BA SE Biotechnol. Agron. Soc. Environ. 2011 15(3), 435-447 Focus on: Large carrion beetles (Coleoptera, Silphidae) in Western Europe: a review Jessica Dekeirsschieter (1) , François Verheggen (1) , Georges Lognay (2) , Eric Haubruge (1) (1) Univ. Liege - GemblouxAgro-Bio Tech. Department of Functional and Evolutionary Entomology. Passage des Déportés, 2. B-5030 Gembloux (Belgium). E-mail: [email protected], [email protected](2) Univ. Liege - Gembloux Agro-Bio Tech. Department of Analysis Quality and Risks. Laboratory of Analytical Chemistry. Passage des Déportés, 2. B-5030 Gembloux (Belgium). Received on April 20, 2010; accepted on October 5, 2010. This review focuses on carrion beetles (Coleoptera, Silphidae) of the Western Palearctic and their potential use in forensic entomology as bioindicators. Few studies have looked at Silphidae in forensic context and investigations. However, some Silphidae present the desirable characteristics of some Diptera used in postmortem estimates and thus may extend the minimum postmortem interval (PMImin). We review here the taxonomy and distribution of Western Palearctic Silphidae. The anatomical and morphological characteristics of both subfamilies are described for adults and larvae. The biology and ecology of silphids are also summarized for Silphinae and Nicrophorinae. A specific chapter gives an overview of the current uses of Silphidae in forensic entomology as postmortem indicator. Keywords. Silphidae, burying beetles, forensic entomology, taxonomy, identification, Western Europe. Les grands coléoptères nécrophages (Coleoptera, Silphidae) en Europe occidentale : synthèse bibliographique. Cette synthèse bibliographique fait le point sur les Silphidae du Paléarctique Ouest et leur utilisation potentielle en entomologie forensique comme bioindicateurs postmortem. Peu d’études s’intéressent aux Silphidae dans un contexte forensique. Cependant, certaines espèces de Silphidae présentent les mêmes caractéristiques que certains Diptères que l’on utilise pour calculer un intervalle postmortem (IPM) et pourraient donc servir à calculer un IPM minimum plus étendu. La classification taxonomique et la distribution géographique des Silphidae sont décrites dans cette synthèse ainsi que leurs caractéristiques morphologiques et anatomiques, et ce pour les deux sous-familles de Silphidae. La biologie et l’écologie des Silphidae ont été synthétisées afin de mieux comprendre leur éventuelle valeur en tant qu’indicateur postmortem. Un chapitre spécifique met en évidence les différentes utilisations des Silphidae en entomologie forensique à l’heure actuelle. Mots-clés. Silphidae, coléoptère nécrophage, entomologie forensique, taxonomie, identification, Europe occidentale. 1. IntroduCtIon Carrion beetles (Coleoptera, Silphidae) consist of a small group of Coleoptera counting less than 200 species that are worldwide spread (Sikes, 2008). Silphids perform vital ecosystem functions (Wolf et al., 2004); they promote the breakdown and recycling of organic matter into terrestrial ecosystems (Peck, 1990; Ratcliffe, 1996; Hastir et al., 2001; Kalinova et al., 2009). Most Silphids are carrion feeders (necrophagous species) but can also prey on other carrion inhabitants such as fly eggs or maggots and other small carrion beetles (necrophilous species) (Racliffe, 1996; Hastir et al., 2001; Sikes, 2005; Sikes, 2008). The “carrion” terminology is not adapted for all silphid species according to their ecological group, some species (Silphinae) are phytophagous or found in dung or fungi (Anderson et al., 1984; Sikes, 2008). Carrion beetles are also referenced as “large carrion beetles” contrary to other smaller carrion beetles such as Agyrtidae, Leiodidae (“small carrion beetles”) or Cholevidae (Peck, 1990; Ratcliffe, 1996; Peck, 2001; Sikes, 2008). Their feeding activities on carrion may also destroy some foci of infection of pathogenic bacteria (Peck, 1990). The necrophagous insects, including carrion beetles, have particular relationships with decomposing remains (vertebrate carcass) which constitute a rich ephemeral resource (Anderson et al., 1996; Grassberger et al., 2004; Carter et al., 2007). These specialized insects, including mainly Diptera and Coleoptera, are attracted to the cadaver that they colonize in a relative predictable sequence called the entomofaunal succession or insect succession
Transcript
BASE Biotechnol. Agron. Soc. Environ.201115(3),435-447 Focus on:
Les grands coléoptères nécrophages (Coleoptera, Silphidae) en Europe occidentale : synthèse bibliographique.Cettesynthèsebibliographiquefait lepointsurlesSilphidaeduPaléarctiqueOuestet leurutilisationpotentielleenentomologieforensique comme bioindicateurs postmortem. Peu d’études s’intéressent aux Silphidae dans un contexte forensique.Cependant,certainesespècesdeSilphidaeprésententlesmêmescaractéristiquesquecertainsDiptèresquel’onutilisepourcalculerunintervallepostmortem(IPM)etpourraientdoncserviràcalculerunIPMminimumplusétendu.LaclassificationtaxonomiqueetladistributiongéographiquedesSilphidaesontdécritesdanscettesynthèseainsiqueleurscaractéristiquesmorphologiquesetanatomiques,etcepourlesdeuxsous-famillesdeSilphidae.Labiologieetl’écologiedesSilphidaeontétésynthétiséesafindemieuxcomprendreleuréventuellevaleurentantqu’indicateurpostmortem.UnchapitrespécifiquemetenévidencelesdifférentesutilisationsdesSilphidaeenentomologieforensiqueàl’heureactuelle.Mots-clés.Silphidae,coléoptèrenécrophage,entomologieforensique,taxonomie,identification,Europeoccidentale.
