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ResearchCite this article Scheyer TM Delfino MKlein N Bunbury N Fleischer-Dogley FHansen DM 2018 Trophic interactions betweenlarger crocodylians and giant tortoises onAldabra Atoll Western Indian Ocean duringthe Late Pleistocene R Soc open sci 5 171800httpdxdoiorg101098rsos171800

Received 3 November 2017Accepted 6 December 2017

Subject CategoryBiology (whole organism)

Subject Areaspalaeontologypalaeontologyevolution

KeywordsSeychelles predatorndashprey interactionscavenging Testudines AldabrachelysAldabrachampsus

Authors for correspondenceTorsten M Scheyere-mail tscheyerpimuzhchDennis M Hansene-mail dennishansenieuuzhch

Trophic interactionsbetween larger crocodyliansand giant tortoises onAldabra Atoll WesternIndian Ocean during theLate PleistoceneTorsten M Scheyer1 Massimo Delfino23 Nicole Klein4

Nancy Bunbury5 Frauke Fleischer-Dogley5 and

Dennis M Hansen61University of Zurich Palaeontological Institute and Museum Karl Schmid-Strasse 48006 Zurich Switzerland2Dipartimento di Scienze della Terra Universitagrave di Torino Via Valperga Caluso 35I-10125 Torino Italy3Institut Catalagrave de Paleontologia Miquel Crusafont Universitat Autogravenoma deBarcelona Edifici ICTA-ICP Carrer de les Columnes sn Campus de la UABCerdanyola del Vallegraves Barcelona 08193 Spain4Steinmann Institut fuumlr Geologie Palaumlontologie und Mineralogie Universitaumlt BonnNussallee 8 53115 Bonn Germany5Seychelles Islands Foundation PO Box 853 Victoria Maheacute Seychelles6Zoological Museum and the Department of Evolutionary Biology and EnvironmentalStudies University of Zurich Winterthurerstrasse 190 8057 Zurich Switzerland

TMS 0000-0002-6301-8983 MD 0000-0001-7836-7265DMH 0000-0002-9584-2766

Today the UNESCO World Heritage Site of Aldabra Atoll ishome to about 100 000 giant tortoises Aldabrachelys giganteawhose fossil record goes back to the Late Pleistocene NewLate Pleistocene fossils (age ca 90ndash125 000 years) from theatoll revealed some appendicular bones and numerous shellfragments of giant tortoises and cranial and postcranialelements of crocodylians Several tortoise bones show circularholes pits and scratch marks that are interpreted as bite marksof crocodylians The presence of a Late Pleistocene crocodylianspecies Aldabrachampsus dilophus has been known for sometime but the recently found crocodylian remains presentedherein are distinctly larger than those previously describedThis indicates the presence of at least some larger crocodylianseither of the same or of a different species on the atoll These

2018 The Authors Published by the Royal Society under the terms of the Creative CommonsAttribution License httpcreativecommonsorglicensesby40 which permits unrestricteduse provided the original author and source are credited

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larger crocodylians likely the apex predators in the Aldabra ecosystem at the time were well capableof inflicting damage on even very large giant tortoises We thus propose an extinct predatorndashpreyinteraction between crocodylians and giant tortoises during the Late Pleistocene when both groupswere living sympatrically on Aldabra and we discuss scenarios for the crocodylians directly attackingthe tortoises or scavenging on recently deceased animals

1 BackgroundThe identification of species interactions in the form of predation is fundamental to understandecosystem complexity and community structure [1] but evidence of predatorndashprey interactions is rarelypreserved in the fossil record [2] Known cases are either related to rare direct evidence such as findinginterlocked and associated skeletons (eg [34]) or isolated teeth embedded in or around bones [56] andmore frequently stomach contents and feeding traces (eg [7ndash10])

Predation specifically on Testudines (turtles and tortoises) has been documented in the fossil recordand manifold predators have been identified including fishes reptiles and mammals (eg [11]) Besidestortoise remains with cut marks and tooth marks or those found associated with tools left by humans(among others [12ndash15]) Late Cretaceous protostegid turtles were reported to have been bitten by sharks[16] an undetermined Late Cretaceous marine turtle has been ingested by a large lamniform shark[17] and mosasaurs are thought to be the cause of circular depression bite marks in the shell bonesof Cretaceous sea turtles such as Protostega gigas [18ndash20] Badger predation on a European pond turtlein the Holocene was reported where the attack occurred from the anterior opening of the turtle shellleaving irregular bite marks [2] Protostegid turtle remains also showed up as gut content in an EarlyCretaceous ichthyosaur (Platypterygius longmani) from Australia [21] Finally compression puncturesand tapering scratches have been identified as bite marks in a number of fossil turtles from the Eoceneof North America caused by either mammals (carnivorans lsquocreodontsrsquo and lsquocondylarthrsquo mammals) orcrocodylians such as Borealosuchus and Allognathosuchus among others [22]

