Amphibia-Reptilia 31 (2010) 571-575

On the occurrence of facultative paedomorphosis in the three newtspecies of Southern Iberian Peninsula (Amphibia Salamandridae)

Francisco Ceacero1lowast David Donaire-Barroso2 Enrique Garciacutea-Muntildeoz3

Juan Francisco Beltraacuten4 Miguel Tejedo5

Abstract We report the occurrence of facultative paedomorphosis in the three species of newts (Pleurodeles waltl Lissotritonboscai and Triturus pygmaeus) from dry and seasonal Mediterranean areas from southern Spain These are the first records ofpaedomorphosis for P waltl and L boscai and the second for T pygmaeus Other than the previous T pygmaeus record theseare the first observations of paedomorphosis in the southern half of the Iberian Peninsula Most of specimens demonstratingpaedomorphosis live in artificially permanent aquatic environments Nevertheless a paedomorphic individual of L boscai wasfound in a natural yearly temporary brook that held water during the previous two years Paedomorphs are at low frequencyin most cases However a single isolated population of P waltl is probably composed entirely of paedomorphs

Keywords Lissotriton boscai paedomorphs Pleurodeles waltl Spain Triturus pygmaeus

Facultative paedomorphosis is widespreadthrough caudate families and across a largediversity of environments (Wells 2007) It isconsidered an adaptive strategy to highly het-erogeneous aquaticterrestrial environments dueto the multitude of ecological and evolution-ary trade-offs of each individual strategy (De-noeumll Joly and Whiteman 2005) Facultativepaedomorphosis has been reported in severalEuropean newts of the former genus Triturusincluding T cristatus T carnifex T vittatusMesotriton alpestris Lissotriton italicus Lis-sotriton helveticus and L vulgaris (Kalezic etal 1996 Denoeumll and Joly 2000 Denoeumll 20032007 Sindaco et al 2006 Kaya et al 2008

1 - Departamento de Ciencia y Tecnologiacutea Agroforestal yGeneacutetica ETSIA UCLM Campus Universitario sn02071 Albacete Spain

2 - Calle Mar Egeo 7 11407 Jerez de la Frontera Spain3 - Departamento de Biologiacutea Animal Biologiacutea Vegetal y

Ecologiacutea Campus de las Lagunillas sn Universidad deJaeacuten 23071 Jaeacuten Spain

4 - Departamento de Fisiologiacutea y Zoologiacutea Facultad de Bi-ologiacutea Universidad de Sevilla Avda Reina Mercedes 641012 Sevilla Spain

5 - Departamento de Ecologiacutea Evolutiva Estacioacuten Bioloacuteg-ica de Dontildeana CSIC Avda Ameacuterico Vespucio sn41092 Sevilla SpainlowastCorresponding author e-mailfranciscoceacerouclmes

Denoeumll et al 2009) showing a wide occur-rence among species and with an apparent in-traspecific geographic variation Paedomorpho-sis occurs more commonly in southern Europe(the Alps and the Balkan and Italian Peninsu-las Denoeumll et al 2001) However few pae-domorphic accounts exist at the Iberian Penin-sula which is inhabited by 10 species of nativesalamandrids Most of the records correspondto large overwintering larvae Chioglossa lusi-tanica Salamandra salamandra T marmora-tus (Salvador and Garciacutea-Pariacutes 2001) T pyg-maeus (Reques 2007) Pleurodeles waltl (Al-berch and Gonzaacutelez 1973 Alvarez Salvadorand Arguello 1988 Bogaerts and van Uche-len 2003) L boscai (Bedriaga 1896 O Ar-ribas personal observation) L helveticus (OArribas personal observation) M alpestris (Ar-ribas 2008) Calotriton asper (Campeny Mon-tori and Llorente 1986) However very fewof these records were considered paedomorphsThe two reports of paedomorphosis are Malpestris (species living at northern Spain) (Ar-ribas 2008) and a population of T pygmaeusin southern Spain (Reques 2007) Here we re-port the occurrence of paedomorphosis in threenewt species P waltl L boscai and T pyg-maeus from dry and seasonal Mediterranean

copy Koninklijke Brill NV Leiden 2010 DOI101163017353710X521528

572 Short Notes

Table 1 Characteristics of the aquatic environments where paedomorphs were found

Species Locality Aquatic Drying Terrestrialhabitat probability habitat

1 P waltl Cantildeada de las Azadillas Sa

Sur (Jaeacuten) 3740N 343W880 m

60 m2 swimming pool fedby rain streams Max depth1 m

No Pine wood forest

2 P waltl El Cuervo (Sevilla) 3652N601W 33 m

25 m2 ancient agriculturewell Max depth 4 m

No Agricultural landscape

3 T pygmaeus Fuente la Zarza Sierra Sur(Jaeacuten) 3746N 349W740 m

5 m2 round pond fed bya small source Max depth05 m

No Pasture scrubland andpine wood

4 L boscai La Sorda Sierra de Ara-cena (Huelva) 3754N634W 660 m

15 m2 small puddle rem-nant of a dried temporarybrook Max depth 05 m

High Mediterraneanscrubland

areas from southern Iberian Peninsula and de-scribe their phenotypes and environments

Sampled locations with paedomorphic individuals areshown in table 1 and dates are indicated in the results sec-tion In all cases animals were captured by dip-nettingBody length was measured using digital calliper (meanplusmnSEthroughout the manuscript) Paedomorphs were assessed byobservation of adult traits such as swollen cloacae presenceof nuptial pads and eventually courtship behaviour in com-bination with very large size open gill slits and morphologyand colouration that either differed clearly from the larvalphenotype All the animals were subsequently released al-though in some cases animals were transported to the lab-oratory for other research purposes All ponds with paedo-morphic newts were periodically monitored thereafter al-though paedomorphs were not always observed again

