DISEASES OF AQUATIC ORGANISMSDis Aquat Org

Vol. 119: 9199, 2016doi: 10.3354/dao02988

Published May 3

INTRODUCTION

Shell disease in Crustacea is a complex syndrome,which includes several independent and apparentlyunrelated infections. It is characterized by various lev-els of damage to the crustacean integument from asingular pitting to an extensive loss of the integument(Smolowitz et al. 1992, Shields & Overstreet 2007),sometimes resulting in exposure of the underlyingsoft tissue (e.g. Comeau & Benhalima 2009). Shell dis-ease has been studied extensively in economically im-portant crustacean species such as the American lob-ster Homarus americanus H. Milne-Edwards, 1837(reviewed by Cobb & Castro 2006 and Gomez-Chiarri& Cobb 2012) and the European edible crab Cancerpagurus Linnaeus, 1758 (Vogan et al. 2001, 2002, Vo-gan & Rowley 2002, Costa-Ramos & Rowley 2004), aswell as, to a lesser extent, in the blue crab Callinectes

sapidus Rathbun, 1896 (Noga et al. 1998, 2000). Mi-crobial pathogens involved in shell disease are uni-versally accepted to be chitinolytic bacteria (Shields &Overstreet 2007, Vogan et al. 2008, Gomez-Chiarri &Cobb 2012), although cases of fungally induced shelldisease have been described for freshwater crus-taceans, and true fungi and oomycetes are onoccasion observed in lesions of marine crustaceans(e.g. Noga et al. 2000, Quinn et al. 2009).

At least 3 different forms of shell disease have beendescribed in wild populations of the American lobster(epizootic, endemic, and cigarette-burn shell disease;Cobb & Castro 2006). In addition, 2 forms of shell dis-ease, impoundment (Hess 1937) and diet-induced shelldisease (Tlusty et al. 2008), are known for theAmerican lobster when kept in captivity. Unlike lob-sters, crabs commonly develop shell disease on theirventral surfaces, and lesions appear to be shallow and

Inter-Research 2016 www.int-res.com*Corresponding author: adielklompmaker@gmail.com

Possible shell disease in 100 million-year-old crabs

Adil A. Klompmaker1,2,3,*, Andrei Y. Chistoserdov4, Darryl L. Felder4

1Florida Museum of Natural History, University of Florida, 1659 Museum Road, PO Box 117800, Gainesville,Florida 32611, USA

2Department of Geology, Kent State University, 221 McGilvrey Hall, Kent, Ohio 44242, USA3Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley,

1005 Valley Life Sciences Building #3140, Berkeley, California 94720, USA4Department of Biology, University of Louisiana at Lafayette, PO Box 42451, Lafayette, Louisiana 70504, USA

ABSTRACT: Modern organisms exhibit evidence of many diseases, but recognizing such evidencein fossils remains difficult, thus hampering the study of the evolution of disease. We report on 2molts of the goniodromitid crabs Distefania incerta and Goniodromites laevis from the mid-Creta-ceous (late Albian) of Spain, with both species exhibiting damage to the dorsal carapace inotherwise well-preserved specimens. The subcircular to quadratical holes, found in

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diffuse (Shields & Overstreet 2007). Scraping of thesediment surface appears to be the most likely inocu-lating cause for this type of lesion. However, the mani-festation of shell disease in crabs, when the lesions de-

velop on the extremities or carapace, is sometimes verysimilar in appearance to endemic and/or cigarette-burn disease in lobsters: lesions appear as scoopedmaterial in singular or multiple pits (Figs. 1 & 2).

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Fig. 1. Modern brachyuran crabs from the Gulf of Mexico and Atlantic coast of Florida (USA) exhibiting varied examples of cu-ticular lesions and shell disease (black spots in A,B,D,E,F and white encircled area in C). (A) Paractaea nodosa (Stimpson,1860), female, carapace width (cw) 11.4 mm, dorsal surface, archived in the University of Louisiana at Lafayette ZoologicalCollection (ULLZ 6760). (B) Chaceon quinquedens (Smith, 1879), female, cw 27.9 mm, ventral right surface (ULLZ 14055). (C)Callinectes ornatus Ordway, 1863, female, cw 31.0 mm, dorsal surface (ULLZ 9664). (D) Micropanope sculptipes Stimpson,1871, male, cw 7.8 mm, dorsal surface (ULLZ 3655). (E) Euphrosynoplax clausa Guinot, 1969, female, cw 18.7 mm (ULLZ

