Crypic Species Complexes Widespreadspecies Leptodactylus Mormaratus Group

7/31/2019 Crypic Species Complexes Widespreadspecies Leptodactylus Mormaratus Group

1/15

This article was downloaded by: [SENESCYT ]On: 16 October 2012, At: 12:03Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House37-41 Mortimer Street, London W1T 3JH, UK

Systematics and BiodiversityPubl icat i on detai ls , inc luding inst ruct i ons for authors and subscript ion inform at ion:h t t p : / / www. tand fonl ine. com/ lo i / t sab20

Crypt ic species complexes, widespread speciesand conservat ion: lessons from Amazonian f rogsof the Leptodactylus marmoratus group (Anura:Leptodactylidae)Ariadne Angulo

a& Javier Icochea

b

aDepart ament o de Herpet ologa, Museo de Hist oria Natur al de San Marcos, Apart ado,

140434, Lim a 14, Perub

Calle Ari ca 371 dpto U-2, Lim a 18, Peru

Version of recor d f irst p ubli shed: 15 Sep 2010.

To cite this article: Ariadne Angulo & Javier Icochea (2010): Crypti c species complexes, wi despread species andconservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae), Systematicsand Biodiversity, 8:3, 357-370

To link to this article: ht t p : / / dx .doi .org/ 10.1080/ 14772000.2010.507264

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.
http://www.tandfonline.com/page/terms-and-conditionshttp://www.tandfonline.com/page/terms-and-conditionshttp://dx.doi.org/10.1080/14772000.2010.507264http://www.tandfonline.com/loi/tsab20


2/15

Systematics and Biodiversity (2010), 8(3): 357370

Research Article

Cryptic species complexes, widespread species and conservation: lessons

from Amazonian frogs of the Leptodactylus marmoratus group (Anura:Leptodactylidae)

ARIADNE ANGULO1 & JAVIER ICOCHEA2

1Departamento de Her petologa, Museo de Historia Natural de San Marcos, Apartado 140434, Lima 14, Peru2Calle Arica 371 dpto U-2, Lima 18, Peru

(Received 17 September 2009; revised 10 May 2010; accepted 30 June 2010)

Morphologically cryptic species act as a wild card when it comes to biodiversity assessments and conservation, with thecapacity to dramatically alter our understanding of the biological landscape at the taxonomic, ecological, biogeographic,evolutionary, and conservation levels. We discuss the potential effects that cryptic species may have on biodiversityassessments and conservation, as well as some of the current issues involving the treatment of cryptic species both attaxonomic and conservation levels. In addition, using a combination of advertisement call and morphological data, wedescribe a new species of the Leptodactylus marmoratus group from the upper Amazon basin, and we assess how crypticspecies can affect conservation assessments of species in the Leptodactylus marmoratus group by examining how recentfindings affect our understanding of the distribution of what is assumed to be a widespread Amazonian species,Leptodactylus andreae.

Key words: Adenomera, advertisement call, anurans, conservation, cryptic species complexes, IUCN Red List,Leptodactylus marmoratus group, taxonomy, widespread species

IntroductionWith nearly a third of all nominal amphibian species con-

sidered to be globally threatened (Stuart et al., 2004),

amphibian declines and extinctions are now a recognized

phenomenon at the forefront of the biodiversity crisis. A

critical aspect of engaging in effective conservation ac-

tion, however, depends on our ability to correctly identify

species as such, given that different characteristics and life

histories may lead to differing conservation needs among

species. Morphologically cryptic species (two or more dis-

tinct species that are classified as a single species) act as

a wild card when it comes to biodiversity assessments and

conservation (Bickford et al., 2007), with the capacity to

dramatically alter our perceptionof the biological landscapeat the taxonomic, ecological, biogeographic, evolutionary

and conservation levels.

Cryptic species are a familiar part of the amphibian land-

scape as any amphibian field researcher will attest, but they

are by no means exclusive to this class. There are numerous

Correspondence to: Ariadne Angulo. E-mail: [email protected]

examples of cryptic species reported for a very broad range

of living beings [e.g. birds (Cuervo et al., 2005), fishes(Colborn et al., 2001), fungi (Pringle et al., 2005), insects

(Copren et al., 2005; Paredes-Esquivel et al., 2009), mol-

luscs (Calvo et al., 2009) and reptiles (Torres-Perez et al.,

2009), and see also Pfenninger & Schwenk (2007) and

Trontelj & Fiser (2009) for meta-analyses of cryptic species

reports across major metazoan taxa], which suggests not

only that this is a widespread phenomenon across the taxo-

nomic board, but also that wemay be vastly underestimating

the planets species richness and current biodiversity loss.

Candidates for cryptic species complexes are often con-

cealed within widespread species. Therefore, what appears

to be a single, nominal widespread species may in fact be

comprised of morphologically similar but geographically

restricted species (Funk et al., 2008). Widespread species

do, in fact, occur; even in organisms traditionally consid-

ered to be of relatively low vagility, such as amphibians

(see e.g. Goweret al., 2007); however, it is not known what

proportion of cases flagged as widespread species are truly

genuine instances of widespread taxa, and what proportion

comprises species complexes.