Pleurodeles waltl paedomorphs were ob-served in two locations (1 and 2 table 1)On June 17th 2007 a mature paedomorph maleexhibiting adult and metamorph aspect andcolouration nuptial pads and swollen cloacaewas found in location 1 (SVL = 880 mmTL = 1843 fig 1A) On January 31st 2009a paedomorph female was observed at the samelocation (SVL = 456 mm TL = 828 mm)with the same characteristics as the previouslydescribed individual Paedomorphs in location2 were first visually recorded on March 17th2007 This population was sampled on Feb-ruary 8th 2008 containing only paedomorphs[SVL = 623 plusmn 15 mm (range = 516-788mm) TL = 1327 plusmn 26 mm (range = 1057-1721 mm) n = 13] All individuals exhibitedsexual characters such as swollen cloacae andstrong forelimbs with black nuptial pads The

coloration was dark brownish with small blotsThe gill slits remained open One male and onefemale paedomorph were transported to the laband to date (May 2010) none of them resumedto metamorphosis In January 2010 they wereobserved in amplexus On March 12th 2010we captured two distinct groups of individualswidely different in size larvae [TL = 372plusmn11mm (range = 301-412 mm) n = 12] and largesize paedormorphs three males and one female[TL = 1433 plusmn 38 mm (range = 1212-1623mm) n = 4] all of them branchiated and withswollen cloacae Males did not exhibit nuptialpads

Triturus pygmaeus paedomorphs were ob-served in location 3 on April 1st 2005 Elevenindividuals with two distinct phenotypes (re-garding size and aspect) were captured Paedo-morphs [SVL = 363 plusmn 14 mm (range = 325-413 mm) TL = 740 plusmn 16 mm (range =657-837 mm) n = 4 fig 1B] were clearlybigger than larvae [SVL = 182 plusmn 03 mm(range = 167-199 mm) TL = 361 plusmn 07 mm(range = 330-403 mm) n = 7] Paedomorphsshowed a similar and opaque colouration to thatof the adults and metamorphs from the samepopulation with swollen cloacae and extensionof caudal and dorsal fins similar to adult maleswhile larvae showed the normal traits and theirnormal translucent colouration This populationwas subsequently monitored in 2007 and 2009but no paedomorph was observed

Short Notes 573

Figure 1 (A) Pleurodeles waltl paedomorph male from location 1 Note the adult colouration and the absence of dorsalcrest (larval trait) (B) Triturus pygmaeus paedomorph male from location 3 Note the adult colouration and the swollencloaca (white arrow) (C) Lissotriton boscai paedomorph male from location 4 Note the adult colouration and the swollencloaca (white arrow)

574 Short Notes

A Lissotriton boscai paedomorph male wascaptured in location 4 on September 8th 2004(SVL = 306 mm TL = 636 mm) whichexhibited a mosaic of juvenile and male adulttraits Dorsal coloration was brownish withsome black spots along the tail and body sidesBelly was yellowish with a swollen roundedcloaca with a long obvious opening Addition-ally it exhibited a small tail crest and a tiny fila-ment of around 2-3 mm at the end of the tail (fig1C) The paedomorph was maintained in the laband on October 10th 2004 courtship activity wasobserved and voluntarily repeated for severaldays The newt was kept during three monthsin the lab until it was released Courtship be-haviour was repeatedly observed and no signsof metamorphosis were evidenced to that dateNo L boscai larvae were found at this later datesuggesting that remaining larvae resumed meta-morphosis during late spring and summer Thislocality was periodically sampled since 2004but no other paedomorph has been recorded todate

This report describes the occurrence of pae-domorphosis in the three newt species occurringin southern Iberia Paedomorphosis is describedfor the first time in P waltl and L boscaisince previously both species only had recordsfor non-paedomorphs big size larvae (Bedriaga1896 Alberch and Gonzaacutelez 1973 AlvarezSalvador and Arguello 1988 Bogaerts and vanUchelen 2003 O Arribas personal observa-tion) and the second record of paedomorphosisin T pygmaeus (see Reques 2007)

P waltl paedomorphs were found in man-made permanent aquatic habitats with no pres-ence of predatory fishes (Collins Zerba andSredl 1993) although intraspecific cannibal-ism in P waltl has been observed at location1 and it seems likely at location 2 In gen-eral paedomorphs of P waltl at location 1and T pygmaeus at location 3 coexisted in avery low frequency with metamorphic individu-als However P waltl population at location 2which inhabits a steep-sided and narrow wellthat rarely oscillates in its water level was com-

prised of only paedomorphs No metamorphicindividuals were found during two samplingsthus suggesting that it may be a completely pae-domorphic population Interestingly a P waltlmetamorphic population occupies a wider andbigger nearby well less than 200 m away Tpygmaeus paedomorphs were also observed ina permanent natural source however the pae-domorphic male of L boscai was found in apuddle within a temporary creek which gener-ally desiccates each summer This sexually ma-ture individual presumably had a maximum ageof one-two years since the puddle had lastedapproximately two years without drying Thusthe specimen could have attained its large sizeand maturity during that time However no ev-idence of paedomorphic newts has been foundto date despite intensive sampling of nearbypermanent environments thus suggesting thatthe frequency of this alternative developmentalpathway is very low in this species