14473). (F) Micropanope lobifrons A. Milne-Edwards, 1881, female, cw 6.9 mm (ULLZ 10935)

Klompmaker et al.: Shell disease in fossil crabs

The environmental triggers of shell disease in crus-taceans are not well known, but there may be multi-ple causes. In epizootic shell disease, 2 specificpathogens are suspected (Chistoserdov et al. 2012),and infection appears to be triggered by a higherthan usual temperature (Quinn et al. 2012a, Tlusty &Metzler 2012). Similar pathogens are observed inlesions produced by impoundment and endemicshell disease, but not in cases of diet-induced shelldisease (Chistoserdov et al. 2012, Quinn et al. 2012b).Remarkably, integument lesions of crabs only occa-sionally harbor the 2 lobster pathogens, but Vibrioand Pseudoalteromonas spp. appear to be ubiquitous(Getchell 1989, Vogan et al. 2002, Shields & Over-street 2007). The role of metal contamination hasbeen shown to usually be a minor factor for thedevelopment of shell disease in wild populations ofcrustaceans (Weinstein et al. 1992). The presence ofenvironmental pollutants correlates with shell dis-ease in some cases (Ziskowski et al. 1996, but seePowell & Rowley 2005). It is usually assumed, how-ever, that a physical trauma may cause shell diseasein crustaceans, although there is little field and ex -perimental evidence for this assumption (Comeau &Benhalima 2009, Quinn et al. 2013). Apart from obvi-ous teeth marks and scratches left by potential pred-ators and those resulting from territorial/sexual be -havior, breaking off of ectosymbionts, specificallybarnacles, also cannot be ruled out. The latter partic-ularly applies to singular, almost circular lesionssometimes found on crabs.

Bacteria and decapod crustaceans have co-existedin the biosphere for at least ~160 million years (Robinet al. 2015a,b). Despite extensive fossil collections ofcrustaceans, shell abnormalities with a biotic originhave not often been reported for fossil crabs, partlybecause they are not easily recognized in the fossilrecord and because they do not preserve well. Thebest known examples of shell abnormalities in fossildecapods in terms of stratigraphic coverage, num-bers of specimens, and numbers of species infectedare those evident as swellings caused by isopods inthe metabranchial regions of fossil decapods, re fer -red to as the trace fossil Kanthyloma crusta Klomp-maker et al., 2014. They are known from the Jurassiconwards and are encountered in many different fos-sil decapod taxa (Wienberg Rasmussen et al. 2008,Klompmaker et al. 2014b, Klompmaker & Boxshall2015). Here, we report on 2 mid-Cretaceous crabsfrom northern Spain with damage on the moltedcarapace that we hypothesize to be shell diseasecaused by bacterial lesions. To our knowledge, this isthe first report of such disease in fossil decapods.

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Fig. 2. Modern brachyuran crabs affected by black shell dis-ease and trauma. (A) Example of black spot (= enzootic)shell disease in the Atlantic rock crab Cancer irroratus Say,1817, collected from the Rhode Island Sound, Rhode Island(USA). Note that the lesion penetrates the shell in some areas. Exact specimen size not known. Photograph courtesyof Kathleen Castro (Rhode Island Sea Grant). (B) Blue crabCallinectes sapidus with bacterially induced shell disease(epizootic = black spot) and (C) another specimen of bluecrab with trauma shell disease (note that melanization isminimal). The dactyli and fixed fingers of the blue crabs areheld together by black tape. Both specimens were collectedin the Gulf of Mexico near Grand Isle, Louisiana (USA) and