ISSN 1477-2000 print / 1478-0933 onlineC 2010 The Natural History Museum

DOI: 10.1080/14772000.2010.507264


3/15

358 A. Angulo and J. Icochea

A growing use of alternative (non-morphological) and

complementary suites of features, such as genetic and/or

call data, are useful in the identification of cryptic species

in amphibians (e.g. Angulo et al., 2003; Camargo et al.,

2006; Ron et al., 2006; Fouquet et al., 2007; Padial et al.,

2008). Many members of the Leptodactylus marmoratus

group (formerly assigned to the genus Adenomera) consti-

tute good candidates for harbouring morphologically cryp-

tic species complexes. This is largely because (1) there

is considerable morphological variation within and among

populations (De la Riva, 1996; Kwet & Angulo, 2002;

Kwet, 2007; Ponssa & Heyer, 2007; Kwet et al., 2009),

(2) there is an overall similarity among several species, and

(3) many of the nominal species are considered to occur

over vast tracts of land (e.g. the Amazon basin, Atlantic

rainforests of Brazil and cerrado/chaco environments). In

the specific case of the Amazon basin, for example, two

widespread species of the L. marmoratus group have been

traditionally considered to occur in sympatry: Leptodacty-

lus andreae Muller, 1923, andLeptodactylus hylaedactylus(Cope, 1868), with one species thought to occur in forests

[L. andreae] and the other one occurring in open environ-

ments [L. hylaedactylus] (Heyer, 1984).

Recent studies on the L. marmoratus group that made

use of different suites of features (acoustic signals, life

history traits) have, in fact, unearthed cryptic species for

geographical regions that were considered to harbour one or

two widespread species (Kwet & Angulo, 2002; Angulo &

Icochea, 2003; Angulo et al., 2003; Kokubum & Giaretta,

2005; Almeida & Angulo, 2006; Kwet, 2007; Angulo &

Reichle, 2008).

In the course of several biological inventory field expedi-

tions conducted in a natural gas prospecting area near RioCamisea and Rio Urubamba, region of Cusco, upper Ama-

zon basin of Peru, a previously unknown population of the

Leptodactylus marmoratus group was observed, recorded

and collected. Morphological differences with other mem-

bers of theL. marmoratus group suggested that this popula-

tion merited further attention (Icochea et al., 2001). Exam-

ination of advertisement call features, voucher specimens

and comparisons with other species, in addition to infor-

mation in the primary literature, reveal that this population

is a new taxon in the Leptodactylus marmoratus group. We

describe the new species in the present paper.

In addition, we assess how recent findings affect our un-

derstanding of the distribution of what is assumed to bea widespread Amazonian species, Leptodactylus andreae,

and how cryptic species can affect conservation assess-

ments of species in the Leptodactylus marmoratus group

based on the IUCN Red List Categories and Criteria (IUCN,

2001).

Cryptic species complexes and their

biodiversity impacts

The phenomenon of undetected cryptic species richness is

likely to be more of a norm rather than an exception with

regards to amphibians, as numerous cases of such instances

have been reported throughout this taxonomic class (e.g.

Heyeret al., 1996; Ron et al., 2006, and references within;

Stuart et al., 2006; Elmeret al., 2007; Fouquet et al. 2007;

Sumida et al., 2007; Fu & Zeng, 2008; Inger et al., 2009;

Padial & De la Riva, 2009; Vieites et al., 2009). The im-

pacts and implications of this biodiversity in hiding can be

considerable, affecting everything from estimates of total

number of species, biogeography, evolution, etc. to eco-

nomic prospecting of this biodiversity, conservation, and,

of course, extinction rates. Two dramatic examples of the

magnitude of this phenomenon are illustrated by Fouquet

et al. (2007), who begin their study with 60 nominal species

but estimate the existence of 129 species upon concluding

the study, and by Vieites et al. (2009), who begin their

study with 244 described species but upon conclusion of

the study estimate that the number of species should be

somewhere between 373 and 465. In both these studies, the

estimated total number of species comprises roughly a two-

fold increase from the original sampled number of nominalspecies.

Morphologically cryptic species complexes lurking un-

der the guise of a presumed widespread species may have

the potential to significantly change our understanding of

biodiversity as a whole. If the numbers of known or sus-

pected cryptic amphibian species are anything to go by,

the answers to questions such as why and how these forms

evolved, how did they get to be where they are, how they

differ among themselves, and whether or not they require

conservation efforts may be a long way coming in view

of the current global economic climate, limited amount of

resources and available expertise that can be dedicated to

address these questions at a global level. This is of partic-ular concern in view of the current amphibian decline and

extinction crisis.

In their study of distribution patterns of amphibians from

the Kakamega Forest in Kenya, Schick et al. (2005) as-

sess how our understanding of biogeographic patterns can

be affected by cryptic species concealed under nominal

widespread species, where particular distribution patterns

may be more common than initially thought, and their

unveiling may better support particular biogeographic hy-

potheses. From a conservation perspective, Angulo (2002)

provides some hypothetical examples in which cryptic

species hiding under the guise of widespread nominal

species can affect biodiversity assessments. Expanding onthis argument, we provide a modified version of the illus-

trated example in Angulo (2002) and an additional exam-

ple based on habitat use (Figs 1 and 2). The first example

(Fig. 1) depicts a scenario where multiple populations of

a presumed widespread species (species X) are assessed

over a given geographical area. If only a very limited num-

ber of these populations show some evidence of decline,

the species as a whole may still be assessed as being not

threatened because most of its populations may be consid-

ered as being stable. However, if the populations that are in


4/15

Cryptic species, conservation and new Leptodactylus 359

Fig. 1. One possible scenario of the way in which cryptic speciescomplexes can affect conservation assessments: Where severalpopulations of a presumed widespread species (species X) areassessed and declines are detected in only a limited number ofpopulations, which pertain to cryptic species Y (modified fromAngulo, 2002).

decline pertain to a cryptic species with a more restricted

geographicrange (species Y), the cryptic species conserva-

tion needs may go unnoticed. The second example (Fig. 2)depicts an apparently single population of a widespread

species (species X) occupying a variety of different habi-

tats. However, it is possible that cryptic species Y may be

restricted to a specific habitat type within this range of habi-

tats, affecting our understanding of habitat associations and

needs for both the widespread and the cryptic species.