In conclusion southern Iberian newts seemto maintain the capacity to exhibit alternativedevelopmental pathways under different kindsof environmental conditions Thus our obser-vations suggest that paedomorphosis althoughrare seems to be relatively widespread in south-ern Iberia than often thought and deserves moreattention to explain its maintenance

Acknowledgements The authors wish to thank AHidalgo-Pontiveros and L Pedrajas for their help duringfield trips A Conejo for the picture of L boscai larvae andJ Leonard for the useful suggestions and linguistic revisionAnimals transported to the laboratory were collected withthe authorisation of the ldquoConsejeriacutea de Medio Ambiente dela Junta de Andaluciacuteardquo

References

Alberch P Gonzaacutelez D (1973) Notas sobre la distribu-cioacuten biotopo morfologiacutea y biometriacutea de Pleurodeleswaltl Michahelles en el NE de la Peniacutensula Ibeacuterica (Am-phibia Salamandridae) Misc Zool 3 71-82

Alvarez J Salvador A Arguello JA (1988) Desarrollolarvario del gallipato (Pleurodeles waltl) en una charcatemporal del noroeste Ibeacuterico (Amphibia Salamandri-dae) Ecologiacutea 2 293-301

Short Notes 575

Arribas O (2008) Neotenia y longitud excepcional enMesotriton alpestris de Fuentes Carrionas (Palencia)Bol Asoc Herpetol Esp 19 23-24

Bedriaga J von (1896) Die lurchfauna Europa II UrodelaSchwanzlurche B Soc Imp Nat Moscou 10 38-705

Bogaerts S van Uchelen E (2003) Fund einer riesenlarvedes rippenmolches Pleurodeles waltl Michaelles 1830in der provinz Huelva Spanien Sauria 25 13-15

Campeny R Montori A Llorente GA (1986) Nuevosdatos sobre la permanencia de caracteres larvarios enindividuos adultos de una poblacioacuten de tritoacuten pirenaico(Euproctus asper) en el valle de Aran Dontildeana ActaVertebrata 13 170-173

Collins JP Zerba KE Sredl MJ (1993) Shaping in-traspecific variation development ecology and the evo-lution of morphology and life history variation in tigersalamanders Genetica 89 167-183

Denoeumll M (2003) How do paedomorphic newts cope withlake drying Ecography 26 405-410

Denoeumll M (2007) Priority areas of intraspecific diversityLarzac a global hotspot for facultative paedomorphosisin amphibians Anim Conserv 10 110-116

Denoeumll M Joly P (2000) Neoteny and progenesis as twoheterochronic processes involved in paedomorphosis inTriturus alpestris (Amphibia Caudata) Proc R SocLond B Biol Sci 267 1481-1485

Denoeumll M Duguet R Dzukic G Mazzotti S (2001)Biogeography and ecology of paedomorphosis in Trit-urus alpestris (Amphibia Caudata) J Biogeogr 281271-1280

Denoeumll M Joly P Whiteman HH (2005) Evolutionaryecology of facultative paedomorphosis in newts andsalamanders Biol Rev 80 663-671

Denoeumll M Ficetola GF Cirovic R Radovic D DžukicG Kalezic ML Vukove TD (2009) A multi-scaleapproach to facultative paedomorphosis of Europeannewts (Salamandridae) in the Montenegrin karst Distri-bution pattern environmental variables and conserva-tion Biol Conserv 142 509-517

Kalezic ML Cvetkovic D Djorovic A Dzukic G(1996) Alternative life-history pathways paedomor-phosis and adult fitness in European newts (Triturus vul-garis and T alpestris) J Zool Syst Evol Res 34 1-7

Kaya U Sayım F Baskale E Ccedilevik IE (2008) Paedo-morphosis in the banded newt Triturus vittatus (Jenyns1835) Belg J Zool 138 196-197

Reques R (2007) Tritoacuten pigmeo ndash Triturus pygmaeus InEnciclopedia Virtual de los Vertebrados Espantildeoles Car-rascal LM Salvador A Eds Madrid Museo Nacionalde Ciencias Naturales

Salvador A Garciacutea-Pariacutes M (2001) Anfibios EspantildeolesTalavera de la Reina Canseco Eds

Sindaco R Doria G Razzetti E Bernini F (2006) Atlasof Italian Amphibians and Reptiles Firenze EdizioniPolistampa

Wells KD (2007) The Ecology and Behaviour of Am-phibians Chicago The University of Chicago Press

Received January 14 2010 Accepted May 23 2010

572 Short Notes

Table 1 Characteristics of the aquatic environments where paedomorphs were found

Species Locality Aquatic Drying Terrestrialhabitat probability habitat

1 P waltl Cantildeada de las Azadillas Sa

Sur (Jaeacuten) 3740N 343W880 m

60 m2 swimming pool fedby rain streams Max depth1 m

No Pine wood forest

2 P waltl El Cuervo (Sevilla) 3652N601W 33 m

25 m2 ancient agriculturewell Max depth 4 m

No Agricultural landscape

3 T pygmaeus Fuente la Zarza Sierra Sur(Jaeacuten) 3746N 349W740 m

5 m2 round pond fed bya small source Max depth05 m

No Pasture scrubland andpine wood

4 L boscai La Sorda Sierra de Ara-cena (Huelva) 3754N634W 660 m

15 m2 small puddle rem-nant of a dried temporarybrook Max depth 05 m

High Mediterraneanscrubland

areas from southern Iberian Peninsula and de-scribe their phenotypes and environments