Indeed crocodylian predation on turtles (only a few are given here see [23] for more documentedexamples) would be expected to be common as these two groups often occur in the same habitat[10] Early Campanian protostegid turtles (Chelospargis advena) and marine pleurodire turtles (egChedighaii barberi) were likely bitten by the giant alligatorid Deinosuchus [24] leaving round- or teardrop-shaped crater-like collapse structures or circular holes in the shell bones Possible crocodylian bitingtraces on bones (including turtle shell bones) that do not pierce the bones were described as theichnofossil Machichnus bohemicus from the Miocene Ahniacutekov site in Czech Republic [2526] Similarmarks were also found on an early Palaeocene turtle shell fragment from Denmark [27] Predationon a Late Cretaceous bothremydid turtle (Foxemys) in Iharkuacutet Hungary was probably done by alarge Allodaposuchus-like crocodyliform [10] The authors point out however that an adult specimenof Foxemys would likely have been too large to be directly attacked by an eusuchian crocodyliformand that it would thus be more reasonable to assume the crocodyliform was scavenging on an alreadydead individual

To positively identify potential predation on fossils comparison with extant evidence is necessaryBinford [28] developed a classification scheme for bite marks and feeding traces which still serves asbasis for many subsequent studies (and is also followed herein) such as those of Drumheller amp Brochu[2329] which also reported a broad spectrum of extant animals that can act as turtle predators Accordingto contact area penetration depth and movement criteria of the teeth feeding traces on bones can beclassified as pits punctures scores and furrows [28] with the former two categories lacking lateralmovement of the marking tooth (also see [23] for further discussion)

Tiger sharks bite out large parts of shell and soft tissues of marine turtles [30ndash32] (see also [33] forfurther discussion) whereas attacks on leatherback turtles by crocodiles (likely by Crocodylus porosusrather than the smaller C novaeguineae though not explicitly stated therein) included decapitation ofone individual in shallow waters close to a nesting beach site near Piguwa Papua New Guinea [34] Arange of terrestrial mammals including racoons bears coyotes badgers and jaguars prey on turtles andtortoises both on hatchlings and on larger individuals [35ndash37] Predation on hatchlings or small juvenileturtles as well as on tortoises is also documented for birds [3839] and crabs [40] These predatorsusually lack the necessary forces to puncture older individualsrsquo shells with their beaks and claws [3341]Predatory birds are known to overcome this by dropping turtlestortoises from great heights to crackthem open [42] and at least the coconut crab Birgus latro has strong enough chelae to sever limbs and

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crush bones of larger-sized turtles and tortoises [43] Predation by dwarf caimans on red-eared sliders[44] is evidenced by scratches and puncture marks and in a documented case the turtle shell was crushedwith the bridge region in a vertical orientation Similar cases of predation by Alligator mississippiensis[45] have been observed but the shells can also be crushed when held in horizontal position Forthat hard-shelled prey items such as turtles are often manipulated to the posterior part of the snoutby crocodylians either inertially or gravitationally [46ndash48] Despite attempts to classify some extinctcrocodylians as specifically lsquocheloniphagousrsquo (turtle-eating) taxa (eg [49ndash53]) globular teeth are notnecessarily an indicator that turtles are part of the diet [54] (see [1045] for further discussion) Predationmarks on the extinct Bahamas giant tortoise Chelonoidis alburyorum were suggested to have been causedby the Cuban crocodile Crocodylus rhombifer [55] This crocodile is usually 2ndash25 m in body length butcan reach up to 35 m with a recorded maximum size of 49 m [5657] The crocodile-inflicted bite marksin the form of sub-circular or ovoid holes on the shell were in some cases healed over providing evidencethat this giant tortoise survived the initial attack

Modern giant tortoises in the Seychelles and those of the Galapagos Islands are much larger than thegiant tortoise from the Bahamas and they currently do not share habitats with crocodylians In the recentpast however at least on the Seychelles and on Madagascar giant tortoises and crocodylians seem tohave shared habitats and thus probably interacted with each other [58ndash61] Little is known on the otherhand about the palaeobiogeographic history and body size evolution of the Aldabran crocodylians andtheir impact on the ancient island ecosystem We here thus report on novel fossil remains from Aldabraproviding the first evidence of a trophic interaction in the form of predation of larger crocodylians on thegiant tortoises during the Late Pleistocene

2 Material and methods21 FossilsRecent surface collection by a research team led by one of us (DH) in the surrounding area of a pondon Grande Terre Island on Aldabra yielded over 180 individual fossilized bones most coming fromcrocodylians and the shells of giant tortoises Several tortoise bones carry conspicuous sub-circular holescompletely piercing the elements or pits that did not penetrate the bone and other marks on the bonesurface that are identifiable as feeding traces The giant tortoise remains studied herein (figure 1) includeone large nuchal with first left peripheral attached (SNHM 144817) one small nuchal (SNHM 144917)a larger costal fragment (SNHM 145017) a smaller costal fragment with sulcus (SNHM 145117) asmaller (SNHM 145217) and a larger (SNHM 145317) hyo- or hypoplastron fragment one small shellfragment (SNHM 145417) which might also pertain to a costal and a pelvic girdle consisting of thedistal part of a right ilium (SNHM 145517) and associated fused pubes (SNHM 145617) and fusedischia (SNHM 145717)

The crocodylian remains studied herein (figure 2) include one large left dentary fragment with alveolid3ndashd8 preserved (SNHM 145817) a small left dentary fragment with alveoli d4ndashd6 preserved (SNHM145917) a skull roof fragment consisting mainly of the left postorbital sutured to small parts of thefrontal and parietal (SNHM 146017) one dorsal procoelous vertebra with neural arch showing onlypostzygapophyses (SNHM 146117) one strongly eroded procoelous vertebral centrum still preservingthe prezygapophyses (SNHM 146217) one isolated left prezygapophysis (SNHM 146317) and theposterior half of an osteoderm (SNHM 146417)

