large carrion beetles (coleoptera, silphidae) in western europe: a … · 2011-09-07 · entomology...
TRANSCRIPT
BASE Biotechnol. Agron. Soc. Environ.201115(3),435-447 Focus on:
Largecarrionbeetles(Coleoptera,Silphidae)inWesternEurope:areviewJessicaDekeirsschieter(1),FrançoisVerheggen(1),GeorgesLognay(2),EricHaubruge(1)(1)Univ.Liege-GemblouxAgro-BioTech.DepartmentofFunctionalandEvolutionaryEntomology.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:[email protected],[email protected](2)Univ.Liege-GemblouxAgro-BioTech.DepartmentofAnalysisQualityandRisks.LaboratoryofAnalyticalChemistry.PassagedesDéportés,2.B-5030Gembloux(Belgium).
ReceivedonApril20,2010;acceptedonOctober5,2010.
Thisreviewfocusesoncarrionbeetles(Coleoptera,Silphidae)oftheWesternPalearcticandtheirpotentialuseinforensicentomologyasbioindicators.Fewstudieshave lookedatSilphidae inforensiccontextand investigations.However,someSilphidaepresentthedesirablecharacteristicsofsomeDipterausedinpostmortemestimatesandthusmayextendtheminimumpostmorteminterval(PMImin).WereviewherethetaxonomyanddistributionofWesternPalearcticSilphidae.Theanatomicalandmorphologicalcharacteristicsofbothsubfamiliesaredescribedforadultsandlarvae.ThebiologyandecologyofsilphidsarealsosummarizedforSilphinaeandNicrophorinae.AspecificchaptergivesanoverviewofthecurrentusesofSilphidaeinforensicentomologyaspostmortemindicator.Keywords.Silphidae,buryingbeetles,forensicentomology,taxonomy,identification,WesternEurope.
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
436 Biotechnol. Agron. Soc. Environ. 201115(3),435-447 DekeirsschieterJ.,VerheggenF.,LognayG.etal.
(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.
Subfamilynicrophorinae KIrby, 1837 Silphinae LatrEILLE, 1807
Genus NicrophorusFABRICIUS,1775 AblattariaREITTER,18851884AclypeaREITTER,1884OiceoptomaLEACH,1815PhosphugaLEACH,1817SilphaLINNAEUS,1758ThanatophilusLEACH,1815NecrodesLEACH,1815DendroxenaMOTSCHULSKY,1858
Species * Nicrophorus germanicusLINNAEUS,1758 *Necrodes littoralisLINNAEUS,1758* Nicrophorus humatorGLEDITSCH,1767 *Thanatophilus disparHERBST,1793* Nicrophorus investigatorZETTERSTEDT,1824 *Thanatophilus rugosusLINNAEUS,1758*Nicrophorus interruptusSTEPHENS,1830 *Thanatophilus sinuatusFABRICIUS,1775*Nicrophorus sepulchralisHEER,1841 *Oiceoptoma thoracicumLINNAEUS,1758* Nicrophorus sepultorCHARPENTIER,1825 *Silpha carinataHERBST,1783* Nicrophorus vespilloLINNAEUS,1758 *Silpha obscura obscura LINNAEUS,1758* Nicrophorus vespilloidesHERBST,1783 *Silpha tristisILLIGER,1798* Nicrophorus vestigatorHERSCHEL,1807 *Silpha olivieriBEDEL,1887* Nicrophorus nigricornisFALDERMANN,1835 *Silpha puncticollisLUCAS,1846* Nicrophorus antennatusREITER,1884 *Silpha tyrolensis LAICHARTING,1781
Phosphuga atrata atrataLINNAEUS,1758Dendroxena quadrimaculataSCOPOLI,1772Ablattaria laevigata laevigataFABRICIUS,1775Aclypea opacaLINNAEUS,1758Aclypea undataMULLER,1776Aclypea souverbieiFAIRMAIRE,1848
*: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.
438 Biotechnol. Agron. Soc. Environ. 201115(3),435-447 DekeirsschieterJ.,VerheggenF.,LognayG.etal.
(Newton,1991).Eachsubfamilyhasaverydistinctivehabitus(Newton,1991)(Figure 4).
3.1. Silphinae
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.
ReviewofEuropeanSilphidae 439
clearly separate, but strongly constricted medially(Peck,1990;Sikes,2005).Theantennaehaveelevenwell differentiated segments broaden gradually;particularlythelastthreeorfoursegments(Figure 3b,3c,3d).