There are other potential scenarios involving the IUCN

Red List Categories and Criteria. One such scenario in-

volves a nominal species already assessed as threatened,

but which could comprise more than one morphologically

cryptic species that, if recognized as distinct, would each

qualify for a higher threat category than that assigned to

the original nominal species. An example of this would bean instance where a nominal species may be assessed as

Endangered (EN) or Vulnerable (VU) but is later found to

comprise three separate cryptic species, all of which meet

the Criteria for Critically Endangered (CR).

Alternatively, a nominal species may be assessed as

threatened, but upon review it might be that not all of the

composite species meet the IUCN Red List Criteria, i.e.

Fig. 2. A second scenario of how cryptic species complexes mayaffect assessments: where a single population of a widespreadspecies (species X) appears to occupy several different habitats,but cryptic species Y is restricted to a specific habitat type withinits range.

threats and/or declines may only be occurring in part of

the nominal species range, and not affecting all popula-

tions equally. The nominal threatened species may there-

fore consist of both threatened and non-threatened cryptic

species.

While it is clear that cryptic species complexes area com-

mon phenomenon and that they have the potential to affect

many aspects of our interpretations of the natural world,

one major issue is that until they are formally recognized as

full species it will be difficult to allocate resources for their

conservation, should they need it.

Cryptic species, taxonomy and

conservation

With regards to amphibian taxonomy, the IUCN Red List of

Threatened Species generally follows Amphibian Species

of the World (Frost, 2009) as a taxonomic standard. The

IUCN Red List encourages that, where there are instances

of known species complexes, details of these undescribedcryptic species, especially pertaining to distribution, habi-

tat and ecology, threats and conservation status, as well

as details of the person providing the information, be pro-

vided under the account of the nominal species to which

the cryptic species have been associated. This is a compro-

mise, but allows the nominal species to be split quickly in

the Red List upon publication of the cryptic species, with

all of the supporting data in place already. However, the

conservation assessment is ultimately made on the nomi-

nal species. The IUCN Red List does not normally assess

undescribed species separately (it only does so under ex-

ceptional circumstances and a number of strict conditions

must be met for this to happen) (IUCN Standards and Pe-titions Working Group, 2008), and there are valid reasons

for this, such as the nomenclatural and practical issues that

would arise from such a practice (e.g. one researchers Lep-

todactylus sp. 1 may be another researchers Leptodactylus

sp. Z and there would be no published source to go to so as

to ensure that they are the same species; the ever-increasing

number of undescribed species; the proliferation of tem-

porary designations and their management within the Red

Lists database; and the further merging and splitting of

undescribed taxa), and the chaos that would ensue from

implementing this approach across the taxonomic board

within the Red List. In light of this scenario, one alternative

is to encourage resolution of these species complexes andpublication of their component cryptic species. However,

in many instances this is no simple matter, either. Often

times taxonomists do not have easy or direct access to type

material to compare against their own samples, the taxo-

nomic history of such cryptic groups can be quite complex

and the provenance of some nominal species can be ob-

scure at best, and researchers do not have the time and/or

are not rewarded for publishing species descriptions, as

these are not as valued (and therefore not encouraged) as


5/15


publications in more trendy and modern approaches to bio-

diversity issues.

Unfortunately, an additional, recent issue stemming from

a combination of some of these factors is that studies using

phylogenetic approaches with molecular and/or other char-

acters focusing on addressing a specific question are of-

ten built around that question, with secondary (taxonomic)

findings being relegated to a second plane. In many in-

stances these studies identify populations that pertain to

crypticspecies, butbecause their descriptionsare notwithin

the scope of the study and/or the numbers of species in-

volved can be potentially high, these taxa often go unde-

scribed (and the senior author will be the first one to admit

to having done this in the past, e.g. Angulo et al., 2003;

Angulo, 2004). Published results from some recent molecu-

lar studies have often led to splitting of the original nominal

taxa, better circumscribing the name carriers, but leaving

all other cryptic species in taxonomic and therefore con-

servation limbos.

The combination of theissues outlined above makes mor-phologically cryptic species the castaway species of the

taxonomic and conservation realms. In many instances de-

scribing new cryptic species identified in the course of a

targeted study may not be practical or even possible; how-

ever, given the current crisis facing amphibians in particular

and biodiversity as a whole, we urge researchers to consider

describing and validating cryptic species whenever possible

within the scope of their study and within reason.

Materials and methods

Field work was conducted in the localities of Segakiato(11

4823S, 72

5251W, c. 340 m asl; Valencia & Alonso,

1998), Konkariari (11

48S, 72

52W, 300 m asl; Valencia

& Alonso, 1998), Cashiriari II (11

5151S, 72

4645W,

469 m asl; Comiskey et al., 2001) and Cashiriari III

(11

5256.693S, 72

392.132W, c. 694 m asl), in or

near Machiguenga territory, near Ro Camisea and Ro

Urubamba, District of Echarate, Province of La Con-

vencion, Region of Cusco, Peru, and in San Sebastian

(1124S, 6901W, c. 280 m asl; Alverson et al., 2000),

close to Ro Tahuamanu, Department of Pando, Bolivia.