Some of the crocodylian material belongs to an individual or individuals that are considerably largerthan has been previously reported for the only described crocodylian from Aldabra Aldabrachampsusdilophus Brochu 2006 [62] The possibility remains that the new material does not belong to A dilophusbut could represent a larger-sized species eg osteolaemines close to Voay robustus (note that thepostorbital region in V robustus shows peculiar tuberosities not present in the new sample [63]) orCrocodylus niloticus instead (see [62])

All described material derives from calcarenitic sediments of Late Pleistocene age the so-calledAldabra Limestone with an age of 90 000ndash125 000 years [64] surrounding a partially dried-out pondon Grande Terre Island (coordinates S0942759 E04651408) All specimens are stored in the SeychellesNatural History Museum (SNHM) The bones were cleaned and prepared with a set of pneumatic scribetools and measurements were taken with an iGaging digital caliper Photographs were taken with aNikon D2X camera and Nikon AF Nikkor 35ndash70 mm lens and resulting images were processed withAdobe CREATIVE SUITE CS6 A summary of individual measurements has been compiled into tables 1and 2

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(a)

(b)(c) (d)

(e)

( f ) (g)

(h)

(i) (k)

( j)

200 mm

100 mm

100 mm

100 mm

100 mm

100 mm100 mm 100 mm

100 mm

200 mm

100 mm

Figure 1 Overviewof newgiant tortoisematerial from the Late PleistoceneofAldabraAtoll (a) Largenuchal (SNHM144817) still suturedto first left peripheral in dorsal and ventral view (b) small nuchal (SNHM 144917) in dorsal and ventral view note cervical scute in bothnuchals (c) larger costal fragment (SNHM 145017) in ventral view (d) a smaller costal fragment (SNHM 145117) with sulcus in dorsaland ventral view (e) smaller hyo- or hypoplastron fragment (SNHM 145217) in ventral and dorsal view (f ) larger hyo- or hypoplastronfragment (SNHM 145317) in ventral and dorsal view (g) small shell fragment (SNHM 145417) which might also pertain to a costal inpurported dorsal view (hndashk) associated pelvic girdle elements (h) distal part of an ilium in lateral and medial view (SNHM 145517) (i)fused pubes in angled anterodorsal view (SNHM 145617) (j) fused ischia in angled posterodorsal angled posteroventral and posteriorview (SNHM 145717) (k) fused pubes and ischia in natural articulated position in dorsal view

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(a) (b)

100 mm

100 mm

100 mm

100 mm

100 mm

100 mm

100 mm

(c)

(d) (g)

(e)( f )

Figure 2 Overview of new crocodylian material from the Late Pleistocene of Aldabra Atoll (a) Larger left dentary fragment (SNHM145817) with alveoli d3ndashd8 preserved in dorsal medial and lateral view (b) small left dentary fragment (SNHM 145917) with alveolid4ndashd6 preserved in dorsal and ventral view (c) skull roof fragment (SNHM 146017) consisting mainly of the left postorbital andpartial frontal and parietal fragments in dorsal and ventral view (d) dorsal procoelous vertebra (SNHM 146117) with neural archpreserving the postzygapophyses in left lateral right lateral and anterior view (e) strongly eroded vertebral centrum still preservingthe prezygapophyses (SNHM 146217) in dorsal ventral right lateral and anterior view (f ) isolated left prezygapophysis (SNHM 146317)in dorsal view (g) posterior half of osteoderm (SNHM 146417) in dorsal ventral and posterior view

22 Institutional abbreviationsBMNH Natural History Museum London UK SNHM Seychelles Natural History Museum VictoriaMaheacute Island Seychelles ZM Zoological Museum University of Zurich

3 ResultsThe newly collected crocodylian material includes three skull and mandible fragments and postcranialremains (three vertebral remains and an osteoderm fragment) Based on the lack of diagnostic featuresthe fossils were identified only as Crocodyloidea indet based on the diastema after the eighth dentary

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Table 1 Measurements of fossilised crocodylian remains (in mm rounded to the first decimal place)

crocodylian remains

larger left dentary fragment (SNHM 145817)

maximum length 1175 as preserved

anterior maximumwidth 373

posterior maximumwidth 265

maximum height at fourth dentary alveolus 366

maximum height at ninth dentary alveolus 301

symphysial scar 298 as preserved

width of dentary alveolus 3 61

width of dentary alveolus 4 153

width of dentary alveolus 5 94

width of dentary alveolus 6 97

width of dentary alveolus 7 97

width of dentary alveolus 8 87

width of dentary alveolus 9 82

width of dentary alveolus 10 117

thickness of bone wall separating dentary alveoli 7 and 8 62

thickness of bone wall separating dentary alveoli 8 and 9 112

thickness of bone wall separating dentary alveoli 9 and 10 49

smaller left dentary fragment (SNHM 145917)

maximum length 418 as preserved

maximumwidth 253

maximum thickness 181 as preserved

width of dentary alveolus 4 93

width of dentary alveolus 5 79

width of dentary alveolus 6 82

skull roof fragment (SNHM 146017)

maximum length 391

maximumwidth 401

maximum thickness (excluding ventral postorbital pillar) 123

dorsal procoelous vertebra (SNHM 146117)

maximum length of centrum 427

maximumwidth of centrum (anterior border) 311

maximum height of centrum (anterior border to floor of central canal) 276

length of neural arch 335 as preserved

height of neural arch 216 as preserved

width of neural arch (at postzygapophyses) 228

maximum diameter of neural canal 97

strongly eroded vertebra (SNHM 146217)

maximum length of centrum 365

maximumwidth of centrum (anterior border) 263

maximum height of centrum (anterior border to floor of central canal) 162

(Continued)