measure ~90 mm 130 mm carapace width and length

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MATERIALS AND METHODS

The 2 fossil brachyuran crabs were found in theKoskobilo quarry, Spain (42.8823 N, 2.1990 W,WGS84) in the Albeniz Unit of the Eguino Formation,which is interpreted to be late Albian (~100 millionyears ago) in age (Klompmaker 2013). The carbonaterocks, in which numerous colonial and solitary coralsand algae are the main reef builders, yielded a highlydiverse decapod crustacean assemblage (Fraaije etal. 2009, 2012, 2013, Klompmaker et al. 2011a,b,c,2012a,b, 2013a, Klompmaker 2013) consisting of 38species based on ~1100 specimens. The 2 crab speci-mens were found in the southwestern corner of theKoskobilo quarry by breaking the limestones intoapproximately equal pieces. These specimens aredeposited at Oertijdmuseum De Groene Poort, Box-tel, The Netherlands (specimen numbers precededby the designation MAB k). Comparisons were madeto external integuments of modern decapods pho-tographed from the northern Gulf of Mexico and theAtlantic coast of Florida, USA, and archived in the

University of Louisiana at Lafayette Zoological Col-lection (ULLZ). Comparison was also made to a pho-tographed carcinid crab from Rhode Island Sound,RI, USA.

RESULTS

The 2 crab specimens are interpreted to representnearly pristine molts of Distefania incerta (Bell, 1863)and Goniodromites laevis (Van Straelen, 1940)(Fig. 3), both from the Goniodromitidae family. Bothcarapace specimens are internal molds because nocuticle was observed. However, the general outline,groove pattern, tubercles, and lateral projections areremarkably well-preserved in general. Both speci-mens show a part where the cuticle was absent (i.e.the imprint of cuticle is missing and relatively struc-tureless rocks remain). No evidence for regenerationis found around this damage. The damage in D.incerta is subcircular to subquadratical in outlinewithout sharp edges located at the central-left por-

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Fig. 3. (AC) Internal molds of carapaces of the crabs Distefania incerta, archived at the Oertijdmuseum De Groene Poort,Boxtel, The Netherlands (reference no. MAB k2940), and (DG) Goniodromites laevis (MAB k2499) from the Cretaceous (lateAlbian, ~100 Myr) of northern Spain with the damage shown from various angles. (A) Dorsal view, maximum carapace width(cw) excluding spines: 9.1 mm. (B) Dorsal view with damage outlined. (C) Ventral view showing that the specimen is a molt.(D) Dorsal view, maximum cw excluding spines: 6.5 mm. (E) Dorso-right-lateral view. (F) Dorso-right-lateral view with thedamage outlined. (G) Ventral view showing that the specimen is a molt. Specimens were whitened prior to photography

Klompmaker et al.: Shell disease in fossil crabs

tion of the carapace (Fig. 3AC). Its maximum widthis 3.3 mm, the maximum length is 3.2 mm, and thearea is ~8.0 mm2. Although the very rim of the hole(~0.1 mm) was not fully prepared to avoid damage tothe carapace, the damage in G. laevis is subcircular inoutline and contains no sharp edges (Fig. 3DG). It islocated in the right branchial region of the carapace.Measurements include: maximum width = 1.7 mm,maximum length = 1.9 mm; area ~2.5 mm2. Suchdamage was rare among complete and partially bro-ken decapod carapaces from this locality (2 out of~1100 specimens, or

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scribed from fossil decapods (e.g. Tshudy & Feldmann1988, Feldmann 2003, Jakobsen & Feldmann 2004,Waugh et al. 2004, Feldmann et al. 2006, Petit &Charbonnier 2012, Robin et al. 2013, 2015c, 2016,Hyn et al. 2016). Limpets have been argued tocause perfectly circular holes, unlike the damage re -ported here, in the shells of Late Cretaceous am -monites (Kase et al. 1998), although others have sug-gested that these holes represent mosasaur bitemarks (e.g. Kauffman & Kesling 1960). Barnacles usu-ally leave at least some evidence of their basal platebehind on the crab shell upon death (Waugh et al.2004, see their Fig. 2.2.), and thus would not likelycause the damage shown here. Some modern crabsuse ane mones and sponges for camouflage, butthese biotic relationships do not affect skeletal com-ponents (Waugh et al. 2004, p. 961). The nubeculariidforaminifera encrusted on Late Jurassic deca podshave a diameter of only 300 m (Robin et al. 2013).Although we cannot be certain, barnacles andlimpets may also be ruled out because the shape ofthe damage is not symmetrical as may be expectedfor these encrusting organisms. Moreover, there is notrace of encrustation near the damage itself.