Specimens were fixed in 10% formalin and preserved in

70% ethanol; these are deposited at the Museo de His-

toria Natural de la Universidad Nacional Mayor de SanMarcos (MHNSM/MUSM), Lima, Peru and Museo Noel

Kempff Mercado (NKA), Santa Cruz, Bolivia. Referred

specimens are deposited at MHNSM, NKA and Coleccion

Boliviana de Fauna (CBF) in La Paz, Bolivia. Other speci-

mens used for comparative purposes are deposited at: CBF;

NKA; the Academy of Natural Sciences of Philadelphia

(ANSP), United States; Museum National dHistoire Na-

turelle (MNHN), Paris, France; Royal Ontario Museum

Fig. 3. Holotype ofLeptodactylus simonstuarti sp. nov.

(ROM), Toronto, Canada; and Zoologische Staatssamm-

lung Munchen (ZSM), Munchen, Germany.

Where possible, specimens were sexed by examining for

presence of vocal slits and callus on snout. With the ex-

ception of snoutvent length (SVL), tibia length (TL) and

foot length (FL), which were measured with digital cal-

lipers, all other measurements were taken with an ocular

micrometer fitted to a dissecting microscope, as follows:

head length (HL), head width (HW), eye diameter (ED),

tympanic diameter (TYD), eyenostril distance (END), in-

terorbital distance (IOD), internarial distance (IND), fore-

arm length (FAL), hand length (HDL), thigh length (THL),

tibia length (TL), tarsus length (TSL) and foot length (FL).

Measurements were made to the nearest 0.1 mm and fol-

lowed Heyeret al. (1990).

Vocalizations were recorded using a Sony Walkman pro-

fessional WM D6C tape recorder and an AKG D 1200E mi-crophone and were later digitized at a sampling rate of 44.1

kHz and 16-bit precision. Call analysis was performed us-

ing the Macintosh-based software Signalyze (Keller, 1994),

and calls were illustrated using a combination of DADiSP

(DSP Development Corporation, 1998) and Corel Draw.

Call parameters used to describe the call are: call length,

call rate, call rise time, fundamental frequency, dominant

frequency, change in dominant frequency and other fre-

quencies. Our use of terminology follows mostly Cocroft

& Ryan (1995); we follow Ewing (1989) for fundamen-

tal frequency and Almeida & Angulo (2006) for other

frequencies.

ResultsLeptodactylus simonstuartisp. nov.

HOLOTYPE. Adult male, MHNSM 18218, collected at

Campamento Segakiato, c. 340 m asl, R o Camisea,

District of Echarate, Province of La Convencion, Region


6/15


Fig. 4. Dorsal view ofLeptodactylus simonstuarti sp. nov.

Fig. 5. Ventral view ofLeptodactylus simonstuarti sp. nov.

of Cusco, Peru, on 11 October 1997 at 18:20 h by Javier

Icochea.

PARATYPES. MHNSM 18221 collected at Campamento

Konkariari, Ro Urubamba, on 21 October 1997 at 13:30 h

by Javier Icochea; MHNSM 18220, collected at Cashiriari

II on 11 October 1998 at 12:20 h by Alfredo Portilla; and

MHNSM 18229 collected at Cashiriari III on 1 September1998 by Eliana Quispitupac.

REFERRED MATERIAL. NKA 3597 collected in San Se-

bastian, Department of Pando, Bolivia, on 11 March 2001

at 23:53 h by Ariadne Angulo, and CBF 4294, collected in

1999 by Steffen Reichle.

DIAGNOSIS. Leptodactylus simonstuarti sp. nov. can be

distinguished from other congeners by the following com-

bination of features: (1) a distinct advertisement call (see

under Comparison with other advertisement calls), (2) a

relatively large SVL (maximum SVL in males 26.2 mm;

in females 25.2 mm), (3) very dark dorsal colouration, and

(4) very dark, nearly solid stripes on undersides of arms,

running from wrist to arm insertion.Within Amazon-associated species, it can be distin-

guished from Leptodactylus heyeri (Boistel, Massary (de)

& Angulo, 2006) in lacking two distinct pairs of dorsolateral

folds and males lacking a yellow throat and belly (Boistel

et al., 2006), and from Leptodactylus lutzi (Heyer, 1975) by

having a smaller body size (SVL in L. lutzi males 30 mm)

and absence of distinct spotting on the posterior face of

the thigh (Heyer, 1975). Leptodactylus simonstuarti differs

fromLeptodactylus coca Angulo & Reichle, 2008 in having

a relatively more developed inner metacarpal tubercle, dark

dorsum, and a dark, continuous stripe running the length of

the underside of the arm, and it differs from Leptodactylus

andreae, Leptodactylus diptyx Boettger, 1885 and Lepto-

dactylus hylaedactylus by having a larger SVL (L. andreae

21 mm, L. diptyx 22 mm andL. hylaedactylus 24.6 mm; see

Angulo & Reichle, 2008 for details), dark dorsum, and very

dark stripe running along the underside of the arm from the

wrist to arm insertion.

DESCRIPTION OF HOLOTYPE. Body small but robust;

limbs relatively short. Head marginally wider than long;

dorsal outline of snout rounded; in profile snout nearly

acuminate; nostrils oriented dorsolaterally, approximately

equidistant between tip of snout and anterior corner of eye;

internarial distance >25% of head width. Tympanum dis-

tinct, nearly 60% of eye diameter; supratympanic fold welldeveloped, extending from back of eye to arm insertion;

dark, contouring outline above fold following the extent

of the fold; oval cream-coloured gland below angle of jaw

and supratympanic fold present and distinct; canthus ros-

tralis indistinct. Single, internal vocal sac; paired elongate

vocal slits present. Vomerine teeth posterior to choanae, ar-

ranged in transverse series parallel to choanae. Inner edge

of series slightly convergent to each other. Arms short,

robust; fingers slender, lacking fringes, finger lengths III


7/15


Fig. 6. Ventral view of palm of left hand of holotype of Lepto-dactylus simonstuarti sp. nov. Scale bar equals 1 mm. Note darkstripe running along arms back (white arrow).