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Table 1 (Continued)

crocodylian remains

width of neural arch (at prezygapophyses) 467 (as preserved)

maximum diameter of neural canal 91

length of prezygapophyseal articulation facet 21

width of prezygapophyseal articulation facet 117

isolated left prezygapophysis (SNHM 146317)

length of prezygapophyseal articulation facet 231

width of prezygapophyseal articulation facet 166

osteoderm fragment (SNHM 146417)

maximum length 179 as preserved

maximumwidth 398

maximum height at median keel 93

alveolus (see also [65]) Compared to extant C niloticus [6667] both the size of the dentary fragmentsand vertebrae ( table 1) as well as the isolated left prezygapophysis which shows 13 incremental growthmarks on the articular facet (figure 2f ) indicate that the bones were derived from sexually matureindividual(s) This assessment is supported by the complete closure of the neurocentral sutures betweenthe vertebral centra and arches [68]

The newly collected tortoise material included mostly shell bones and fragments (table 2) and also awell-preserved associated pelvic girdle Both nuchals carry imprints of a cervical scute and are overallmorphologically indistinguishable from modern Aldabrachelys gigantea (Schweigger 1812) [69] This wasalready noted on earlier collections of Pleistocene tortoise material from Aldabra [70] Comparison ofthe large nuchal with shells of extant A gigantea (figure 3) indicates an overall size of 100ndash120 cm curvedcarapace length (CCL) of the complete fossil shell Notably this size is considerably larger than thoseof A gigantea living on eastern Grande Terre today While tortoises living on the north-western parts ofthe atoll (Picard and Malabar islands) can grow to sizes greater than 1 m in straight carapace length theones found across most of Grande Terre rarely exceed 50ndash60 cm (based on third scute lengths reported inTurnball et al [71]) The reason for these distinct morphotypes is unknown but suggested causes includedensity-dependent competition and the availability of different vegetation types [71]

We identified several structures on the tortoise bones as crocodylian feeding traces (figure 4)Following the feeding trace identification used in Drumheller amp Brochu [23] circular punctures withdepressed fractures are found on the larger nuchal plate (SNHM 144817) and the fused pubes (SNHM145617) The outline is somewhat irregular and chips of bone have flaked off the internal (ie visceral)surface of the tortoise shell bones Bisected marks in the form of punctures or pits are found on the smallernuchal (SNHM 144917) and on the larger hyo-hypoplastron fragment (SNHM 145317) indicatingthat these traces might have been inflicted by unworn carinated teeth (comparable to similar feedingtraces on mammal bones [72]) Again the bisection pits are accompanied by flakes of internal compactbone Circular pits that do not penetrate the shell bones completely are present on the larger nuchal plate(SNHM 144817) externally and internally the smaller costal internally (SNHM 145117) the smallerhyo-hypoplastron fragment externally (SNHM 145217) and on the small shell fragment (SNHM145417) externally Superficial scores (shallow parallel scratches scores and J-shaped hook scores) arerecognized only on the dorsal surface of the fused pubes (SNHM 145617) In addition two deep obliquefurrows are found on the posterior surface of the fused ischia (SNHM 145717) None of the shell orskeletal bones surrounding the feeding traces shows any signs of healing processes or callus formation

4 Discussion41 Crocodylians as the sole source for feeding tracesSo far there is no evidence for the presence of predatory mammals in the Pleistocene sediments onAldabra whereas crocodylian remains are well represented (eg [6270]) Furthermore the feeding traces

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Table 2 Measurements of fossilised giant tortoise remains (in mm rounded to the first decimal place)

giant tortoise remains

larger nuchal (SNHM 144817)

maximumwidth 1942

maximum length 1279

maximum thickness of anterior border 264

maximumwidth of cervical scute 329

maximum length of vertebral sulcus (left) 1031

posterior median thickness of nuchal 66

diameter of puncture (completely penetrating plate) 97

smaller nuchal (SNHM 144917)

maximumwidth 979 as preserved (complete width estimated ca 107)

maximum length 629 as preserved

maximum thickness of anterior border 119

maximumwidth of cervical scute 147

maximum length of vertebral sulcus (left) 473

posterior median thickness of nuchal 38

diameter of bisected mark (completely penetrating plate) 69times 48

larger costal (SNHM 145017)

maximum length 979 as preserved

maximumwidth 703 proximally

maximum thickness 54

diameter of puncture hole 66

smaller costal (SNHM 145117)

maximum length 645 as preserved

maximumwidth 615 as preserved

maximum thickness 66

smaller hyo- or hypoplastron (SNHM 145217)

maximum length (of flat part) 333

maximumwidth (of flat part) 311

diameter of pit 75

larger hyo- or hypoplastron (SNHM 145317)

maximum length (of flat part) 612

maximumwidth (of flat part) 867

diameter of bisected mark 74times 46

small shell fragmentndashcostal fragment (SNHM 145417)

maximum length 398

maximumwidth 374

maximum thickness 37

maximum diameter of pit 77

distal right ilium fragment (SNHM 145517)

antero-posterior length 491

dorsoventral length 614 as preserved

(Continued)