1. IntroduCtIon
Carrion beetles (Coleoptera, Silphidae) consistof a small group of Coleoptera counting less than200species that areworldwide spread (Sikes, 2008).Silphids perform vital ecosystem functions (Wolf etal.,2004);theypromotethebreakdownandrecyclingof organic matter into terrestrial ecosystems (Peck,1990; Ratcliffe, 1996; Hastir et al., 2001; Kalinovaet al., 2009). Most Silphids are carrion feeders(necrophagous species) but can also prey on othercarrion inhabitants such as fly eggs or maggots andother small carrion beetles (necrophilous species)(Racliffe,1996;Hastiretal.,2001;Sikes,2005;Sikes,2008). The “carrion” terminology is not adapted forallsilphidspeciesaccordingtotheirecologicalgroup,some species (Silphinae) are phytophagous or found
indungorfungi(Andersonetal.,1984;Sikes,2008).Carrion beetles are also referenced as “large carrionbeetles”contrarytoothersmallercarrionbeetlessuchasAgyrtidae, Leiodidae (“small carrion beetles”) orCholevidae(Peck,1990;Ratcliffe,1996;Peck,2001;Sikes,2008).
Their feeding activities on carrion may alsodestroysomefociof infectionofpathogenicbacteria(Peck, 1990). The necrophagous insects, includingcarrion beetles, have particular relationships withdecomposing remains (vertebrate carcass) whichconstitutearichephemeralresource(Andersonetal.,1996; Grassberger et al., 2004; Carter et al., 2007).These specialized insects, including mainly DipteraandColeoptera,areattractedto thecadaver that theycolonize in a relative predictable sequence calledthe entomofaunal succession or insect succession
(Megnin,1894;Putman,1983;Schoenlyetal.,1987;Marchenko,1988;Marchenko,2001).Theirstudyinamedico-legalcontextisapartoftheforensicentomology(Amendt etal., 2004; Amendt et al., 2007). Manypublished reports or reviews are focused on DipterapatterncolonizationandneglectColeopterasuccession(Kocarek, 2003; Matuszewski et al., 2008; Midgleyetal.,2009).Carrionbeetleshavebeenreferenced toasbeingapartof theentomofaunalcolonizationofadeadbodybut very few studies have looked at themin a forensic context.However, the use of beetles inforensic entomology can be relevant (Kulshresthaetal.,2001;Watsonetal.,2005;Midgleyetal.,2009;Midgley et al., 2010). Carrion beetles can provideinformation on postmortem colonization on remainsandtimesincedeath(Smith,1986;Haskelletal.,1997;Watsonetal.,2005).ThisreviewfocusesonPalearcticcarrionbeetles(Coleoptera,Silphidae)thatarecarrionfeederorassociatedwithdecomposingremains.