Sampled locations with paedomorphic individuals areshown in table 1 and dates are indicated in the results sec-tion In all cases animals were captured by dip-nettingBody length was measured using digital calliper (meanplusmnSEthroughout the manuscript) Paedomorphs were assessed byobservation of adult traits such as swollen cloacae presenceof nuptial pads and eventually courtship behaviour in com-bination with very large size open gill slits and morphologyand colouration that either differed clearly from the larvalphenotype All the animals were subsequently released al-though in some cases animals were transported to the lab-oratory for other research purposes All ponds with paedo-morphic newts were periodically monitored thereafter al-though paedomorphs were not always observed again

Pleurodeles waltl paedomorphs were ob-served in two locations (1 and 2 table 1)On June 17th 2007 a mature paedomorph maleexhibiting adult and metamorph aspect andcolouration nuptial pads and swollen cloacaewas found in location 1 (SVL = 880 mmTL = 1843 fig 1A) On January 31st 2009a paedomorph female was observed at the samelocation (SVL = 456 mm TL = 828 mm)with the same characteristics as the previouslydescribed individual Paedomorphs in location2 were first visually recorded on March 17th2007 This population was sampled on Feb-ruary 8th 2008 containing only paedomorphs[SVL = 623 plusmn 15 mm (range = 516-788mm) TL = 1327 plusmn 26 mm (range = 1057-1721 mm) n = 13] All individuals exhibitedsexual characters such as swollen cloacae andstrong forelimbs with black nuptial pads The

coloration was dark brownish with small blotsThe gill slits remained open One male and onefemale paedomorph were transported to the laband to date (May 2010) none of them resumedto metamorphosis In January 2010 they wereobserved in amplexus On March 12th 2010we captured two distinct groups of individualswidely different in size larvae [TL = 372plusmn11mm (range = 301-412 mm) n = 12] and largesize paedormorphs three males and one female[TL = 1433 plusmn 38 mm (range = 1212-1623mm) n = 4] all of them branchiated and withswollen cloacae Males did not exhibit nuptialpads

Triturus pygmaeus paedomorphs were ob-served in location 3 on April 1st 2005 Elevenindividuals with two distinct phenotypes (re-garding size and aspect) were captured Paedo-morphs [SVL = 363 plusmn 14 mm (range = 325-413 mm) TL = 740 plusmn 16 mm (range =657-837 mm) n = 4 fig 1B] were clearlybigger than larvae [SVL = 182 plusmn 03 mm(range = 167-199 mm) TL = 361 plusmn 07 mm(range = 330-403 mm) n = 7] Paedomorphsshowed a similar and opaque colouration to thatof the adults and metamorphs from the samepopulation with swollen cloacae and extensionof caudal and dorsal fins similar to adult maleswhile larvae showed the normal traits and theirnormal translucent colouration This populationwas subsequently monitored in 2007 and 2009but no paedomorph was observed

Short Notes 573

Figure 1 (A) Pleurodeles waltl paedomorph male from location 1 Note the adult colouration and the absence of dorsalcrest (larval trait) (B) Triturus pygmaeus paedomorph male from location 3 Note the adult colouration and the swollencloaca (white arrow) (C) Lissotriton boscai paedomorph male from location 4 Note the adult colouration and the swollencloaca (white arrow)

574 Short Notes

A Lissotriton boscai paedomorph male wascaptured in location 4 on September 8th 2004(SVL = 306 mm TL = 636 mm) whichexhibited a mosaic of juvenile and male adulttraits Dorsal coloration was brownish withsome black spots along the tail and body sidesBelly was yellowish with a swollen roundedcloaca with a long obvious opening Addition-ally it exhibited a small tail crest and a tiny fila-ment of around 2-3 mm at the end of the tail (fig1C) The paedomorph was maintained in the laband on October 10th 2004 courtship activity wasobserved and voluntarily repeated for severaldays The newt was kept during three monthsin the lab until it was released Courtship be-haviour was repeatedly observed and no signsof metamorphosis were evidenced to that dateNo L boscai larvae were found at this later datesuggesting that remaining larvae resumed meta-morphosis during late spring and summer Thislocality was periodically sampled since 2004but no other paedomorph has been recorded todate

This report describes the occurrence of pae-domorphosis in the three newt species occurringin southern Iberia Paedomorphosis is describedfor the first time in P waltl and L boscaisince previously both species only had recordsfor non-paedomorphs big size larvae (Bedriaga1896 Alberch and Gonzaacutelez 1973 AlvarezSalvador and Arguello 1988 Bogaerts and vanUchelen 2003 O Arribas personal observa-tion) and the second record of paedomorphosisin T pygmaeus (see Reques 2007)

P waltl paedomorphs were found in man-made permanent aquatic habitats with no pres-ence of predatory fishes (Collins Zerba andSredl 1993) although intraspecific cannibal-ism in P waltl has been observed at location1 and it seems likely at location 2 In gen-eral paedomorphs of P waltl at location 1and T pygmaeus at location 3 coexisted in avery low frequency with metamorphic individu-als However P waltl population at location 2which inhabits a steep-sided and narrow wellthat rarely oscillates in its water level was com-

prised of only paedomorphs No metamorphicindividuals were found during two samplingsthus suggesting that it may be a completely pae-domorphic population Interestingly a P waltlmetamorphic population occupies a wider andbigger nearby well less than 200 m away Tpygmaeus paedomorphs were also observed ina permanent natural source however the pae-domorphic male of L boscai was found in apuddle within a temporary creek which gener-ally desiccates each summer This sexually ma-ture individual presumably had a maximum ageof one-two years since the puddle had lastedapproximately two years without drying Thusthe specimen could have attained its large sizeand maturity during that time However no ev-idence of paedomorphic newts has been foundto date despite intensive sampling of nearbypermanent environments thus suggesting thatthe frequency of this alternative developmentalpathway is very low in this species