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Table 2 (Continued)

giant tortoise remains

fused pubes (SNHM 145617)

midline length 772 as preserved

width of right pubis measured frommidline 869

fused ischia (SNHM 145717)

midline length 577

width of right ischiummeasured frommidline 616

maximum length of scores on posterior bone surface 127

maximumwidth of scores on posterior bone surface 88

encountered in the newly collected material do not hint at any mammalian dental features but areall referable to the conical or carinated teeth typical of modern crocodylians [73] (see also crocodylianfeeding traces on larger mammal bones [72])

Crocodylian remains from the Pleistocene of Aldabra specifically the Basin Cabri locality on PicardIsland and the Pointe Hodul locality of Grande Terre Island have been described previously [586274]The latter were subsequently identified as belonging to a new crocodylid species Aldabrachampsusdilophus Brochu 2006 [62] based mostly on a very characteristic broadly convex crest on the squamosalsprotruding posterolaterally as a set of lsquohornsrsquo but the species is furthermore distinguishable lsquofromall extant crocodylians on the basis of a dorsoventrally low premaxilla with highly vaulted palatalsurface and anterodorsally oriented external naris and linear arrangement of premaxillary alveolirsquo [62p 151] Given the overall small size of the fragments of the holotype specimen BMNH R8795 as wellas of the referred specimens which were identified as belonging to a skeletally mature animal (orseveral individuals) the total body length was estimated to be approximately 2ndash25 m [6274] Basedon the fragmentary nature of the finds the phylogenetic position could not be fully resolved but aclose relationship either with other members of the genus Crocodylus or with osteolaemines such asVoay (lsquoCrocodylusrsquo) robustus [75] from Madagascar also a horned species (see [6376] for descriptionsof morphology) was suggested [62] The question remains however whether a crocodylian of 2ndash25 mlength would attack a fully grown giant tortoise with straight carapace lengths approaching or exceeding1 m

The newly recovered crocodylian material on the other hand is interpreted to belong to animals thatwere distinctly larger than previous estimates for A dilophus Comparing the size and dimensions ofthe new materials such as the larger dentary fragment and the skull roof fragment with the holotypematerial and referred specimens of A dilophus the former are not only larger but also more robust Thisbecomes apparent when the new specimens (and the right dentary and the left squamosal of the holotypeof A dilophus BMNH R8795) are scaled and fitted to a similarly robust skull and associated lower jaw ofan extant C niloticus (ZM 100302 lsquono datarsquo specimen identification based on skull morphology dorsalcranial length of 46 cm figure 3) Thus based on the new fossils a reconstructed dorsal cranial skulllength of 40ndash50 cm is feasible Using these numbers in the allometric regressions of Webb amp Messel [77]for Crocodylus porosus the animal had a purported snout vent length of 140ndash175 cm which correspondsto a total body length of approximately 290ndash370 cm The new material could therefore belong either toan individual of A dilophus distinctly larger than previously reported or to a different species Bothassumptions are equally possible based on the currently available fossil material The presence of adifferent crocodylid species at Aldabra immigrated from elsewhere however is not unlikely becausecrocodylids can survive in salt water (among others [78ndash80]) Crocodylus porosus is well known todisperse across salt water [578182] and indeed inhabited the granitic Seychelles until its extirpationin 1819 [58]

42 Scenarios explaining feeding tracesTwo scenarios are equally possible to explain the feeding traces on the giant tortoise bones (figure 5) Inboth cases the tortoise bones were not ingested by the crocodylians as can be deduced by their generallywell-preserved state

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(a) (b)

250 mmd4

po

p

250 mmd3

d4

d5d6

d7

d8

d9

d10

df

500 mmsq

(c) m1

m2

ce m1 (d)

m2m1cem1

200 mm

v1

n

p1

p1

n

Figure 3 Size comparison of crocodylian andgiant tortoise remains (a) Image and interpretative drawing of larger left dentary fragment(SNHM 145817 broken bone surface area indicated by grey patch) scaled and fitted to lower jaw of extant C niloticus (ZM 100302)In addition the outline of right dentary fragment of Aldabrachampsus dilophus (holotype BMNH R8795 see [62]) has been added forcomparison (b) image and interpretative drawing of skull roof fragment (SNHM 146017) consisting of the postorbital (broken bonesurface area indicated by grey patch) and frontal and parietal fragments scaled and fitted to skull of extant C niloticus (ZM 100302) Forcomparison the outline of the right squamosal of Albadrachampsus dilophus (holotype BMNH R8795 see [62]) is shown (c) dorsal andventral sides of the larger nuchal (SNHM 144817)with interpretative drawings of sutures and scute sulci superimposed Note equidistanceof some of the feeding traces (marked bywhite arrowheads connected by thinwhite stippled line)whichmight indicate repeated bites ofthe same crocodylian jawportion (d) larger nuchal (SNHM144817) scaled tofit a largemaleAgiganteawith aheadwidthof 951 mmanda CCL of 1144 cm This specimen has a cervical scute width of about 30 mm comparable to the maximumwidth of the same element inthe fossil ce cervical scutem1ndash2marginal scute 1ndash2 d3ndashd10 dentary alveolus 1ndash10 df dental foramina f frontal n nuchal p parietalp1 first peripheral po postorbital sq squamosal v1 first vertebral scute