2. taxonoMy and dIStrIbutIon
ThefamilyofSilphidaebelongstothesuperfamilyoftheStaphylinoideaandisdividedintotwosubfamilies:the Nicrophorinae, called burying beetles or sextonbeetles, and the Silphinae (Lawrence et al., 1982;Peck et al., 1993; Ratcliffe, 1996; Dobler et al.,2000; Sikes, 2005). Some taxonomists often includeathirdsubfamilyinthesilphidbeetles:theAgyrtinae(Madge, 1980; Hastir etal., 2001; Debreuil, 2003a;Debreuil, 2004a). However, recent phylogeneticanalyses(Hansen,1997;Newton,1998;Dobleretal.,2000;Caterinoetal.,2005)separatetheAgyrtinaeofotherSilphidaeandconsider theAgyrtidaeasavalidfamily into itself (Lawrenceetal., 1982;Peck,1990;Ratcliffe, 1996; Newton, 1997; Dobler et al., 2000;Caterino etal., 2005). The world fauna of Silphidaeis currently composed of 183species distributed in15genera (Ratcliffe, 1996; Peck, 2001; Sikes, 2005;Sikes,2008).Thisfamilyhasaworldwidedistribution,but is predominant in Holarctic regions (temperateregions)(Pecketal.,1985;Peck,2001;Sikes,2005).The Palearctic region is considered as the center oftheirdistribution(Pecketal.,1985;Dobleretal.,2000).Thereare themostgeneraand thehighestnumberofspeciesofSilphidaeinthePalearctic(Pecketal.,1985;Dobleretal.,2000).Carrionbeetlesarerareorabsentin tropical regionsbecause theyareout-competedbyants,fliesandvertebrates(Ratcliffe,1996).Although,therearesomeAustralianandLatinAmericanendemicspecies (Diamesus,Ptomophila,Nicrophorus mexico)(Ratcliffe, 1996;Scott, 1998).Nicrophorinae are lesswidely distributed than Silphinae, being found inthe temperate northern climate (Sikes, 2005; Sikes,2008).Silphines seem tobemore tolerant towarmer
climate than the nicrophorines (Sikes, 2008). ThesubfamilyofSilphinaehasagreatestgenericdiversity(12genera) than theNicrophorinae (3genera) (Sikes,2005).InnorthWesternEurope,thereare28speciesofSilphidae:11speciesofNicrophorinaeand17speciesofSilphinae.table 1liststhespeciesinWesternEurope(Heinz, 1971;Hastir et al., 2001; Sikes et al., 2002;Debreuil, 2003a; Debreuil, 2003b; Debreuil, 2004a;Debreuil, 2004b; Debreuil, 2004c; Ružicka et al.,2004;Sikes,2005).Amongthem,thereare22species(11Nicrophorusspp.and11Silphinae)thatarecarrionobligateorpredaciousspecies.ThereisonlyonegenusofnicrophorineintheWesternPalearctic:Nicrophorus.In the past, the spelling of this genus name variedfromNicrophorus toNecrophorus and back again toNicrophorus, the valid genus name (Ratcliffe, 1996;Debreuil, 2004b), but it is not rare to see thewrongspellinginsomepublications.
3. anatoMIC and MorphoLogICaL dESCrIptIonS
Silphidbeetlesareusuallymediumtolargeinsize(7to45mm)(Peck,1990;Ratcliffe,1996;Hastiretal.,2001;Debreuil,2003a;Sikes,2008).Although,adultsandlarvaevarygreatlyinsizeandshape(Byrdetal.,2009).Adultshaveanovate(Silphinae)tomoderatelyelongate shape with protuberant eyes (Sikes, 2005)(Figure 1).Theyareflattened (Silphinae)or stronglyconvex (Ratcliffe,1996).Silphidsareoftendarkenedorhavedistinctivered-orange-yellowmarkingsontheelytra (Nicrophorus spp.) that may serve as warningcoloration (Ratcliffe, 1996; Hastir et al., 2001). Theelytra are often short and leave several abdominalsegmentsexposed(1or5abdominalsegmentsamongthesubfamily).TheelytraarepunctuateandtruncateinNecrodes (Silphinae)andNicrophorinae,not truncatein the remaining Silphinae (Sikes, 2005) (Figure 2).Thescutellumisoftenverylargeandthepronotumisenlarged(Peck,1990;Sikes,2005;Sikes,2008).
The antennae are constituted by eleven segmentsand capitate (abruptly clubbed) for Nicrophorinae orclavate(graduallyclubbed)forSilphinae(Hastiretal.,2001) (Figure 3). The antennae are widely spreadand inserted on the lateral side of head. They haveoftenmicrosetaecoveringonlyapical three segments(segments9to11)(Hastiretal.,2001).Theabdomenwith sternite2 is not visible between hind coxae butvisiblelaterallyofmetacoxae(Sikes,2008).Thetarsiorterminalportionofeachleghasfivesegments(tarsi5-5-5)(Peck,1990;Hastiretal.,2001).Silphidlarvaeare recognizable by the possession of a combinationof mandible without a molar lobe; maxilla withbroad,apicallycleftmalabearingsetaeonouterlobe;and usually a two-segmented articulated urogomphi
ReviewofEuropeanSilphidae 437
table 1.Listof theWesternEuropean speciesof “carrion”beetles (includingMediterranean species), family SilphidaeLATREILLE,1807—Liste des espèces de Silphidae de l’Europe de l’ouest (incluant les espèces méditerranéennes), famille Silphidae LATREILLE, 1807.
