Naja (Boulengerina) subfulva Laurent, 1955

Wüster, Wolfgang, Chirio, Laurent, Trape, Jean-François, Ineich, Ivan, Jackson, Kate, Greenbaum, Eli, Barron, Cesar, Kusamba, Chifundera, Nagy, Zoltán T., Storey, Richard, Hall, Cara, Wüster, Catharine E., Barlow, Axel & Broadley, Donald G., 2018, Integration of nuclear and mitochondrial gene sequences and morphology reveals unexpected diversity in the forest cobra (Naja melanoleuca) species complex in Central and West Africa (Serpentes: Elapidae), Zootaxa 4455 (1) : -

Naja (Boulengerina) subfulva Laurent, 1955

Naia melanoleuca (not Hallowell); Boulenger, 1896: 376 (part, vars A [c] & E).

Naja melanoleuca subfulva Laurent, 1955 , Revue Zool.– Bot. Afr. 51: 132. Type locality: Lwiro, 1850 m, Kabare, Kivu, Belgian Congo [= Democratic Republic of Congo], holotype MRAC 17514.

Naja melanoleuca aurata Stucki-Stirn, 1979 , Snake Report 721: 617–620. Type locality: Bamenda, Cameroon . No type designated.

Naja subfulva ; Chirio & Ineich, 2006: 54.

Naja melanoleuca subfulva ; Chirio & LeBreton, 2007: 584.

Naja (Boulengerina) melanoleuca subfulva ; Broadley & Blaylock, 2013: 139.

Naja (Boulengerina) melanoleuca ; Conradie et al., 2016: 28.

Diagnosis. MidbOdy scAlE rOws 19, ExcEpt AlONg cOAstAl rEgiONs Of EAst AfricA ( KENyA, TANzANiA), whErE mOst spEcimENs hAvE 17 rOws. PAttErN highly vAriAblE. Adults Of mOst pOpulAtiONs distiNguishAblE iN hAviNg A brOwN fOrEbOdy, OftEN with spOts, gENErAlly bEcOmiNg dArkEr Or blAckish pOstEriOrly. LAbiAl pAttErN mAy bE AttENuAtEd iN mANy Adults. VENtEr with sEvErAl blAck, dArk brOwN Or grEyish crOssbANds ON thE first 50 vENtrAls, grAduAlly bEcOmiNg uNifOrm blAck cAudAd iN sOmE pOpulAtiONs, but OftEN rEmAiNiNg ENtirEly light, OftEN with ExtENsivE dArkEr spOttiNg Or spEckliNg. WhErE prEsENt, thE light fOrEbOdy ANd/Or light pOstEriOr vENtEr ArE diAgNOstic fOr this spEciEs. GENErAlly fEwEr vENtrAl bANds ANd vENtrAl scAlEs thAN N. melanoleuca Or N. savannula ANd fEwEr subcAudAls thAN N. savannula ( TAblE 8). GENEticAlly diAgNOsAblE thrOugh pOssEssiON Of uNiquE mitOchONdriAl hAplOtypEs (cyt b: GENBANk MH337603 –633; ND4: MH337409 –439) ANd uNiquE PRLR ANd UBN1 hAplOtypEs (PRLR: MH337441 –471; UBN1: MH337531 , MH337536 –562, MH337564 –566).

Variation. DOrsAl scAlE rOws ON NEck 19–27, At midbOdy 19 (vEry rArEly 17 Or 21); vENtrAls 196–226; ANAl ENtirE; subcAudAls 55–71 ( TAblE 8). SuprAlAbiAls 7 (vEry rArEly 5 Or 6), thE third ANd fOurth ENtEriNg Orbit; iNfrAlAbiAls 8 (rArEly 7), thE first fOur (rArEly thrEE) iN cONtAct with thE ANtEriOr subliNguAls, NO cuNEAtE (vEry rArEly ONE); prEOculAr 1; pOstOculArs 3; tEmpOrAl 1+2 Or 1+3; tEmpOrAl bOrdEriNg pAriEtAls 5–9, usuAlly 7.

Colouration. HEAd brOwN, thE suprAlAbiAls usuAlly bArrEd blAck ANd yEllOw, chiN yEllOw. DOrsum uNifOrm blAck, Or with fAiNt whitE crOssbArs Or whitE-tippEd dOrsAl scAlEs, rEsultiNg iN A stippliNg EffEct, iN All juvENilEs. Adults frOm thE pEriphEry Of LAkE VictOriA ANd pArts Of thE CONgO BAsiN ( Fig. 9 ) hAvE A uNifOrmly blAck dOrsum As Adults, whErEAs iN mOst Of thE rANgE, Adults bEcOmE brOwN ANtEriOrly. ThErE mAy bE 2 Or 3 fAiNt yEllOw dividEd crOssbArs ON thE NEck. VENtrAl bANdiNg OftEN fAiNt iN Adults, with grEy Or pAlE brOwN vENtrAl bANds thAt mAy bE vEry iNcONspicuOus, Or lAckiNg AltOgEthEr. NArrOw AccEssOry vENtrAl bANds usuAlly AbsENt.