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(a)

(b)

(c)

(k)

(e)

( f )( j)

(i)

(h)

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(l) (m)

(d)

100 mm

100 mm

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100 mm 100 mm 100 mm

100 mm 100 mm

Figure 4 Close-up views of crocodylian feeding traces on giant tortoise bones (a) Dorsal surface of larger nuchal (SNHM 144817) onepuncturewithdepressed fractures (white asterisk) andonepit (bc) dorsal andventral bone surfaceof larger nuchal (SNHM144817) largecircular puncture with depressed fractures (white asterisk) note loss of internal cortical bone surrounding the puncture (c) ventral bonesurface of larger costal (SNHM 145017) circular puncture with depressed fractures (white asterisk) (e) ventral bone surface of smallercostal (SNHM 1451) three shallow pits (white asterisks) and set of sub-parallel scores (white arrows) the latter could reflect distanceof adjacent teeth in crocodylian jaw (f ) dorsal bone surface of larger hyo- or hypoplastron fragment (SNHM 145317) bisected mark(orientation indicated by white arrowheads) with depressed fractures (white asterisks) likely produced by unworn carinated tooth (gh)dorsal and ventral bone surface of smaller nuchal (SNHM 144917) bisectedmark (orientation indicated bywhite arrowheads) completelypiercing the bone Note loss of internal cortical bone surrounding the puncture hole (i) dorsal bone surface of smaller nuchal (SNHM144917) bisected mark (orientation indicated by white arrowheads) (j) posterior bone surface of fused ischia (SNHM 145717) deepoblique furrows (white arrows) (k) dorsal bone surface of fusedpubes (SNHM145617) puncturewith loss of internal cortical bone aroundit (in comparison with (c) and (h) impact likely occurred from the opposite side of the bone) and about nine short deeper furrows (whitearrow heads) and few longer shallow scores (white arrows) (l) ventral bone surface of fused pubes (SNHM 145617) same puncture asin (k) with depressed fractures (white asterisk) and deep furrow (white arrow) (m) dorsal bone surface of fused pubes (SNHM 145617)three hook scores (white arrows)

(1) Living giant tortoises were attacked by the crocodylians This likely would have occurred asan ambush attack in a water hole where the tortoise cannot easily spot the attacker Thefeeding marks on the nuchals might support the notion that the crocodylian attacked the tortoisefrontally or from an anterolateral direction when the tortoise came to drink rather than from thelateral side where the tortoise shell is highest The absence of healing on the tortoise shells wouldindicate that the animal did not survive the encounter with the crocodylian

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(b)

(a)

Figure 5 Possible Pleistocene trophic interaction scenarios including crocodylian and giant tortoise based on new fossil evidence (a)Hunting crocodylian attracted by drinking tortoise The attack likely occurred frontally or fronto-laterally where the head neck and softtissueparts of the anterior shell aperture are exposed (b) decomposing tortoise carcass at breakdownstage 2 (putrid stagewithdipteransand ants [43]) attracting scavenging crocodylian and coconut crab The spreading of the latter throughout the Indo-Pacific regionhas beenproposed to have happened during the Pleistocene [83] and today this crab is one of the most active decomposition agents on AldabraAtoll [43] As in the previous scenario the crocodylian is hypothesized to approach the carcass from the front at the point of easiest accessto the viscera

(2) The crocodylians scavenged on tortoise carcasses A recently deceased tortoise close to awaterhole could have attracted crocodylians which show opportunistic scavenging behaviour[5784] Similar to scenario 1 the shell apertures especially the high anterior one facilitate easieraccess to the viscera than the lateral flanks of the shell With the tortoise already dead no healingof the tortoise shell is to be expected either Dead tortoises would also have been scavenged onby the smaller Aldabrachampsus dilophus among other animals such as the coconut crab

Besides the localized feeding traces on the shell and pelvic bones the tortoise bones themselves arewell preserved and appear to have separated by decay and not forcefully by shaking or inertial feeding[294445]

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In the case of the smaller Hungarian Late Cretaceous bothremydid turtle remains from Iharkuacutet

differently arranged tooth row marks were proposed to be the result of inertial feeding as the turtlemight have been moved around by the predator [10 p 314] We speculate that a giant tortoise of hugedimensions (size) as indicated by the recent fossil finds (figure 3cd) would not have been easy to handleby a crocodylian predatorscavenger As such equidistant punctures and pits on the larger nuchal mightindicate repeated biting with rearrangement of the crocodylian jaws on the shell rather than vice versa

According to Hu et al [33] large to very large turtles or tortoises grow to such sizes that predatorsare basically unable to break apart their shells Modern A gigantea and their relatives that lived duringthe Late Pleistocene reach masses beyond 100 kg (reported up to 120ndash140 kg and 130ndash140 cm CCL for thelargest males in the wild [85]) putting them well into the lsquosize refugersquo sensu [33] In those cases where theshell could thus not be cracked open the predatorscavenger likely fed only on the exposed soft tissuesof the neck and head or the limbs (compare also to [44])