Genus NicrophorusFABRICIUS,1775 AblattariaREITTER,18851884AclypeaREITTER,1884OiceoptomaLEACH,1815PhosphugaLEACH,1817SilphaLINNAEUS,1758ThanatophilusLEACH,1815NecrodesLEACH,1815DendroxenaMOTSCHULSKY,1858
*:indicatesnecrophagousorpredaceousspecies— indique des espèces nécrophages ou prédatrices(Heinz,1971;Hastiretal.,2001;Sikesetal.,2002;Debreuil,2003a;Debreuil,2003b;Debreuil,2004a;Debreuil,2004b;Debreuil,2004c;Ružickaetal.,2004;Sikes,2005)
a b c
Figure 1. Habitus of Silphinae (a), (b) andNicrophorinae(c);(a)Thanatophilus sinuatus♀, (b) Necrodes littoralis, (c) Nicrophorus interruptus—Habitus des Silphinae (a), (b) et d’un Nicrophorinae (c) ; (a) Thanatophilussinuatus ♀, (b) Necrodes littoralis, (c) Nicrophorusinterruptus.Source:Sustek,1981.
adults.Silphinespecieshaveoftenadarkenedcolorandaredorsoventrallyflattened(Figure 5).Theirsizeis ranging from 8 to 25mm (Debreuil, 2003a).Theelytra have apices rounded or acute, not truncate orshortened(Peck,1990;Ratcliffe,1996).Theelytraareusuallycostateorcarinate(0-3perelytronwith0forthe genusAblattaria) (Peck, 1990; Debreuil, 2003a)butneverstriate(Figure 2a,2b,2c).Thefrontoclypealsutureisabsent(Figure 6b)andthegularsuturesare
a
b c
d
a b c d
Figure 2. Left elytron of (a) Silphinae with threelongitudinal costae and (d) Nicrophorinae with fasciae ormaculae.Detailoftheelytronof(b)Thanatophilus rugosus and (c) Thanatophilus sinuatus — élytre gauche d’un Silphinae (a) avec trois côtes longitudinales et (d) élytre d’un Nicrophorinae avec des taches ou bandes orangées aussi appelée fasciae ou maculae. Détail d’un élytre de (b) Thanatophilus rugosus et (c) Thanatophilus sinuatus. Source:Sustek,1981.
Figure 3. Antennae of (a) Nicrophorus humator, (b)Aclypea undata, (c) Aclypea opaca and (d) Necrodes littoralis — Antennes de (a) Nicrophorus humator, (b) Aclypea undata, (c) Aclypeaopaca et (d) Necrodeslittoralis.Source:a,b,c:Sustek,1981;d:Portevin,1926.
a b
Figure 4. Larval habitus of (a) Silphinae and (b)Nicrophorinae—Habitus d’une larve (a) de Silphinae et (b) d’un Nicrophorinae.Source:Ratcliffe,1996.
a b
Figure 5. (a) Thanatophilus sinuatus ♀, (b) apex ofThanatophilus sinuatus ♂—(a)Thanatophilussinuatus♀,(b) détail de l’apex de l’élytre♂ Thanatophilus sinuatus.Source:Portevin,1926.
a b
Figure 6. (a) Head of Nicrophorus species with clypealmembrane and (b) head of silphine species withoutfrontoclypeal suture. Pictures from Sustek (Sustek,1981) — (a) Tête d’un Nicrophorus sp. avec la suture frontoclypéale et (b) tête d’une espèce de Silphinae sans suture frontoclypéale. Source:Sustek,1981.
Larvae.Silphinelarvaearecampodeiformwithbodysurfacesheavilypigmentedand sclerotized (Newton,1991;Sikes,2005;Sikes,2008)(Figure 4a).Thebodylengthofmaturelarvaeisrangingfrom12to40mm(Newton, 1991).On each side of the head, there are6pigmented stemmata (ocelli). The anal lobes bearnumerous fine teeth (Sikes, 2005). The tergites arelarge, laterallyproduced; each tergite is usuallywithposterior angles attenuated (Anderson et al., 1985;Ratcliffe,1996).