> I = II > IV; finger tips rounded and without expan-

sions; palm of hand with two large ovoid-shaped cream-

coloured metacarpal tubercles; inner metacarpal tubercle

more elliptical in shape and slightly larger at greatest diam-

eter than outer metacarpal tubercle; conspicuous, distinct

cream-coloured rounded subarticular tubercles on under-

side of fingers, nuptial asperities absent. Hindlimbs robust,

tibia longer than thigh; toe lengths IV > III > V > II

> I; toe tips slightly flattened or not, with visible expan-sions (character states CD of Heyer, 1973); toes without

fringes; underside of toes with dark lines. Metatarsal tuber-

cles distinct; inner tarsal fold lined with scant, small white

tubercles; which are also present on tarsus and sole of foot.

Skin on dorsal surface smooth and glandular/tuberculate

with very small tubercles sparsely distributed from about

the shoulder down to thevent;thighs mostly smooth, shanks

with very small, white-tipped tubercles. Venter surface

smooth.

Fig. 7. Ventral view of sole of left foot of holotype of Leptodacty-lus simonstuarti sp. nov. Scale bar equals 1 mm.

COLOUR IN LIFE. Figure 3 shows the male holotype in

life. Dorsum a greyish dark brown, with irregular dark

markings on the lower back running from mid-dorsum to

groin. A tan-orange discontinuous dorsolateral glandular

line on each side of the body, running from behind the eye to

just anterior to the groin. Dorsal surfaces of hind limbs withirregular dark crossbars, white-tipped tubercles noticeable

on shanks. Dorsal surfaces of arms and heels an orange-

reddish colour; arms with two dark, incomplete crossbars.

Tympanum dark brown, supratympanic fold lined with a

dark stripe running from behind the tympanum to the arm

insertion and continuing irregularly from behind the arm

to the groin, running roughly parallel to the discontinu-

ous dorsolateral glandular line above. A second, marginally

lighter stripe runs roughly parallel and ventral to the first

stripe, lining the boundary with the ventral surface. A small

orange gland is located under each supratympanic fold and

anterior to the arm, between the tympanum and arm. Two

dark bars below each eye, each of them roughly diagonal toanterior and posterior angles of eye. Some white spotting

on edges of upper and lower lips. A dark, nearly continuous

stripe along the length of the underside of the arm, from

the wrist to arm insertion, with a slight break or narrowing

at the elbow level. A yellowish, mid-dorsal hairline stripe

from below the shoulders to the vent. Two dark glands flank

the cloaca on each side. Venter greyish-white.

COLOUR IN PRESERVATIVE. Dorsum dark brown, with

dark melanophore marks as described for live specimen.


8/15


Table 1. Morphometric measurements forLeptodactylus simonstuarti sp. nov. Numbers on first row are means standard deviation,numbers in parentheses are ranges. All measurements expressed in mm.

Males (N = 2) Females (N = 4)

Snoutvent length (SVL) 26.03 0.25 (25.926.2) 24.07 1.095 (23.225.2)Head length (HL) 9.52 0.45 (9.209.84) 8.61 0.27 (8.358.99)Head width (HW) 9.95 0.76 (9.4210.49) 9.42 0.17 (9.209.63)

Eye diameter (ED) 2.78 0.30 (2.573.00) 2.51 0.11 (2.352.57)Tympanum diameter (TYD) 1.71 0.0 (1.711.71) 1.71 0.17 (1.501.93)Eyenostril distance (END) 2.03 0.15 (1.932.14) 2.19 0.20 (1.932.35)Interorbital distance (IOD) 2.57 0.30 (2.352.78) 2.46 0.12 (2.352.57)Internarial distance (IND) 2.46 0.15 (2.352.57) 2.27 0.10 (2.142.35)Forearm length (FAL) 5.03 0.45 (4.715.35) 4.92 0.17 (4.715.14)Hand length (HDL) 5.35 0.0 (5.355.35) 5.24 0.12 (5.145.35)Thigh length (THL) 10.17 0.76 (9.6310.70) 10.71 0.41 (10.2711.18)Tibia length (TL) 11.16 0.56 (10.7611.56) 11.32 0.38 (10.9311.69)Tarsus length (TSL) 6.42 0.30 (6.216.63) 5.78 0.0 (5.785.78)Foot length (FL) 11.69 0.80 (11.1312.26) 11.48 0.54 (10.8612.17)

Venter white, immaculate; throat white, some mottling

along the edges of the lower lip. Fingers IIIII with short,dark lines on palm of hand.

SECONDARY SEXUAL CHARACTERS. Male holotype

and male paratype MHNSM 18220 have a projecting ridge

on snout, above upper lip, similar to L. lutzi (Kok et al.,

2007 and Fig. 8, this paper). We agree with Kok et al. that

this callus-like ridge, present in adult males, is probably

used to excavate nesting chambers. A similar ridge used for

nest construction is found in theL. fuscus group (Reading &

Jofre, 2003). It is not known if these ridges are a permanent

feature or develop only for the breeding season.

MEASUREMENTS OF HOLOTYPE (IN MM). SVL 25.9;

HL9.2; HW9.4; ED3.0; TYD 1.7; END 1.9;IOD2.8; IND

Fig. 8. Lateral view of head of holotype ofLeptodactylus simon-stuarti sp. nov. Note hardened ridge above upper lip (white arrow).