Rather, we hypothesize that the damage is prima-rily caused by shell disease, a common phenomenonaffecting modern freshwater and marine crustaceans(Sindermann 1989). Morphologically similar damagecaused by bacterial infection is known from the cuti-cle in modern decapod specimens (Fig. 1), includingon shells of some decapod crustaceans following themassive BP Deepwater Horizon oil spill in the north-ern Gulf of Mexico in 2010 (Felder et al. 2014). Insome cases, the entire cuticle is affected (Smolowitzet al. 1992, Noga et al. 2000), which is consistent withour specimens, because the cuticle is lacking com-pletely in the damaged areas. Molting can be ef -fective in deterring the disease in the early stagesof the bacterial infection for Homarus americanus(Smolowitz et al. 1992). The area of the observed fos-sil damage (2.5 and ~8.0 mm2) is within the lower sizerange of modern shell disease lesions: Noga et al.(2000) reported affected areas from 1 to 200 mm2 forCallinectus sapidus. Moreover, they also reportedthat severe lesions accompanied by the loss of theepi-, exo-, and possibly even the endocuticle, may beas small as 3 mm in diameter, which is comparable tothe diameter of the damage in Distefania incerta.

The shapes of these lesions vary. Noga et al. (2000)mentioned round, oblong, and irregular shapes forsevere lesions in C. sapidus. The shapes usually donot have sharp angles (Fig. 1; see also Figs. 17 inNoga et al. 2000), which matches the damage in the

fossil specimens reported here. The shape and singularity of the lesion is suggestive of bacteriallyinduced enzootic shell disease. However, we cannotbe sure, since the term enzootic implies somethingopposite of epidemic, and there is no way to establishwhether shell disease was or was not widely spreadin this crab population because the internal moldcarapaces are often broken and shell disease doesnot always lead to complete loss of the cuticle. Bacte-rial infection initiated after molting rather than priorto molting seems unlikely in this case because therelatively pristine nature of the carapaces other thanthe holes suggests relatively rapid burial. Thisimplies that bacterial infection is unlikely to haveoccurred between molting and burial, certainly not tothe extent that it could have penetrated the shell.

We conclude that bacterial infection that startedprior to molting is the most likely cause for theobserved holes in the carapaces of D. incerta andGoniodromites laevis, although other agents mayhave initiated the damage. To date, this is the onlyknown example of possible bacterial infections indecapod crustaceans from the fossil record. Thus,bacterial infection and subsequent shell loss indecapods may have been ongoing ~100 million yearsearlier than previously known.

Acknowledgements. Ninon Robin (Musum national dhis-toire naturelle, Paris) and the anonymous reviewers pro-vided very useful comments that substantially improved thiswork. We further thank Rodney Feldmann (Kent State Uni-versity, USA) for bringing the authors in contact with eachother and for items of literature. The specimen of Distefaniaincerta was collected by A.A.K. in 2010 during a field tripsupported by a Molengraaff Fonds, Amoco Alumni Scholar-ship, Graduate Student Senate (Kent State University)research grant, and Sigma Gamma Epsilon (Gamma ZetaChapter) research grant to A.A.K. This work was furthersupported by the Jon L. and Beverly A. Thompson Endow-ment Fund to A.A.K. and a grant from the Gulf of MexicoResearch Initiative (GoMRI) to D.L.F. The specimen ofGoniodromites laevis was collected by Ren Fraaije (Oerti-jdmuseum De Groene Poort, The Netherlands) in 2008. Wealso thank Yvonne Coole, Barry van Bakel (OertijdmuseumDe Groene Poort & Naturalis Biodiversity Center, TheNetherlands), Rodney Feldmann, Carrie Schweitzer (KentState University), and Pedro Artal (Museo Geolgico delSeminario de Barcelona) for their help in the field. RoxannaSmolowitz (Roger Williams University) kindly provided theimage for Fig. 2. This is University of Florida Contribution toPaleobiology 769 and University of Louisiana at LafayetteLaboratory for Crustacean Research Contribution 181.

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Editorial responsibility: Stephen Feist,Weymouth, UK

Submitted: October 16, 2015; Accepted: February 25, 2016Proofs received from author(s): April 18, 2016

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