3.2. nicrophorinae
adults. Nicrophorina species are darkened withred-orangemarkings (bands or spots), called fasciaeor maculae, on elytra extending to the epipleura(Figure 1c), except for the species Nicrophorushumator and Nicrophorus germanicus which arecompletelydarkened(blackorbrown)(Ratcliffe,1996;Hastir et al., 2001; Sikes, 2008). Elytra have apicestruncate (always smooth) and shortened exposing3 or 4abdominal segments (Peck, 1990; Ratcliffe,1996) (Figures 1c and2d).The frontoclypeal sutureis present as a fine line (Peck, 1990; Sikes, 2005)(Figure 6a);thegularsuturesareconfluentposteriorlyand reduce gula to a small triangular piece (Peck,1990;Sikes,2005).Onthefifthdorsalsegment,thereis a pair of stridulatory files in both sexes which isused for communication (Lane et al., 1965; Peck,1990; Ratcliffe, 1996; Sikes, 2008). The antennaeareclubbed,thesecondantennalsegment(pedicel)isoftenreducedandfewerdifferentiatedthanthescape(appearing 10-segmented) (Peck, 1990) (Figure 3a).The compact club is constituted by the last fourantennalsegments(Peck,1990;Ratcliffe,1996;Hastiret al.,2001). InmostNicrophorus species, there isasexual dimorphism in tarsomeres. The nicrophorinemales possess expanded segments of the protarsus(foretarsus)(Peck,1990;Ratcliffe,1996).
Larvae. Nicrophorinae larvae are campodeiform oreruciform and body surfaces are lightly pigmentedandunsclerotizedwith theexceptionof theheadandlegs (Newton, 1991; Ružicka, 1992; Sikes, 2005)(Figure 6b). The body length of mature larvae israngingfrom12to40mm(Newton,1991).Theventralsurfaceissoftandcreamywhite(Andersonetal.,1985;Ružicka, 1992;Ratcliffe, 1996).Oneach sideof thehead,thereisonlyoneunpigmentedstemma(Ratcliffe,1996;Sikes,2005).Contrary toSilphinae larvae, the
anal lobes are without teeth (Newton, 1991; Sikes,2005).Thetergitesaresmall;thoseonabdomenhave4smallspines(Andersonetal.,1985;Ratcliffe,1996).Formoredetailed informationabout themorphologyof larvae of Nicrophorus, Ružicka (1992) describesthe immature stages of the following Europeanspecies: N. vespillo, N. vespilloides, N. humator,N. investigator,N.(fossor)interruptus.
4. ECoLogy and bIoLogy
Carrion beetles (Coleoptera, Silphidae) performvitalecosystemfunctions(Wolfetal.,2004);theypromotethe breakdown and recycling of organic matter intoterrestrial ecosystems (Ratcliffe, 1996; Hastir et al.,2001;Kalinova et al., 2009).tables 2 and3 list thedifferent ecological characteristics of Nicrophorinaeand Silphinae Western European species based onthe relevant literature (Portevin, 1926; Heinz, 1971;Anderson et al., 1984; Ružicka, 1994; Scott, 1998;Kocarek,2001;Hastiretal.,2001;Gueorguievetal.,2002;Kocarek,2002;Ružicka,2002;Sikesetal.,2002;Kocarek, 2003; Debreuil, 2003a; Debreuil, 2003b;Debreuil, 2004a; Debreuil, 2004b; Debreuil, 2004c;Ružicka et al., 2004; Aleksandrowicz et al., 2005;Chauvet et al., 2008). Silphidae are mainly carrionfeeder(necrophagousspecies)orpreyonothercarrioninhabitants such as fly eggs or maggots and othercarrionbeetles(necrophilousspecies)(Racliffe,1996;Hastiretal.,2001;Sikes,2005;Sikes,2008).TherearesomespeciesofSilphinaethatfeedonsoilinvertebrates(snails, caterpillars