to describe and specifythe diet of the M andamanica specimens associated towood falls from Vanuatu in order to have a better under-standing about the role they play in these particular ecosys-tems In addition comparisons with specimens from Wveother geographic areas were carried out to determinewhether M andamanica is a specialist of sunken woods oran opportunistic generalist with various food sources ascommonly admitted for squat lobsters

We also looked for microorganisms in the digestivetract in order to determine whether the specimens ofM andamanica have developed digestive andor chemo-synthetic microbial symbioses Indeed previous studieshave highlighted chemosynthetic bacterial symbioses inthe branchial tissues of bivalves from wood falls (Disteland Roberts 1997 Gros and Gaill 2007 Duperron et al2008) and the digestion of vegetal cells often implies aheterotrophic gut microXora providing the host with exo-enzymes for metabolizing constituents of plant cell wallssuch associations are well known in xylophagous insects(Foglesong et al 1975 Potrikus and Breznak 1977Bayon 1980 Bignell 1984 Margulis et al 1990 Zurekand Keddie 1998 Dolan 2001)

Materials and methods

Biological material

Specimens of M andamanica associated to wood fallswere collected oV Vanuatu Islands during the BOA1cruise (September 2005 Vanuatu) and during the Santo-BOA cruise (October 2006) on the RV Alis Duringthese cruises the large bay (Big Bay) located at the northof Espiritu Santo Island in Vanuatu was thoroughlyexplored by trawling Over the two cruises 55 stationswere explored in this bay at depth ranging from 150 to1000 m Most of the time trawl brought back sunkenwoods and other plant debris The sunken plant materialwas always associated to a speciWc fauna Among otherorganisms wood-boring bivalves of the genus Xyloph-aga wood-eating limpets of the genus Pectinodonta andwood or reed housing hermit crabs of the genus Xylopag-urus were very abundant During these cruises M and-amanica were repeatedly caught in relatively greatnumber together with woods other plant debris and thetypical associated fauna We here examined six speci-mens from the wood falls of Vanuatu four from thestation CP2432 (14deg597S 166deg550E 630ndash705 m 08Sep 2005 BOA1) one from the station CP2421(14deg571S 166deg551E 677ndash771 m 06 Sep 2005