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,
440 Biotechnol. Agron. Soc. Environ. 201115(3),435-447 DekeirsschieterJ.,VerheggenF.,LognayG.etal.ta
ble
2.EcologicalandbodysizeofN
icrophorinaeofW
esternEurope(trophicgroup:necrophagousp
redaceous)—
Car
acté
rist
ique
s éc
olog
ique
s et m
orph
olog
ique
s de
s Nic
roph
orin
ae d
e l’E
urop
e de
l’ou
est (
grou
pe tr
ophi
que
: pré
date
ur n
écro
phag
e).
Spec
ies
dist
ribu
tion
abu
ndan
cebo
dy si
ze(inmm)
tem
pora
l act
ivity
hab
itat p
refe
renc
e &
/or
loca
tion
dai
ly a
ctiv
ity
Nic
roph
orus
ger
man
icus
BE-FR
-GE-LU
-NL-DE-
GB-IT-SZ
rare
20-35
May-September
field,largecadaver,dung
nocturnal
Nic
roph
orus
hum
ator
BE-FR
-GE-LU
-NL-DE-
GB-IT-PT-SP-SZ
verycom
mon
14-33
April-Septem
ber
forest(hardw
ood),cadaver,rotten
mushrooms
nocturnal
Nic
roph
orus
inve
stig
ator
BE-FR
-GE-LU
-NL-DE-
GB-IT-SP-SZ
common
11-22
April-Septem
ber
forest,openareas,cadaver
crepuscular
Nic
roph
orus
inte
rrup
tus
BE-FR
-GE-LU
-NL-DE-
GB-IT-PT-SP-SZ
rare
10-22
April-October
field,som
etimesinforest,cadaver
crepuscular
Nic
roph
orus
sepu
lchr
alis
FR
-IT-SZ
rare
19-21
N.A.
cadaver,Europeanmountainspecies
(Alps)
N.A.
Nic
roph
orus
sepu
ltor
DE-FR
-GE-IT-NL-SP-SZ
veryrare
11-22
April-Septem
ber
forest,openareas,cadaver,rotten
mushrooms
N.A.
Nic
roph
orus
ves
pillo
BE-FR
-GE-LU
-NL-DE-
GB-IT-PT-SP-SZ
common
10-23
May-September
field,openareas,sometimesinforest,
cadaver
crepuscular,
nocturnal
Nic
roph
orus
ves
pillo
ides
BE-FR
-GE-LU
-NL-DE-
GB-IT-SP-SZ
verycom
mon
9-19
April-Septem
ber
forest,cadaver,rottenmushrooms
diurnal
Nic
roph
orus
ves
tigat
or
BE-FR
-GE-LU
-NL-DE-
GB-IT-PT-SP-SZ
common
9-23
April-October
field,openareas,cadaver
N.A.
Nic
roph
orus
nig
rico
rnis
FR
rare
12-20
N.A.
cadaver,mountainspecies(Caucasius)
N.A.
Nic
roph
orus
ant
enna
tus
FR-IT-NL
rare
N.A.
N.A.
cadaver
N.A.
BE:Belgium
—B
elgi
que;FR:France—F
ranc
e;Ge:Germany—A
llem
agne;L
u:Luxem
bourg—L
uxem
bour
g;NL:TheNetherlands—
Pay
s-Ba
s;DE:Denmark—D
anem
ark;
GB:G
reatBritain—G
rand
e-Br
etag
ne;IT:Italy—It
alie;PT:Portugal—
Por
tuga
l;SP:Spain—
Esp
agne;SZ:Switzerland—
Sui
sse.N.A.:notavailabledatainthespecific
literature—d
onné
esin
disp
onib
les d
ans l
a lit
téra
ture
spéc
ialis
ée (P
ortevin,1926;Heinz,1971;Andersonetal.,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;
Ružickaetal.,2004;Aleksandrow
iczetal.,2005;Chauvetetal.,2008).
ReviewofEuropeanSilphidae 441
tabl
e 3.EcologicalandbodysizeofS
ilphinaeofWesternEurope—C
arac
téri
stiq
ues é
colo
giqu
es e
t mor
phol
ogiq
ues d
es S
ilphi
nae
de l’
Euro
pe d
e l’O
uest
.Sp
ecie
sd
istri
butio
na
bund
ance
body
size
(inmm)
tem
pora
l act
ivity
hab
itat
pref
eren
ce &
/or
loca
tion
dai
ly
activ
itytr
ophi
c gr
oup
Nec
rode
s litt
oral
is
BE-FR
-LU-GE-NL-
SP-DE-GB-IT-PT-SZ
common
15-25
April-Septem
ber
forestoropenareas,
cadaver(largecarcass),
below
seaw
eeds
N.A.