or slugs predators: Silpha spp.,Dendroxena spp.) or are phytophagous species (e.g.Aclypea spp.) (Sikes,2005; Ikedaet al., 2007; Ikedaet al., 2008). Some Silphidae may be attracted bydecayingfungi(e.g. Phallusimpudicus),dungorrottenplant(Ratcliffe,1996;Hastiretal.,2001;Sikes,2005).Silphidae have reduced interspecific competition inpartitioningspecies(nichedifferentiation)(Anderson,1982; Peck, 1990; Ohkawara et al., 1998; Hockinget al., 2007): they have different temporal activities;some species aremore active during springwhereasother species are active in summer, few species areactive during autumn (Ružicka, 1994; Scott, 1998;Kocarek, 2001). In carrion beetles communities,niche differentiation can occur along dimensionsof season, habitat (biotope) and carcass size (Scott,1998;Hockingetal.,2007).Thedailyactivityisalsodifferent,Silphidaeareprimarilynocturnal insectbutsome species are diurnal (e.g. Thanatophilus spp.)or crepuscular (Ohkawara et al., 1998; Scott, 1998;Kocarek,2001).Habitatpreferencesarealsodifferent;some species are subservient to forest biotope (e.g. O. thoracica, N. vespilloides), whereas other speciesprefer open habitats (field/meadow species) (Scott,
1998;Kocarek, 2001). The type of carrion (age andcarcass size) that theyuse is an important parameter(Anderson,1982;Peck,1990;Scott,1998).Silphinaetend to use preferentially large vertebrate carcasseswhereas Nicrophorinae prefer small carcasses(Anderson, 1982; Peck, 1990; Eggert et al., 1992).Bothsubfamilieshavedifferentreproductivestrategy.Nicrophorinaehaveasurprisingbehaviorforinsects:thebiparentalcareoftheiroffspring(Pukowski,1933;Anderson, 1982; Scott, 1998; Smiseth et al., 2006).ThisisthehighestlevelofsociabilityattainedintheColeoptera (Milne et al., 1976; Ratcliffe, 1996).Atcontrary, Silphinae showno parental care (Ratcliffe,1996). Silphidae have particular relationships withnematodes and mites (phoresy) (Springett, 1968;Richter, 1993; Ratcliffe, 1996; Sikes, 2008). Theserelationships, poorly known, could be mutualism,commensalismorparasitism(Sikes,2008).
4.1. Silphinae
Contrary to theNicrophorinae, little is known aboutthe biology and ecology of the Silphinae (Ratcliffe,1996; Hoback et al., 2004; Ikeda et al., 2007).Concerning necrophagous silphine species, femalesare semelparous and lay their eggs in or on the soilaroundlargevertebratecarcassesandprovidenocareof their offspring (Sikes, 2005; Ikeda et al., 2008).Silphine appear usually on large carcasses (>300g)(Peck, 1990; Sikes, 2005) because these providesufficientfoodresourceforthegreatnumberofbeetlesthatmaybepresent (Anderson, 1982;Watson et al.,2005).Eggshatchin4-5daysandsilphinelarvaefeedoncarrionremains(Anderson,1982).Theymayalsocompetewithnicrophorinespeciesforsmallvertebratecarcassesthattheyuseforfeedbutnotforreproductionandlarvaldevelopment(Bishop,2001;Hobacketal.,2004).Silphinaecolonizeacarcassduringtheearlyormid-stageofdecayandthuscompetewithflies(Diptera)forthefoodresource(Payne,1965;Anderson,1982).Contrary toNicrophorinae, there are some flightlesssilphine species or some flight-dimorphic species(Ikedaetal.,2007;Ikedaetal.,2008).