Largest recorded. 2016+380 = 2396 mm (tAil truNcAtEd) [JPT 1856 – ZiNAvE, MOzAmbiquE], but NMZB-UM 17594 frOm INyANgANi TEA EstAtEs, ZimbAbwE, hAd A tOtAl lENgth Of 2690 mm (ONly hEAd ANd NEck prEsErvEd).

Suggested common name. BrOwN fOrEst cObrA. This suggEstiON rEflEcts thE fAct thAt iN mOst pOpulAtiONs, with thE ExcEptiON Of thE surrOuNdiNgs Of LAkE VictOriA ANd sOmE lOcAtiONs iN thE CONgO BAsiN, thE ANtEriOr bOdy Of Adults is brOwN rAthEr thAN blAck. WE NOtE thAt thE distributiON Of this spEciEs iNcludEs mANy NON-fOrEstEd hAbitAts, iNcludiNg sAvANNAs ANd OpEN wEtlANds (SpAwls et al., 2018). HOwEvEr, rEtENtiON Of thE wOrd “fOrEst” iN thE cOmmON NAmE cONvEys thE phylOgENEtic iNfOrmAtiON thAt this spEciEs is pArt Of thE Naja melanoleuca cOmplEx.

Distribution. FOrEst/sAvANNA mOsAic, ENcircliNg thE CONgO BAsiN, frOm thE grAssfiElds Of wEstErN CAmErOON NOrthwArd, rEAchiNg 13.45°N At BOl, ChAd, ON thE NOrthErN shOrE Of LAkE ChAd (IRD 2802.N), EAst thrOugh thE CAR ANd SOuth SudAN tO wEstErN EthiOpiA, sOuth thrOugh UgANdA, wEstErN KENyA, EAstErN DRC, RwANdA, BuruNdi ANd wEstErN TANzANiA tO NOrthErN MAlAwi, wEst thrOugh ZAmbiA ANd KAtANgA tO ANgOlA ANd thE LOwEr CONgO rEgiON ( Fig. 6 ). ThE distributiON ExtENds disjuNctly EAst ANd sOuth tO thE EAst AfricAN cOAst frOm KENyA tO NOrthErN KwAZulu-NAtAl ( SOuth AfricA), iNcludiNg iNlANd lOcAtiONs iN wEstErN ZimbAbwE. ThE prEcisE distributiON Of this tAxON iN thE CONgO rEgiON rEmAiNs tO bE AscErtAiNEd: wE hAvE hErE prOvidEd mOlEculAr EvidENcE Of multiplE spEcimENs Of this spEciEs frOm thE EvErgrEEN fOrEst zONE Of NOrthErN REpublic Of CONgO (LikOuAlA FOrEst – JAcksON et al., 2007) ANd thE NOrthEAstErN DRC (NOrthwEstErN OriENtAlE PrOviNcE AlONg thE CONgO RivEr). SOmE Of thEsE spEcimENs ANd pOpulAtiONs ArE difficult tO diffErENtiAtE frOm sympAtric N. melanoleuca , NEcEssitAtiNg thE usE Of DNA bArcOdiNg ApprOAchEs (HEbErt et al., 2003; ClAusE et al., 2016) tO ENsurE rEliAblE idENtificAtiON. TwO spEcimENs frOm sOuthEAstErN NigEriA with lOw vENtrAl scAlE cOuNts ANd lAckiNg vENtrAl bANdiNg Or displAyiNg A siNglE fAdEd bANd mAy AlsO bE AssigNAblE tO this spEciEs (DEgEmA, RivErs StAtE: BMNH 1902.11.10.9, ANd “Oil RivEr ”: BMNH 88.8.29.20), suggEstiNg A widEr distributiON iN EAstErN NigEriA.

Comment. This spEciEs displAys cONsidErAblE gEOgrAphic vAriAtiON iN pAttErN ANd scAlAtiON, As wEll As iNdicAtiONs Of phylOgEOgrAphic structurE. ThE prEsENt study fOcusEd ON thE rElAtiONships AmONg thE fivE mitOchONdriAlly dEfiNEd cANdidAtE spEciEs, ANd did NOt ENcOmpAss thE full rANgE Of mOrphOlOgicAl vAriAtiON iN N. subfulva . It is pOssiblE thAt futurE wOrk mAy idENtify AdditiONAl cryptic divErsity withiN this widE-rANgiNg ANd vAriAblE spEciEs.

Figures

FIGURE 6. Distribution of the five species of the N. melanoleuca complex. A full list of voucher specimens beyond those included in multivariate analyses and Appendix 2 is available on request from the first author.

FIGURE 9. Naja (Boulengerina) subfulva. Variation in colour and pattern. Top left: specimen from Kakamega, western Kenya, illustrating the typically deep black and white specimens with strong facial markings from the periphery of Lake Victoria. Bottom left: specimen from Chuka, Mount Kenya, Kenya, illustrating an extreme of the brown forebody and reduced facial pigmentation typical of the species in much of its range. Photos W. Wüster, courtesy Royjan Taylor / Bio-Ken snake farm live collection, Watamu, Kenya. Right: specimen from Bamenda, Cameroon, representing the form described by Stucki-Stirn (1979) as Naja melanoleuca aurata. Note the indistinct ventral bands and the lack of accessory ventral bands, as is typical of this species. Photo J.-F. Trape.