In conclusion southern Iberian newts seemto maintain the capacity to exhibit alternativedevelopmental pathways under different kindsof environmental conditions Thus our obser-vations suggest that paedomorphosis althoughrare seems to be relatively widespread in south-ern Iberia than often thought and deserves moreattention to explain its maintenance

Acknowledgements The authors wish to thank AHidalgo-Pontiveros and L Pedrajas for their help duringfield trips A Conejo for the picture of L boscai larvae andJ Leonard for the useful suggestions and linguistic revisionAnimals transported to the laboratory were collected withthe authorisation of the ldquoConsejeriacutea de Medio Ambiente dela Junta de Andaluciacuteardquo

References

Alberch P Gonzaacutelez D (1973) Notas sobre la distribu-cioacuten biotopo morfologiacutea y biometriacutea de Pleurodeleswaltl Michahelles en el NE de la Peniacutensula Ibeacuterica (Am-phibia Salamandridae) Misc Zool 3 71-82

Alvarez J Salvador A Arguello JA (1988) Desarrollolarvario del gallipato (Pleurodeles waltl) en una charcatemporal del noroeste Ibeacuterico (Amphibia Salamandri-dae) Ecologiacutea 2 293-301

Short Notes 575

Arribas O (2008) Neotenia y longitud excepcional enMesotriton alpestris de Fuentes Carrionas (Palencia)Bol Asoc Herpetol Esp 19 23-24

Bedriaga J von (1896) Die lurchfauna Europa II UrodelaSchwanzlurche B Soc Imp Nat Moscou 10 38-705

Bogaerts S van Uchelen E (2003) Fund einer riesenlarvedes rippenmolches Pleurodeles waltl Michaelles 1830in der provinz Huelva Spanien Sauria 25 13-15

Campeny R Montori A Llorente GA (1986) Nuevosdatos sobre la permanencia de caracteres larvarios enindividuos adultos de una poblacioacuten de tritoacuten pirenaico(Euproctus asper) en el valle de Aran Dontildeana ActaVertebrata 13 170-173

Collins JP Zerba KE Sredl MJ (1993) Shaping in-traspecific variation development ecology and the evo-lution of morphology and life history variation in tigersalamanders Genetica 89 167-183

Denoeumll M (2003) How do paedomorphic newts cope withlake drying Ecography 26 405-410

Denoeumll M (2007) Priority areas of intraspecific diversityLarzac a global hotspot for facultative paedomorphosisin amphibians Anim Conserv 10 110-116

Denoeumll M Joly P (2000) Neoteny and progenesis as twoheterochronic processes involved in paedomorphosis inTriturus alpestris (Amphibia Caudata) Proc R SocLond B Biol Sci 267 1481-1485

Denoeumll M Duguet R Dzukic G Mazzotti S (2001)Biogeography and ecology of paedomorphosis in Trit-urus alpestris (Amphibia Caudata) J Biogeogr 281271-1280

Denoeumll M Joly P Whiteman HH (2005) Evolutionaryecology of facultative paedomorphosis in newts andsalamanders Biol Rev 80 663-671

Denoeumll M Ficetola GF Cirovic R Radovic D DžukicG Kalezic ML Vukove TD (2009) A multi-scaleapproach to facultative paedomorphosis of Europeannewts (Salamandridae) in the Montenegrin karst Distri-bution pattern environmental variables and conserva-tion Biol Conserv 142 509-517

Kalezic ML Cvetkovic D Djorovic A Dzukic G(1996) Alternative life-history pathways paedomor-phosis and adult fitness in European newts (Triturus vul-garis and T alpestris) J Zool Syst Evol Res 34 1-7

Kaya U Sayım F Baskale E Ccedilevik IE (2008) Paedo-morphosis in the banded newt Triturus vittatus (Jenyns1835) Belg J Zool 138 196-197

Reques R (2007) Tritoacuten pigmeo ndash Triturus pygmaeus InEnciclopedia Virtual de los Vertebrados Espantildeoles Car-rascal LM Salvador A Eds Madrid Museo Nacionalde Ciencias Naturales

Salvador A Garciacutea-Pariacutes M (2001) Anfibios EspantildeolesTalavera de la Reina Canseco Eds

Sindaco R Doria G Razzetti E Bernini F (2006) Atlasof Italian Amphibians and Reptiles Firenze EdizioniPolistampa

Wells KD (2007) The Ecology and Behaviour of Am-phibians Chicago The University of Chicago Press

Received January 14 2010 Accepted May 23 2010

Short Notes 573

Figure 1 (A) Pleurodeles waltl paedomorph male from location 1 Note the adult colouration and the absence of dorsalcrest (larval trait) (B) Triturus pygmaeus paedomorph male from location 3 Note the adult colouration and the swollencloaca (white arrow) (C) Lissotriton boscai paedomorph male from location 4 Note the adult colouration and the swollencloaca (white arrow)

574 Short Notes

A Lissotriton boscai paedomorph male wascaptured in location 4 on September 8th 2004(SVL = 306 mm TL = 636 mm) whichexhibited a mosaic of juvenile and male adulttraits Dorsal coloration was brownish withsome black spots along the tail and body sidesBelly was yellowish with a swollen roundedcloaca with a long obvious opening Addition-ally it exhibited a small tail crest and a tiny fila-ment of around 2-3 mm at the end of the tail (fig1C) The paedomorph was maintained in the laband on October 10th 2004 courtship activity wasobserved and voluntarily repeated for severaldays The newt was kept during three monthsin the lab until it was released Courtship be-haviour was repeatedly observed and no signsof metamorphosis were evidenced to that dateNo L boscai larvae were found at this later datesuggesting that remaining larvae resumed meta-morphosis during late spring and summer Thislocality was periodically sampled since 2004but no other paedomorph has been recorded todate