43 Ancient and modern ecosystems on AldabraIn the recent past the population of A gigantea on Aldabra recovered from near extinction in thenineteenth century to a high of about 130 000 during the 1970s and was estimated at around 100 000individuals by the end of the twentieth century [8687] There is no current population estimate availablebut a recent analysis of data from a monitoring database showed that the population has been stableover the last 15 years [71] The population details of Aldabrachelys tortoises on the atoll during theLate Pleistocene are currently not known but this ancient ecosystem differed considerably to that oftoday with crocodylians acting as apex predators While the population details of the crocodyliansare similarly unquantifiable these animals nevertheless influenced the ecosystem structure by directlyimpacting the numbers of their giant living prey and also by lowering the persistence time of tortoisecarcasses through scavenging Today the persistence time of those is much higher due to the absenceof larger predators and decomposition is mainly achieved through invertebrate agents and weathering[43] Modern crocodylians also have a good olfactory sense and using chemical cues allows them todetect deceased animals over large distances [5788] In this regard the Pleistocene crocodylians likelyalso scavenged on carcasses that were not in or close to a pool of water Late Pleistocene fossil material isabundant on Aldabra and collections of additional material from the Cinq Cases region and elsewhereon the atoll could allow population-level morphological studies of the tortoises and crocodylians thatwould shed further light on the details of the extinct trophic relationship (eg prey size selection)

5 ConclusionRecent collection efforts in the Late Pleistocene sediments on the coralline Aldabra Atoll yielded severalbones of giant tortoises with bone surface structures identified as feeding traces (scores pits hooksand punctures) of crocodylians From the same site cranial and postcranial crocodylian remains wererecovered that are interpreted herein as the cause of those feeding traces The size of these remains islarger than previously collected crocodylian remains from Aldabra indicating the hitherto unknownpresence of a crocodylian with larger body size on the atoll (either belonging or not to the same taxon)which likely constituted an apex predator of the ancient ecosystem This is the first report of direct trophicinteraction in the fossil record of these vertebrate groups for the atoll

Data accessibility All fossil specimens are stored in openly accessible public repositories (see Institutional abbreviationsection)Authorsrsquo contributions TMS DMH FF-D and NB conceived the study NK MD DMH and TMS studied andanalysed the fossils TMS and DMH wrote the main text TMS produced the figures All authors contributed tothe drafting of the article and revised it criticallyCompeting interests We have no competing interestsFunding The Zurich-Aldabra Research Platform (ZARP) and the URPP Global Change and Biodiversity (both UZH)as well as the Zoo Zurich are thanked for the financial support We gratefully acknowledge DHL Express Seychellesfor funding the shipping of the fossils to Zurich for analysis TMS acknowledges funding by Swiss National ScienceFoundation (grant no 31003A_173173)Acknowledgements The Seychelles Islands Foundation provided outstanding logistical assistance and we especiallythank April Burt Jude Brice and the Head Office staff We thank Rich Baxter for the assistance in the field and GabrielaSchaepman-Strub and Anne Schaepman Linus Schaepman and Michael Schaepman (all Zurich) for helping dredgingfossils We thank the Seychelles Natural History Museum for facilitating the study of the fossils Beat Scheffoldand Markus Hebeisen (both PIMUZ) are thanked for their advice in the preparation of specimens We thank Georg

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14

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Fluumlckiger (UZH) for his initial assessment of the bones during a student project (UZH course Bio262) in 2017 Wealso thank the editorial team and three anonymous reviewers for their critical comments which helped in improvingthe study

References1 Kelley PH Kowalewski M Hansen TA (eds) 2003

Predatorndashprey interactions in the fossil record NewYork NY Kluwer AcademicPlenum Publishers

2 Kahlke R-D Fritz U Kierdorf U 2015 Badger (Melesmeles) predation on European pond turtle (Emysorbicularis) during the Eemian interglacial (MIS 5e)Palaeobiodivers Palaeoenviron 95 223ndash235(doi101007s12549-014-0170-z)

3 Carpenter K 1998 Evidence of predatory behavior bycarnivorous dinosaurs Gaia 15 135ndash144

4 Wilson JA Mohabey DM Peters SE Head JJ BentonMJ 2010 Predation upon hatchling dinosaurs by anew snake from the Late Cretaceous of India PLoSBiol 8 e1000322 (doi101371journalpbio1000322)

5 Buffetaut E Martill D Escuillieacute F 2004 Pterosaurs aspart of a spinosaur diet Nature 430 33(doi101038430033a)

6 Hone D Choiniere J Sullivan C Xu X PittmanM TanQ 2010 New evidence for a trophic relationshipbetween the dinosaurs Velociraptor andProtoceratops Palaeogeogr PalaeoclimatolPalaeocol 291 488ndash492 (doi101016jpalaeo201003028)

7 Tschanz K 1989 Lariosaurus buzzii n sp from theMiddle Triassic of Monte San Giorgio (Switzerland)with comments on the classification of nothosaursPalaeontogr Abt A 208 153ndash179

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9 Boucot AJ Poinar Jr GO 2010 Fossil behaviorcompendium Boca Raton FL CRC Press

10 Botfalvai G Prondvai E Oumlsi A 2014 Inferred bitemarks on a Late Cretaceous (Santonian)bothremydid turtle and a hylaeochampsidcrocodilian from Hungary Cretac Res 50 304ndash317(doi101016jcretres201405006)