2.6; FAL 4.7; HDL 5.4; THL 10.7; TL 11.6; TSL 6.2; FL

11.1MORPHOLOGICAL VARIATION. Table 1 shows mor-

phometric variation forLeptodactylus simonstuarti sp. nov.

As for other variations, paratypes from Peru as for holo-

type with the following exceptions: MHNSM 18229 with a

slightly lighter dorsum; MHNSM 1822018221 with short,

dark spots or lines on palm of hand (fingers IIIII or IV),

MHNSM 18229 without these. MHNSM 18221 with well

developed supratympanic fold above the tympanum but

weakly marked from tympanum to arm insertion; in the

other two paratypes fold well developed from back of the

eye to the arm insertion. Male paratype with small, white-

tipped tubercles on the dorsal surface from shoulder level to

the vent, other paratypes with either isolated or nearly ab-

sent indistinct dorsal tubercles and a mostly smooth dorsal

appearance.

The Bolivian specimens, both females, as for holotype,

with the following variations: Specimen CBF 4294 without

well marked diagonal dark bars below the eye; thin mid-

dorsal light hairline stripe running from the lumbar region

down to the vent. Neither specimen with dark spots or lines

on palm of hand, and both with well developed supratym-

panic fold from the back of the eye to arm insertion. Both

with dark mottling lining the edges of the lower lip, al-

though less than in specimens from Peru. In life, specimen

NKA 3597 with very dark iris, with small and sparse yellowfreckles.

ADVERTISEMENT CALL. A calling male, holotype

MHNSM 18218, was recorded at 18:20 h on 11 October

1997 at an ambient air temperature of 27 C, beneath the

leaf litter next to a rotting log, in an old abandoned cacao

plantation with some secondary growth, in the vicinity of a

gas exploration campsite.

The advertisement call of L. simonstuarti (Fig. 9 and

Table 2 for call parameter measurements) was first de-

scribed under Adenomera Camisea I by Angulo (2004).


9/15


Fig. 9. Advertisement call ofLeptodactylus simonstuarti sp. nov. (a) Sequence of three calls, (b) one of these calls at higher resolution, (c),section of call in (b) showing detail of waveform, (d) power spectrum and (e) spectrogram of the calls in (a). Upper harmonic frequenciesnot depicted in (d) as they fall below the cutoff point of30 dB.

Compared with other species of the L. marmoratus group,

L. simonstuarti has a shorter mean call duration (65 ms)

repeated at a high call rate (c. 231 calls/min). There are

three to four pulse-like, strong amplitude modulations in the

call. The dominant frequency is the fundamental frequency

(18132035 Hz), and the call may have at least two addi-

tional harmonically related frequencies at 37074049.5 Hz

and 49566024 Hz, at a lower intensity than the


10/15


Table 2. Measurement of advertisement call parameters for theholotype ofLeptodactylus simonstuarti sp. nov. Numbers in firstline are means standard deviation while numbers inparentheses are ranges.

Recording MHNSM 18218 (male)

Number of calls 62

Temperature (

C) 27Call length (ms) 65.3 3.7 (57.171.4)Call rise time (ms) 13.6 6.8 (4.844.8)Call rate (calls/min) 231 (216246)Fundamental frequency

(Hz)-Dominantfrequency (Hz)

1962.7 43.7 (1813.22034.8)

Additional frequency 1 3892.8 86.9 (37074049.5)Additional frequency 2 5773.4 213.4 (49566023.8)Change in dominant

frequency (Hz)298 63.7 (170.9430)

Total number ofharmonics detected

3

fundamental frequency. Call frequency increases slightlyduring the call (171430 Hz).

NATURAL HISTORY. The species inhabits lowland Ama-

zonian primary and secondary terra firme forests, including

regenerating cacao plantations. Individuals can be found on

the forest and cacao plantation floors within the leaf litter,

and calling activity is initiated at dusk.

GEOGRAPHIC DISTRIBUTION. Leptodactylus simon-

stuarti is known from five localities in the Amazonian low-

lands east of the Andes: four geographically close localities

in southern Peru (300694 m) and one in northern Bolivia

(280 m) (Fig. 10). The holotype locality is separated from

the one in Bolivia by c. 407 km. The species may possibly

occur elsewhere in this region given that much of the area

in between these sites is still thought to contain suitable

habitat.

ETYMOLOGY. The new species is named after Dr Si-

mon N. Stuart, in recognition of his considerable efforts to

highlight the global amphibian crisis and to encourage am-

phibian research and conservation efforts across the world.

Species diagnosis and species concepts

Leptodactylus simonstuarti was initially thought to be a

new undescribed species on the basis of its advertisement

call and morphological differences. Subsequent compar-isons of these features among the L. marmoratus group

support this inference. Given that advertisement calls were

the primary line of evidence to suggest the biological iden-

tity of L. simonstuarti, we refer to Patersons Recognition

Species Concept (RSC) (that most inclusive population

of individual biparental organisms which share a common

fertilization system; Paterson & McEvey, 1993: 147) as

an operational species concept, while using Simpsons

(1961) Evolutionary Species Concept (ESC) [a lineage (an

ancestral-descendant sequence of populations) evolving

separately from others and with its own unitary evolu-

tionary role and tendencies] as a primary concept (for a

discussion on the use of species concepts in species descrip-

tions in the L. marmoratus group see Angulo & Reichle,

2008).

Conservation status

While there is limited information on the species popu-

lation status and geographic distribution, there are some

inferences that can be made based on the habitats and lo-

calities which it occupies. It has been found in intervened

forest macrohabitats (i.e. an old abandoned cacao planta-

tion with some secondary growth), which suggests that it

can tolerate some degree of habitat disturbance in the con-

text of a forest environment. It has also been found in five

localities, four that are geographically close and the more

distant locality in Bolivia. If there is sufficient suitable habi-

tat between the Peruvian and Bolivian localities, the new

species could also occur in between known localities.