necrophagous
predaceous
Than
atop
hilu
s d
ispa
r BE-FR
-GE-NL-DE-
GB-IT-SZ
rare
8-11
May-July
field,cadaver
diurnal
necrophagous
Than
atop
hilu
s r
ugos
us
BE-FR
-LU-GE-NL-
DE-GB-IT-PT-SP-SZ
common
9-12
April-Septem
ber
field,openareas,
cadaver
diurnal
necrophagous
predaceous
Than
atop
hilu
s s
inua
tus
BE-FR
-LU-GE-NL-
DE-GB-IT-PT-SP-SZ
verycom
mon
9-12
April-Septem
ber
field,openareas,
cadaver
diurnal
necrophagous
predaceous
Oic
eopt
oma
tho
raci
cum
BE-FR
-LU-GE-NL-
DE-GB-IT-SP-SZ
common
11-16
April-Septem
ber
forest,cadaver,dung,
mushrooms(
e.g.
Pha
llussp.)
diurnal
necrophagous
predaceous
Silp
ha c
arin
ata
BE-FR
-LU-GE-NL-
DE-GB-IT-SZ
common
13-20
April-Septem
ber
(imagohibernatesunder
barkso
ftrees)
forest,cadaver,crushed
slugsandsn
ails,
mushrooms
N.A.
necrophagous
predaceous
Silp
ha o
bscu
ra
obs
cura
BE-FR
-LU-GE-NL-
DE-GB-IT-SP-SZ
common
11.5-17
May-September(imago
hibernatesinlitter&
soil)
field,openareas
N.A.
predaceous
necrophagous
Silp
ha tr
istis
BE-FR
-LU-GE-NL-
DE-GB-IT-PT-SP-SZ
rare
13-15
May-September(imago
hibernatesinlitter&
soil)
field
N.A.
predaceous
necrophagous
Silp
ha o
livie
ri
FR-IT-PT-SP
rare
15-19
MidM
arch-M
idSeptember
Mediterraneanspecies
N.A.
predaceous
Silp
ha p
unct
icol
lis
FR-IT-PT-SP
rare
14-17
MidM
arch-M
idSeptember
Mediterraneanspecies
N.A.
predaceous
Silp
ha ty
role
nsis
FR
-GB-IT-PT-SP
rare
13-14
MidM
arch-M
idSeptember
mountainspecies
N.A.
predaceous
Phos
phug
a at
rata
a
trat
a BE-FR
-KU-GE-NL-
DE-GB-IT-PT-SP-SZ
verycom
mon
9-16
May-October(imagohibernates
underabark,mosso
rlitter)
forest
N.A.
predaceous
(snails)
Den
drox
ena
qua
drim
acul
ata
BE-FR
-KU-GE-NL-
DE-GB-IT-SP-SZ
common
11-14
May-July
forest(deciduous
forest)
N.A.
predaceous
(caterpillars)
Abla
ttari
a la
evig
ata
laev
igat
a BE-FR
-LU-GE-NL-
GB-IT-SP-SZ
rare
11-16
May-October
field,gardens
N.A.
predaceous
(snails)
Acly
pea
opac
a BE-FR
-LU-GE-NL-
DE-GB-IT-SP-SZ
common
9-12
April-Septem
ber
field
N.A.
phytophagous
(Chenopodiaceae,
pestofsugarbeets)
Acly
pea
unda
ta
BE-FR
-LU-GE-NL-
DE-GB-IT-PT-SP-SZ
rare
11-16
April-Septem
ber
field
N.A.
phytophagous
(Chenopodiaceae)
Acly
pea
souv
erbi
ei
FR-GE-SP
rare
10-12
N.A.
N.A.
N.A.
phytophagous
legend—
lége
nde:see
tabl
e 2-v
oirt
able
au 2.
442 Biotechnol. Agron. Soc. Environ. 201115(3),435-447 DekeirsschieterJ.,VerheggenF.,LognayG.etal.
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
ReviewofEuropeanSilphidae 443
thepre-pupalstageforsomespecies(Ratcliffe,1996;Ohkawaraetal.,1998).Sometimes,nicrophorinemaycolonizelargecarcass(toolargetobury)andseveralmale-femalepairsbreedcommunallytheirlarvaeinasubsocial fashion: cooperative breeding (Pukowski,1933; Eggert et al., 1992; Ratcliffle, 1996; Scott,1998).
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;
444 Biotechnol. Agron. Soc. Environ. 201115(3),435-447 DekeirsschieterJ.,VerheggenF.,LognayG.etal.
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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