4.2. nicrophorinae
Many studies on burying beetles behavior havebeen published since the pioneerwork of Pukowski(Pukowski, 1933; Milne et al., 1976; Sikes, 2005).More than 150behavioral ecology studies on theNicrophorusspp.wereconductedinthepast25years(Sikes, 2008). The reviews of Milne et al. (1976),Ratcliffe (1996),Scott (1998)orSikes (2005; 2008)provide detailed information about the nicrophorine(orSilphidae)ecology.Buryingbeetlesspecializedoncarrion (necrophagous and necrophilous species) are
subsocial(Pukowski,1933;Milneetal.,1976;Trumboet al., 1993; Ohkawara et al., 1998; Scott, 1998).Nicrophorus species use small vertebrate carcasses(<300g,usually<100g)suchasrodentsorbirdsthattheyburyandprepareforrearingoffspring(Pukowski,1933;Milneetal.,1976;Trumbo,1990b;Scott,1998;Smithetal.,2001;Sikes,2005;Sikes,2008).Whenthecarcassisfoundbyasinglepairofmaleandfemale,they search a suitable spot for burial that is usuallycompletedin5to8hoursduringthenight(Ratcliffe,1996; Scott, 1998). Carcasses are often located byseveral individuals of both sexes (Pukowski, 1933;Mülleretal.,1998;Steigeretal.,2009).Inthiscase,fightingoccursbetweenindividualsfortheownershipofthecarcassbyasinglemale-femalepair(Pukowski,1933; Müller et al., 1998; Steiger et al., 2009).Searching behavior is guided by olfaction; buryingbeetleshave sensitivechemosensors locatedon theirantennae adapted to detect the smell of a recentlydead animal (Shubeck, 1975; Bartlett, 1987; Peck,1990;Ratcliffe, 1996;Kalinova et al., 2009; Steigeretal.,2009).Ifamalediscoversasuitablecarcassforreproduction,itemitsasexualpheromonetoattractthefemale(Eggertetal.,1989;Eggert,1992;Ohkawaraetal.,1998).Aftertheburial[10-20cmdepth(Hastiret al.,2001)],Nicrophorine removes the skin (furorfeathers)andtheremainsarefashionedintoacompactball. Then, they inoculate the carrion ball with oralandanalsecretionsthathaveantimicrobialpropertiesto delay the decomposition process (Ratcliffe, 1996;Eggertetal.,1997;Scott,1998;Hobacketal.,2004;Rozen et al., 2008; Cotter et al., 2010) and removealsofungi(Scott,1998).Thefemalemakesachamberabove the carrion ball in which it lays 10-50eggs.Bothparentsregurgitatefoodinthiscryptforfeedingtheir larvae. Larvae may also feed directly on thesurfaceofthecarrionball(Ratcliffe,1996;Ohkawaraetal.,1998;Sikes,2008).Thelarvaereceiveparentalcareduringtheirentiredevelopment(Ratcliffe,1996;Scott, 1998). Parents provide extensive care: theyfeedtheiroffspring,theyprotectthemfrompredatorsandintrudingburyingbeetles(inter-andintraspecificcompetitions)andtheymaintainapathogenfreenestwith preservative secretions (Ratcliffe, 1996; Scott,1998; Smiseth et al., 2006). Female stays on thecryptuntilcompletelarvaldevelopment(1-4weeks),whereasthemaleabandonsthebroodafewdaysearlier(Trumbo, 1991;Müller et al., 1998). If the brood istoo large for a successful development, adults mayregulate brood size by selective cannibalism. Theykillsmallerlarvaeduringthefirst24hafterhatching(Trumbo, 1990a; Ratcliffe, 1996). After one week,the larvaehaveconsumed theentirecarrionballandpupateinthenearbysoilduringtwoweeks(Ratcliffe,1996; Ohkawara et al., 1998). Then, adults emergeand theoverwinteringoccurs in theadultstageor in
5. thE utILIty oF CarrIon bEEtLES In ForEnSIC EntoMoLogy
Mostforensicresearcheshavefocusedonflieswhilebeetles have been neglected (Midgley et al., 2009;Midgley et al., 2010).When a corpse colonized byinsects is found, two situations could be considered(Amendtetal.,2007;Lefebvreetal.,2009).Inthefirstsituation,whichisthemostfrequentcaseinforensicinvestigations, insects are pioneer species and theminimum postmortem interval (PMI) is estimatedwith the age of the oldest specimens found on thedeath scene, principally blowflies (Amendt et al.,2007;Lefebvreetal.,2009).In thesecondsituation,laternecrophagousspeciescolonizethecorpsewithadelay,oftenafterthedepartureofpioneerspecies.Theestimation of the PMI is only possible by analyzingthe chronological succession (Amendt et al., 2007;Lefebvre et al., 2009).A frequent objection againsttheuseofColeopterainforensicinvestigationsisthefact that flies (pioneer species) locate corpses fasterthan beetles (later necrophagous species). Thus, theminimum postmortem interval estimates are moreaccurate with Diptera, especially with the familiesof Calliphoridae and Sarcophagidae (Smith, 1986;Midgley et al., 2010). However, recent researcheshave shown that someSilphidae (e.g.Thanatophilus micansFABRICIUS)canlocateacorpsewithin24handtheirlarvaehavebeenobservedsoonafterdeath,during