This report describes the occurrence of pae-domorphosis in the three newt species occurringin southern Iberia Paedomorphosis is describedfor the first time in P waltl and L boscaisince previously both species only had recordsfor non-paedomorphs big size larvae (Bedriaga1896 Alberch and Gonzaacutelez 1973 AlvarezSalvador and Arguello 1988 Bogaerts and vanUchelen 2003 O Arribas personal observa-tion) and the second record of paedomorphosisin T pygmaeus (see Reques 2007)

P waltl paedomorphs were found in man-made permanent aquatic habitats with no pres-ence of predatory fishes (Collins Zerba andSredl 1993) although intraspecific cannibal-ism in P waltl has been observed at location1 and it seems likely at location 2 In gen-eral paedomorphs of P waltl at location 1and T pygmaeus at location 3 coexisted in avery low frequency with metamorphic individu-als However P waltl population at location 2which inhabits a steep-sided and narrow wellthat rarely oscillates in its water level was com-

prised of only paedomorphs No metamorphicindividuals were found during two samplingsthus suggesting that it may be a completely pae-domorphic population Interestingly a P waltlmetamorphic population occupies a wider andbigger nearby well less than 200 m away Tpygmaeus paedomorphs were also observed ina permanent natural source however the pae-domorphic male of L boscai was found in apuddle within a temporary creek which gener-ally desiccates each summer This sexually ma-ture individual presumably had a maximum ageof one-two years since the puddle had lastedapproximately two years without drying Thusthe specimen could have attained its large sizeand maturity during that time However no ev-idence of paedomorphic newts has been foundto date despite intensive sampling of nearbypermanent environments thus suggesting thatthe frequency of this alternative developmentalpathway is very low in this species

In conclusion southern Iberian newts seemto maintain the capacity to exhibit alternativedevelopmental pathways under different kindsof environmental conditions Thus our obser-vations suggest that paedomorphosis althoughrare seems to be relatively widespread in south-ern Iberia than often thought and deserves moreattention to explain its maintenance

Acknowledgements The authors wish to thank AHidalgo-Pontiveros and L Pedrajas for their help duringfield trips A Conejo for the picture of L boscai larvae andJ Leonard for the useful suggestions and linguistic revisionAnimals transported to the laboratory were collected withthe authorisation of the ldquoConsejeriacutea de Medio Ambiente dela Junta de Andaluciacuteardquo

References

Alberch P Gonzaacutelez D (1973) Notas sobre la distribu-cioacuten biotopo morfologiacutea y biometriacutea de Pleurodeleswaltl Michahelles en el NE de la Peniacutensula Ibeacuterica (Am-phibia Salamandridae) Misc Zool 3 71-82

Alvarez J Salvador A Arguello JA (1988) Desarrollolarvario del gallipato (Pleurodeles waltl) en una charcatemporal del noroeste Ibeacuterico (Amphibia Salamandri-dae) Ecologiacutea 2 293-301

Short Notes 575

Arribas O (2008) Neotenia y longitud excepcional enMesotriton alpestris de Fuentes Carrionas (Palencia)Bol Asoc Herpetol Esp 19 23-24

Bedriaga J von (1896) Die lurchfauna Europa II UrodelaSchwanzlurche B Soc Imp Nat Moscou 10 38-705

Bogaerts S van Uchelen E (2003) Fund einer riesenlarvedes rippenmolches Pleurodeles waltl Michaelles 1830in der provinz Huelva Spanien Sauria 25 13-15

Campeny R Montori A Llorente GA (1986) Nuevosdatos sobre la permanencia de caracteres larvarios enindividuos adultos de una poblacioacuten de tritoacuten pirenaico(Euproctus asper) en el valle de Aran Dontildeana ActaVertebrata 13 170-173

Collins JP Zerba KE Sredl MJ (1993) Shaping in-traspecific variation development ecology and the evo-lution of morphology and life history variation in tigersalamanders Genetica 89 167-183

Denoeumll M (2003) How do paedomorphic newts cope withlake drying Ecography 26 405-410

Denoeumll M (2007) Priority areas of intraspecific diversityLarzac a global hotspot for facultative paedomorphosisin amphibians Anim Conserv 10 110-116

Denoeumll M Joly P (2000) Neoteny and progenesis as twoheterochronic processes involved in paedomorphosis inTriturus alpestris (Amphibia Caudata) Proc R SocLond B Biol Sci 267 1481-1485

Denoeumll M Duguet R Dzukic G Mazzotti S (2001)Biogeography and ecology of paedomorphosis in Trit-urus alpestris (Amphibia Caudata) J Biogeogr 281271-1280

Denoeumll M Joly P Whiteman HH (2005) Evolutionaryecology of facultative paedomorphosis in newts andsalamanders Biol Rev 80 663-671

Denoeumll M Ficetola GF Cirovic R Radovic D DžukicG Kalezic ML Vukove TD (2009) A multi-scaleapproach to facultative paedomorphosis of Europeannewts (Salamandridae) in the Montenegrin karst Distri-bution pattern environmental variables and conserva-tion Biol Conserv 142 509-517

Kalezic ML Cvetkovic D Djorovic A Dzukic G(1996) Alternative life-history pathways paedomor-phosis and adult fitness in European newts (Triturus vul-garis and T alpestris) J Zool Syst Evol Res 34 1-7