All four Peruvian localities are within the boundaries of

the Camisea Natural Gas Projects Block 88 [see fig. 4 in

Finer et al. (2008); Block 88 corresponds to the yellow

square pointed as Camisea], which started production in

2004 and has had a reopening of another two wells over the

last two years, diverting gas via pipelines to the main plant

in Malvinas, on the Rio Urubamba. Already there have been

several pipeline ruptures, affecting both the immediate en-

vironment and local communities, posing a real, tangible

threat to local flora and fauna and indigenous communities.

Finer et al. (2008) identify pending oil and gas projects

as currently being the primary threat to Perus Camisea re-gion, among other western Amazonian areas. Neighbouring

blocks 56, 57 and 58 are all already under exploration. In

addition, there are other designated hydrocarbon blocks in

between the Peruvian and Bolivian localities (blocks 113

and 111 in Peru). The Peruvian localities are also rela-

tively close to Manu National Park, soL. simonstuarti could

also occur there, although there are currently no known

records for this Park. Given our limited data at this time, we

suggest that L. simonstuarti be preliminarily considered as

Data Deficient (DD) following IUCNs Red List Categories

and Criteria (IUCN, 2001). If future surveys fail to record

the species in between the known sites it could meet the

IUCN Criteria for a threat category; alternatively, it couldbe assessed as Least Concern if the species is found to occur

more widely and most of the populations are found to be un-

der no significant threat, or possibly Near Threatened (NT)

if intense hydrocarbon explorations expand to other blocks.

Discussion

There have been sevenadditions to theL. marmoratus group

over the last 5 years: Leptodactylus nanus (as Adenomera


11/15


Fig. 10. Map depicting the known localities (black circles) for Leptodactylus simonstuarti sp. nov. Localities Segakiato and Konkariariare very close, so they are depicted as a single circle.

nana, Kwet, 2007), Leptodactylus heyeri (as Adenomeraheyeri, Boistel et al., 2006), Leptodactylus thomei Almeida

& Angulo, 2006, Leptodactylus ajurauna Berneck, Costa

& Garcia, 2008 (Bernecket al., 2008), Leptodactylus coca

(Angulo & Reichle, 2008) Leptodactylus engelsi (as Ade-

nomera engelsi Kwet, Steiner & Zillikens, 2009) andnowL.

simonstuarti. There are currently 15 nominal species recog-

nized for the group, including L. simonstuarti as the latest,

but by no means last, addition. Other species await formal

description/resurrection (e.g. Angulo & Icochea, 2003; An-

gulo et al., 2003; Kokubum & Giaretta, 2005; Kwet, 2007),and while not yet officially tallied, it is clear that the Lepto-

dactylus marmoratus group comprises many more species

than previously thought.

Prior to assigning a new name to Leptodactylus si-

monstuarti we attempted to determine whether we could

associate an existing name to the new species [several

names are available under synonymy within Leptodactylus

hylaedactylus and Leptodactylus diptyx (Frost, 2009)].

Comparisons of type images kindly provided by W.R. Heyer


12/15


Fig. 11. Map depicting current distribution for Leptodactylus andreae (IUCN, 2009) and individual localities for recently recognizedspecies masquerading under this name. Localities are as follows: = type locality forLeptodactylus andreae; = report forL. andreae(Marquez et al., 1995) now known to pertain to L. diptyx (I. De la Riva, pers. comm.); = Tambopata Reserved Zone, Madre de Dios,Peru, where three recently recognized forest-associated cryptic species are found (Angulo et al., 2003); = localities forL. simonstuartisp. nov. (this study).

suggested that those of the lectotype of Leptodactylus

glandulosus appeared most similar to L. simonstuarti. We

were able to access seven of the 14 specimens comprising

the type series ofL. glandulosus, so it was possible to com-

pare specimens directly. Upon examination, Leptodactylus

glandulosus specimens were found to be much smaller

than any of those available for L. simonstuarti [SVL =

14.421.8 mm (n= 7)], lacked a nearly solid dark stripe on

the underside of arms, and had unexpanded, unflattened toe

tips, leading us to conclude thatL. simonstuarti is a different

species from L. glandulosus. Heyer (1973) suggested that

all of the L. glandulosus type specimens are juveniles. We


13/15


concur with this assessment for the subsample that we had

access to.

Comparison of advertisement calls

Angulo & Reichle (2008) provided data (their table 4) sum-

marizing some key acoustic parameters for members of the

Leptodactylus marmoratus group with an Amazonian dis-tribution, we refer to this table formore detailed information

on other species. The most notable difference between the

call of Leptodactylus simonstuarti and other Amazonian

calls for the group, with the exception of Adenomera cf.

andreae [Angulo & Icochea, 2003, orAdenomera Camisea

II sensu Angulo (2004)], is the dominant frequency [fun-

damental frequency in L. simonstuarti; second harmonic in

other Amazonian species (Angulo & Reichle, 2008: 70)].

The call of Adenomera cf. andreae differs from that of

L. simonstuarti in having a shorter call length (2138 vs.

5771 ms, respectively), lower call rate (3078 vs. 216246

calls/min, respectively) and lacking observable amplitude

modulation.A second key difference between the call of L. simon-

stuarti and those of other Amazonian species of the L.

marmoratus group comprises the call rate: the new species

has an extremely high call rate (216246 calls/min), com-

parable only to that of Leptodactylus hylaedactylus from

Tambopata, Peru (162252 calls/min).