11 Drumheller-Horton SK 2012 An actualistic andphylogenetic approach to identifying andinterpreting crocodylian bite marks Theses andDissertations University of Iowa Iowa City IA

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13 Blasco R 2008 Human consumption of tortoises atLevel IV of Bolomor Cave (Valencia Spain)J Archaeol Sci 35 2839ndash2848 (doi101016jjas200805013)

14 Blasco R Blain H-A Rosell J Diacuteez JC Huguet RRodriacuteguez J Arsuaga JL de Castro JMB Carbonell E2011 Earliest evidence for human consumption oftortoises in the European Early Pleistocene fromSima del Elefante Sierra de Atapuerca SpainJ Hum Evol 61 503ndash509 (doi101016jjhevol201106002)

15 Blasco R Rosell J Smith KT Maul LC Santildeudo PBarkai R Gopher A 2016 Tortoises as a dietary

supplement a view from the Middle Pleistocenesite of Qesem Cave Israel Quat Sci Rev 133165ndash182 (doi101016jquascirev201512006)

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17 Amalfitano J Dalla Vecchia FM Giusberti LFornaciari E Luciani V Roghi G 2017 Direct evidenceof trophic interaction between a large lamniformshark Cretodus sp and a marine turtle from theCretaceous of northeastern Italy PalaeogeogrPalaeoclimatol Palaeocol 469 104ndash121(doi101016jpalaeo201612044)

18 Rothschild B 2009 Scientifically rigorous reptile andamphibian osseous pathology lessons for forensicherpetology from comparative andpaleo-pathology Appl Herpetol 6 47ndash79(doi101163157075409X413842)

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20 Rothschild BM Schultze H-P Pellegrini R 2012Herpetological osteopathology New York NYSpringer

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22 Hutchison JH Frye FL 2001 Evidence of pathology inearly Cenozoic turtles PaleoBios 21 12ndash19

23 Drumheller SK Brochu CA 2016 Phylogenetictaphonomy a statistical and phylogenetic approachfor exploring taphonomic patterns in the fossilrecord using crocodylians Palaios 31 463ndash478(doi102110palo2016030)

24 Schwimmer DR 2010 Bite marks of the giantcrocodylian Deinosuchus on Late Cretaceous(Campanian) bones In Crocodyle tracks and traces(eds J Milagraven MG Lockley JA Spielmann) NewMexico Mus Nat Hist Sci Bull 51 pp 183ndash190

25 Mikulaacuteš R Dvořaacutek Z 2010 Possible crocodylian bitetraces Miocene of the Most Basin (Czech Republic)In Crocodyle tracks and traces (eds J Milagraven MGLockley JA Spielmann) NewMexico Mus Nat HistSci Bull 51 pp 191ndash193

26 Mikulaacuteš R Kadlecovaacute E Fejfar O Dvořaacutek Z 2006Three new ichnogenera of biting and gnawingtraces on reptilian and mammalian bones a casestudy from the Miocene of the Czech RepublicIchnos 13 113ndash127 (doi10108010420940600850729)

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28 Binford LR 1981 Bones ancient men and modernmyths New York NY Academic Press

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33 Hu DL Sielert K Gordon M 2011 Turtle shell andmammal skull resistance to fracture due to predatorbites and ground impact J Mech Mater Struct 61197ndash1211 (doi102140jomms201161197)

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37 Smith AL Puffer SR Lovich JE Tennant LA ArundelTR Vamstad MS Brundige KD 2016 A potentialpredatorndashprey interaction of an American badgerand an Agassizrsquos desert tortoise with a review ofbadger predation on turtles Calif Fish Game 102131ndash144

38 Branch WR Els SF 1990 Predation on the angulatetortoise Chersina angulata by the kelp gull Larusdominicanus on Dassen Island Western Cape SAfric J Zool 25 235ndash237 (doi10108002541858199011448218)

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Crocodyle tracks and traces (eds J Milagraven MG LockleyJA Spielmann) NewMexico Mus Nat Hist Sci Bull51 pp 195ndash199

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dynamics of nature (eds J Terborgh JA Estes)pp 163ndash177 Washington WA Island Press

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73 Berkovitz B Shellis P 2017 The teeth of non-mamm-alian vertebrates London UK Academic Press

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77 Webb GJW Messel H 1978 Morphometric analysisof Crocodylus porosus from the north coast ofArnhem Land northern Australia Aust J Zool 261ndash27 (doi101071ZO9780001)

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79 Brochu CA 2001 Congruence between physiologyphylogenetics and the fossil record on crocodylianhistorical biogeography In Crocodilian biology andevolution (eds GC Grigg F Seebacher CE Franklin)pp 9ndash28 Chipping Norton UK Surrey Beatty ampSons

80 Leslie AJ Taplin LE 2001 Recent development inosmoregulation of crocodilians In Crocodilianbiology and evolution (eds GC Grigg F Seebacher CEFranklin) pp 265ndash279 Chipping Norton UK SurreyBeatty amp Sons

81 Read MA Grigg GC Irwin SR Shanahan D FranklinCE 2007 Satellite tracking reveals long distancecoastal travel and homing by translocated estuarinecrocodiles Crocodylus porosus PLoS ONE 2 e949(doi101371journalpone0000949)

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