123

Mar Biol (2009) 1562421ndash2439 2423







123

2424 Mar Biol (2009) 1562421ndash2439



LM and TEM


DAPI staining



Results





123

Mar Biol (2009) 1562421ndash2439 2425



Third maxillipeds




123

2426 Mar Biol (2009) 1562421ndash2439

First maxillae


Mandibles




Gastric mill




123

Mar Biol (2009) 1562421ndash2439 2427




Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

123

2428 Mar Biol (2009) 1562421ndash2439




123

Mar Biol (2009) 1562421ndash2439 2429



123

2430 Mar Biol (2009) 1562421ndash2439



Gut microorganisms





123

Mar Biol (2009) 1562421ndash2439 2431

Discussion







123

2432 Mar Biol (2009) 1562421ndash2439





123

Mar Biol (2009) 1562421ndash2439 2433


How does it feed









123

2434 Mar Biol (2009) 1562421ndash2439









123

Mar Biol (2009) 1562421ndash2439 2435








123

2436 Mar Biol (2009) 1562421ndash2439







References









123

Mar Biol (2009) 1562421ndash2439 2437










































123

2438 Mar Biol (2009) 1562421ndash2439






































123

Mar Biol (2009) 1562421ndash2439 2439






























123

Mar Biol (2009) 1562421ndash2439 2423







123

2424 Mar Biol (2009) 1562421ndash2439



LM and TEM


DAPI staining



Results





123

Mar Biol (2009) 1562421ndash2439 2425



Third maxillipeds




123

2426 Mar Biol (2009) 1562421ndash2439

First maxillae


Mandibles




Gastric mill




123

Mar Biol (2009) 1562421ndash2439 2427




Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

123

2428 Mar Biol (2009) 1562421ndash2439




123

Mar Biol (2009) 1562421ndash2439 2429



123

2430 Mar Biol (2009) 1562421ndash2439



Gut microorganisms





123

Mar Biol (2009) 1562421ndash2439 2431

Discussion







123

2432 Mar Biol (2009) 1562421ndash2439





123

Mar Biol (2009) 1562421ndash2439 2433


How does it feed









123

2434 Mar Biol (2009) 1562421ndash2439









123

Mar Biol (2009) 1562421ndash2439 2435








123

2436 Mar Biol (2009) 1562421ndash2439







References









123

Mar Biol (2009) 1562421ndash2439 2437










































123

2438 Mar Biol (2009) 1562421ndash2439






































123

Mar Biol (2009) 1562421ndash2439 2439






























123

2424 Mar Biol (2009) 1562421ndash2439



LM and TEM


DAPI staining



Results





123

Mar Biol (2009) 1562421ndash2439 2425



Third maxillipeds




123

2426 Mar Biol (2009) 1562421ndash2439

First maxillae


Mandibles




Gastric mill




123

Mar Biol (2009) 1562421ndash2439 2427




Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

123

2428 Mar Biol (2009) 1562421ndash2439




123

Mar Biol (2009) 1562421ndash2439 2429



123

2430 Mar Biol (2009) 1562421ndash2439



Gut microorganisms





123

Mar Biol (2009) 1562421ndash2439 2431

Discussion







123

2432 Mar Biol (2009) 1562421ndash2439





123

Mar Biol (2009) 1562421ndash2439 2433


How does it feed









123

2434 Mar Biol (2009) 1562421ndash2439









123

Mar Biol (2009) 1562421ndash2439 2435








123

2436 Mar Biol (2009) 1562421ndash2439







References









123

Mar Biol (2009) 1562421ndash2439 2437










































123

2438 Mar Biol (2009) 1562421ndash2439






































123

Mar Biol (2009) 1562421ndash2439 2439






























123

Mar Biol (2009) 1562421ndash2439 2425



Third maxillipeds




123

2426 Mar Biol (2009) 1562421ndash2439

First maxillae


Mandibles




Gastric mill




123

Mar Biol (2009) 1562421ndash2439 2427




Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

123

2428 Mar Biol (2009) 1562421ndash2439




123

Mar Biol (2009) 1562421ndash2439 2429



123

2430 Mar Biol (2009) 1562421ndash2439



Gut microorganisms





123

Mar Biol (2009) 1562421ndash2439 2431

Discussion







123

2432 Mar Biol (2009) 1562421ndash2439





123

Mar Biol (2009) 1562421ndash2439 2433


How does it feed









123

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First maxillae


Mandibles




Gastric mill




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Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

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Gut microorganisms





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Discussion







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How does it feed









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References









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Hindgut











Gut contents



Tests of protists

Organic matter

Plant remains


Vanuatu 6 ++++ +++ +++ ++ +++ +++ ++++ ++++

Solomon 4 ++++ +++ ++ +++ +++ ++++ + ++++

New Caledonia 1 ++ + +++ ++ +++ ++ +++ +++ ++ ++

Fiji 1 +++ +++ +++ ++ +++ +++ +++

Indonesia 1 ++ ++ + +++ ++ ++ +++ ++

Philippines 1 +++ ++ ++ +++ ++ +++ +++ ++ ++++

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Gut microorganisms





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Discussion







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How does it feed









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References









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Gut microorganisms





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Discussion







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How does it feed









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Gut microorganisms





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Discussion







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How does it feed









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References









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Gut microorganisms





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Discussion







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How does it feed









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References









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Discussion







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How does it feed









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References









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How does it feed









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References









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How does it feed









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References









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Wood-based diet and gut microflora of a galatheid crab associated with Pacific deep-sea wood falls

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Transcript of Wood-based diet and gut microflora of a galatheid crab associated with Pacific deep-sea wood falls