the early stage of decomposition (Midgleyetal., 2009;Midgley et al., 2010).This implies thatsomecarrionbeetleshavethesameforensicinterestingcharacteristicsthancarrionfliesandcanbeconsideredas pioneer species. In this case, some species ofColeopteracanbeusedasreliableforensicindicatorssuchasblowflies(Midgleyetal.,2009;Midgleyetal.,2010). However, there are no available informationabout early postmortem colonization by EuropeancarrionbeetlessuchasinSouthAfricawithT. micans.Some recent publications (Matuszewski et al., 2008;Matuszewskietal.,2010)associatethesilphidactivityoncarcassesduringtheactivedecaystage,primarilyfor Silphinae (N. littoralis,Thanatophilus spp.).Themost important application of insects in forensicinvestigationsistheestimationoftheminimumPMI(Greenberg,1991;Amendtetal.,2004;Amendtetal.,2007).TheseminimumPMI estimates are primarily
basedon the durationof immature stages ofDiptera(developmentmodels)(Amendtetal.,2007).Contrarytoflies,therearefewstudiesontheratesofdevelopmentof Coleoptera with forensic interest (Midgley et al.,2009; Midgley et al., 2010). For example, Midgleyetal. (2009)studied thedevelopmentofT. micansatten constant temperatures.They established a robuststatistical model of development for this commonAfrican species. Currently, there is no developmentmodel (“size-at-age data”) for forensically relevantEuropeansilphids.However,researchondevelopmentofColeopterawithaforensicinterestcanbeausefultool for medico-legal entomologists (Midgley et al.,2010). In addition, carrion beetles have generally alongerlifecyclethanforensicDiptera(Midgleyetal.,2009;Midgleyetal.,2010).Theycancolonizeacorpseduring later decay stages when manymaggots havealreadyleftthecorpses(Kocarek,2003;Matuszewskietal.,2008;Midgleyetal.,2010).ThePMIestimatescan be established by analyzing the arthropodcommunity present on a corpse including manyColeoptera during the later stage of decomposition(Smith, 1986). However, the biology and ecologyof most forensically relevant species of Coleopteraare unknown (Midgley et al., 2010).To increase theaccuracyandthevalidityofthePMIestimatesbasedon ecological successions, there is a necessity togeneratedataoninsectsuccessionandinsectseasonalactivityoncarrioninspecificgeographicregionsandvarious biotopes within these regions (Catts et al.,1992;Amendtetal.,2004;Sharanowskietal.,2008;Lefebvreetal.,2009).Allcarrionbeetlesdonothavethesameforensicinterest;speciesofSilphinaeseemtohaveamoreimportantvalueasforensicbioindicators(Watsonetal.,2005;Matuszewskietal.,2010).Indeedtheyhaveecologicalpreferences forsmallvertebratecarcasses,whileNicrophorinaepresentlessinterestinforensicentomology(Watsonetal.,2005).However,Nicrophorus spp. could be frequently found onhuman corpses, including in houses (Chauvet et al.,2008). This is an inventory extracted from 700realforensiccasesthatoccurredduring15yearsinFrance.Midgleyetal.(2010)suggesttofocusonthebiologyof bothSilphinae (Silpha andThanatophilus).WhileMatuszewski et al. (2010) highlight the forensicusefulnessofthefollowingsilphinespecies:Necrodes littoralis(larvaeandadults),Thanatophilusspp.(larvaeandadults)andO. thoracica (larvae). Insomecases,necrophagousbeetlescanalsoprovideinformationonthepresenceofdrugsorpoisonsbybioaccumulation(entomotoxicology)(Boureletal.,2001;Intronaetal.,2001;Carvalho,2010).Adults,larvaeorbeetleremainsuch as exuviae, puparial cases or fecal material ofColeopteransmay be used for toxicological analysiswhenconventionaltoxicologicalsamples(blood,urine,internalorgans)arenotavailable(Milleretal.,1994;
Bourel et al., 2001; Introna et al., 2001; Carvalho,2010).
6. ConCLuSIon
The potential uses of European carrion beetles asbioindicators in forensic entomology are obvious.Silphidsandprincipallyburyingbeetles(Nicrophorusspp.)arewidelystudiedinvariouscontextsincludingbiology and ecology (Ratcliffe, 1996; Scott, 1998).Indeed,carrionbeetlesarepoorlystudiedinaforensiccontext(Midgleyetal.,2010).Nevertheless,theirusein forensic investigations can be relevant (Watsonet al., 2005; Midgley et al., 2009; Midgley et al.,2010).Are theresomeEuropeancarrionbeetleswithforensicallyinterestingcharacteristics?BeforecreatingdevelopmentmodelforPalearticSilphidaeofforensicvalue,forensicentomologistsneedtoincreasedataoncarrionbeetle’secologyandinsectsuccession.
acknowledgements
Jessica Dekeirsschieter is financially supported by a PhDgrantfromtheFondspourlaFormationàlaRecherchedansl’Industrieetl’Agriculture(F.R.I.A),Belgium.
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