Kaya U Sayım F Baskale E Ccedilevik IE (2008) Paedo-morphosis in the banded newt Triturus vittatus (Jenyns1835) Belg J Zool 138 196-197

Reques R (2007) Tritoacuten pigmeo ndash Triturus pygmaeus InEnciclopedia Virtual de los Vertebrados Espantildeoles Car-rascal LM Salvador A Eds Madrid Museo Nacionalde Ciencias Naturales

Salvador A Garciacutea-Pariacutes M (2001) Anfibios EspantildeolesTalavera de la Reina Canseco Eds

Sindaco R Doria G Razzetti E Bernini F (2006) Atlasof Italian Amphibians and Reptiles Firenze EdizioniPolistampa

Wells KD (2007) The Ecology and Behaviour of Am-phibians Chicago The University of Chicago Press

Received January 14 2010 Accepted May 23 2010

574 Short Notes

A Lissotriton boscai paedomorph male wascaptured in location 4 on September 8th 2004(SVL = 306 mm TL = 636 mm) whichexhibited a mosaic of juvenile and male adulttraits Dorsal coloration was brownish withsome black spots along the tail and body sidesBelly was yellowish with a swollen roundedcloaca with a long obvious opening Addition-ally it exhibited a small tail crest and a tiny fila-ment of around 2-3 mm at the end of the tail (fig1C) The paedomorph was maintained in the laband on October 10th 2004 courtship activity wasobserved and voluntarily repeated for severaldays The newt was kept during three monthsin the lab until it was released Courtship be-haviour was repeatedly observed and no signsof metamorphosis were evidenced to that dateNo L boscai larvae were found at this later datesuggesting that remaining larvae resumed meta-morphosis during late spring and summer Thislocality was periodically sampled since 2004but no other paedomorph has been recorded todate

This report describes the occurrence of pae-domorphosis in the three newt species occurringin southern Iberia Paedomorphosis is describedfor the first time in P waltl and L boscaisince previously both species only had recordsfor non-paedomorphs big size larvae (Bedriaga1896 Alberch and Gonzaacutelez 1973 AlvarezSalvador and Arguello 1988 Bogaerts and vanUchelen 2003 O Arribas personal observa-tion) and the second record of paedomorphosisin T pygmaeus (see Reques 2007)

P waltl paedomorphs were found in man-made permanent aquatic habitats with no pres-ence of predatory fishes (Collins Zerba andSredl 1993) although intraspecific cannibal-ism in P waltl has been observed at location1 and it seems likely at location 2 In gen-eral paedomorphs of P waltl at location 1and T pygmaeus at location 3 coexisted in avery low frequency with metamorphic individu-als However P waltl population at location 2which inhabits a steep-sided and narrow wellthat rarely oscillates in its water level was com-

prised of only paedomorphs No metamorphicindividuals were found during two samplingsthus suggesting that it may be a completely pae-domorphic population Interestingly a P waltlmetamorphic population occupies a wider andbigger nearby well less than 200 m away Tpygmaeus paedomorphs were also observed ina permanent natural source however the pae-domorphic male of L boscai was found in apuddle within a temporary creek which gener-ally desiccates each summer This sexually ma-ture individual presumably had a maximum ageof one-two years since the puddle had lastedapproximately two years without drying Thusthe specimen could have attained its large sizeand maturity during that time However no ev-idence of paedomorphic newts has been foundto date despite intensive sampling of nearbypermanent environments thus suggesting thatthe frequency of this alternative developmentalpathway is very low in this species

In conclusion southern Iberian newts seemto maintain the capacity to exhibit alternativedevelopmental pathways under different kindsof environmental conditions Thus our obser-vations suggest that paedomorphosis althoughrare seems to be relatively widespread in south-ern Iberia than often thought and deserves moreattention to explain its maintenance

Acknowledgements The authors wish to thank AHidalgo-Pontiveros and L Pedrajas for their help duringfield trips A Conejo for the picture of L boscai larvae andJ Leonard for the useful suggestions and linguistic revisionAnimals transported to the laboratory were collected withthe authorisation of the ldquoConsejeriacutea de Medio Ambiente dela Junta de Andaluciacuteardquo

References

Alberch P Gonzaacutelez D (1973) Notas sobre la distribu-cioacuten biotopo morfologiacutea y biometriacutea de Pleurodeleswaltl Michahelles en el NE de la Peniacutensula Ibeacuterica (Am-phibia Salamandridae) Misc Zool 3 71-82

Alvarez J Salvador A Arguello JA (1988) Desarrollolarvario del gallipato (Pleurodeles waltl) en una charcatemporal del noroeste Ibeacuterico (Amphibia Salamandri-dae) Ecologiacutea 2 293-301

Short Notes 575

Arribas O (2008) Neotenia y longitud excepcional enMesotriton alpestris de Fuentes Carrionas (Palencia)Bol Asoc Herpetol Esp 19 23-24

Bedriaga J von (1896) Die lurchfauna Europa II UrodelaSchwanzlurche B Soc Imp Nat Moscou 10 38-705

Bogaerts S van Uchelen E (2003) Fund einer riesenlarvedes rippenmolches Pleurodeles waltl Michaelles 1830in der provinz Huelva Spanien Sauria 25 13-15

Campeny R Montori A Llorente GA (1986) Nuevosdatos sobre la permanencia de caracteres larvarios enindividuos adultos de una poblacioacuten de tritoacuten pirenaico(Euproctus asper) en el valle de Aran Dontildeana ActaVertebrata 13 170-173

Collins JP Zerba KE Sredl MJ (1993) Shaping in-traspecific variation development ecology and the evo-lution of morphology and life history variation in tigersalamanders Genetica 89 167-183

Denoeumll M (2003) How do paedomorphic newts cope withlake drying Ecography 26 405-410

Denoeumll M (2007) Priority areas of intraspecific diversityLarzac a global hotspot for facultative paedomorphosisin amphibians Anim Conserv 10 110-116

Denoeumll M Joly P (2000) Neoteny and progenesis as twoheterochronic processes involved in paedomorphosis inTriturus alpestris (Amphibia Caudata) Proc R SocLond B Biol Sci 267 1481-1485

Denoeumll M Duguet R Dzukic G Mazzotti S (2001)Biogeography and ecology of paedomorphosis in Trit-urus alpestris (Amphibia Caudata) J Biogeogr 281271-1280

Denoeumll M Joly P Whiteman HH (2005) Evolutionaryecology of facultative paedomorphosis in newts andsalamanders Biol Rev 80 663-671

Denoeumll M Ficetola GF Cirovic R Radovic D DžukicG Kalezic ML Vukove TD (2009) A multi-scaleapproach to facultative paedomorphosis of Europeannewts (Salamandridae) in the Montenegrin karst Distri-bution pattern environmental variables and conserva-tion Biol Conserv 142 509-517

Kalezic ML Cvetkovic D Djorovic A Dzukic G(1996) Alternative life-history pathways paedomor-phosis and adult fitness in European newts (Triturus vul-garis and T alpestris) J Zool Syst Evol Res 34 1-7

Kaya U Sayım F Baskale E Ccedilevik IE (2008) Paedo-morphosis in the banded newt Triturus vittatus (Jenyns1835) Belg J Zool 138 196-197

Reques R (2007) Tritoacuten pigmeo ndash Triturus pygmaeus InEnciclopedia Virtual de los Vertebrados Espantildeoles Car-rascal LM Salvador A Eds Madrid Museo Nacionalde Ciencias Naturales

Salvador A Garciacutea-Pariacutes M (2001) Anfibios EspantildeolesTalavera de la Reina Canseco Eds

Sindaco R Doria G Razzetti E Bernini F (2006) Atlasof Italian Amphibians and Reptiles Firenze EdizioniPolistampa

Wells KD (2007) The Ecology and Behaviour of Am-phibians Chicago The University of Chicago Press

Received January 14 2010 Accepted May 23 2010

Short Notes 575

Arribas O (2008) Neotenia y longitud excepcional enMesotriton alpestris de Fuentes Carrionas (Palencia)Bol Asoc Herpetol Esp 19 23-24

Bedriaga J von (1896) Die lurchfauna Europa II UrodelaSchwanzlurche B Soc Imp Nat Moscou 10 38-705

Bogaerts S van Uchelen E (2003) Fund einer riesenlarvedes rippenmolches Pleurodeles waltl Michaelles 1830in der provinz Huelva Spanien Sauria 25 13-15

Campeny R Montori A Llorente GA (1986) Nuevosdatos sobre la permanencia de caracteres larvarios enindividuos adultos de una poblacioacuten de tritoacuten pirenaico(Euproctus asper) en el valle de Aran Dontildeana ActaVertebrata 13 170-173

Collins JP Zerba KE Sredl MJ (1993) Shaping in-traspecific variation development ecology and the evo-lution of morphology and life history variation in tigersalamanders Genetica 89 167-183

Denoeumll M (2003) How do paedomorphic newts cope withlake drying Ecography 26 405-410

Denoeumll M (2007) Priority areas of intraspecific diversityLarzac a global hotspot for facultative paedomorphosisin amphibians Anim Conserv 10 110-116

Denoeumll M Joly P (2000) Neoteny and progenesis as twoheterochronic processes involved in paedomorphosis inTriturus alpestris (Amphibia Caudata) Proc R SocLond B Biol Sci 267 1481-1485

Denoeumll M Duguet R Dzukic G Mazzotti S (2001)Biogeography and ecology of paedomorphosis in Trit-urus alpestris (Amphibia Caudata) J Biogeogr 281271-1280

Denoeumll M Joly P Whiteman HH (2005) Evolutionaryecology of facultative paedomorphosis in newts andsalamanders Biol Rev 80 663-671

Denoeumll M Ficetola GF Cirovic R Radovic D DžukicG Kalezic ML Vukove TD (2009) A multi-scaleapproach to facultative paedomorphosis of Europeannewts (Salamandridae) in the Montenegrin karst Distri-bution pattern environmental variables and conserva-tion Biol Conserv 142 509-517

Kalezic ML Cvetkovic D Djorovic A Dzukic G(1996) Alternative life-history pathways paedomor-phosis and adult fitness in European newts (Triturus vul-garis and T alpestris) J Zool Syst Evol Res 34 1-7

Kaya U Sayım F Baskale E Ccedilevik IE (2008) Paedo-morphosis in the banded newt Triturus vittatus (Jenyns1835) Belg J Zool 138 196-197

Reques R (2007) Tritoacuten pigmeo ndash Triturus pygmaeus InEnciclopedia Virtual de los Vertebrados Espantildeoles Car-rascal LM Salvador A Eds Madrid Museo Nacionalde Ciencias Naturales

Salvador A Garciacutea-Pariacutes M (2001) Anfibios EspantildeolesTalavera de la Reina Canseco Eds

Sindaco R Doria G Razzetti E Bernini F (2006) Atlasof Italian Amphibians and Reptiles Firenze EdizioniPolistampa

Wells KD (2007) The Ecology and Behaviour of Am-phibians Chicago The University of Chicago Press

Received January 14 2010 Accepted May 23 2010