Geographic patterns and their

implications for conservation

Based on acoustic information currently available, the total

species richness for the L. marmoratus group in southeast-

ern Peru would be at least six species, three times as manyspecies as the currently accepted widespread Amazonian

nominal species Leptodactylus andreae andLeptodactylus

hylaedactylus.

Most of these cryptic species are likely to have been

assigned to the forest-dwelling nominal Leptodactylus an-

dreae given that this is also the broad general habitat that

these previously undetected taxa occupy. Assuming that

recorded acoustic signals from the type locality of L. an-

dreae (Peixe-boi, Para, Brazil) may pertain to this nominal

species (Kokubum, Angulo & Kok, unpubl data), this would

permit resolution of the taxonomic status of most other

forest-dwelling Amazonian populations for whom acoustic

data are available. We use the widely distributedL. andreaeas a model species as a basis for comparison with other

morphologically cryptic species complexes in the genus

Leptodactylus.

The IUCN Red List of Threatened Species (IUCN,

2009) provides an estimate of the geographic range for

Leptodactylus andreae (Fig. 11). This nominal species

is currently considered to occur over most of the Ama-

zon Basin, encompassing nine countries (Bolivia, Brazil,

Peru, Ecuador, Colombia, Venezuela, Guyana, Suriname

and French Guiana) and covering a vast geographic area

ofc. 5 976 957 km2. Accordingly, it is currently considered

to be a Least Concern (LC) species, given its wide dis-

tribution, tolerance of a range of habitats, presumed large

population, and because it is unlikely to be declining fast

enough to qualify for listing in a more threatened cate-

gory (IUCN, 2009). However, the geographic distribution

of L. andreae may require a reassessment in light of the

recent findings involving forest-associated members of the

L. marmoratus group. Figure 11 also plots the individual lo-

calities for those species that are now known to be different

from the nominal L. andreae but whose populations had,

in the past, been considered to be (or allied to) L. andreae

by field researchers. Acoustic data suggest that L. andreae

does not occur in these specific localities and that it may

have a considerably more restricted distribution than the

currently accepted range. If it does not occur in Bolivia or

southeastern Peru, its geographic range would be reduced

by several thousand square kilometres. While it may have a

lesser, yet still relatively widespread distribution, its currentIUCN status may change (or remain the same); further field

work is needed to determine its current distribution. The

main issue is that unrecognized cryptic species may remain

undetected, and the risk is that they may even become ex-

tinct, because vital data on distributions, population status,

life histories, habitat associations and threats are unknown.

AcknowledgementsWe thank the Museo de Historia Natural de San Marcos,

Museo Noel Kempff Mercado and Coleccon boliviana de

fauna for the loan of type specimens. Cesar Aguilar, Jesus

Cordova, Frank Glaw, Ned Gilmore, Ross MacCulloch,Rossy Montano and Annemarie Ohler facilitated loan of

specimens under their care. IUCN kindly facilitated use of

their shapefiles and allowed use of GIS software for elab-

oration of maps. The Man and Biosphere Program (Smith-

sonian Institution) and the Shell Oil Company provided

logistic support, while the Instituto Nacional de Recursos

Naturales (INRENA) granted appropriate research permits.

Parts of the call description and call figures were first de-

veloped in AAs doctoral thesis;Leptodactylus simonstuarti

is referred to as Adenomera Camisea I in this work. AA

is grateful to Steffen Reichle for first pointing out where

to findL. simonstuarti in Bolivia, for support while in this

country, and for facilitating specimen loans, and to GonzaloCalderon and Jhonny for help in the field. We are grateful

to Axel Kwet and Neil Cox for providing feedback on an

earlier version of this manuscript and to Vineet Katariya

for help with GIS software and maps. AA is grateful to

Mike Hoffmann, Neil Cox and Marinus Hoogmoed for in-

sightful discussions on morphologically cryptic species in

the IUCN Red List. We thank two anonymous reviewers

and the Associate Editor, Dr Barry Clarke, for their helpful

revision of our manuscript.


14/15


ReferencesALMEIDA, A.P. & ANGULO, A. 2006. A new species of Lepto-

dactylus (Anura: Leptodactylidae) from the state of EspritoSanto, Brazil, with remarks on the systematics of associatedpopulations. Zootaxa 1334, 125.

ALVERSON, W.S., MOSKOVITS, D.K. & SHOPLAND, J.M. 2000. Bo-livia: Pando, Ro Tahuamanu. Rapid Biological Inventories

Report 1. The Field Museum, Chicago.ANGULO, A. 2002. Anfibios y paradojas: perspectivas sobre ladiversidad y las poblaciones de anfibios. Ecologa Aplicada1, 105109.

ANGULO, A. 2004. The evolution of the acoustic communicationsystem in members of the genus Adenomera (Anura: Lep-todactylidae): A comparative approach. Unpublished Ph.D.Thesis, University of Toronto.

ANGULO, A., COCROFT, R.B. & REICHLE, S. 2003. Species identityin the genus Adenomera (Anura: Leptodactylidae) in south-eastern Peru. Herpetologica 59, 490504.

ANGULO, A. & ICOCHEA, J. 2003. Adenomera cf. andreae (NCN).Vocalization. Herpetological Review 34, 4748.

ANGULO, A . & R EICHLE, S. 2008. Acoustic signals, species diagno-sis and species concepts: the case of a new cryptic species ofLeptodactylus (Amphibia, Anura, Leptodactylidae) from theChapare region, Bolivia. Zoological Journal of the LinneanSociety 152, 5977.

BERNECK, B.V.M., COSTA, C.O.R. & GARCIA, P.C.A. 2008. A newspecies of Leptodactylus (Anura: Leptodactylidae) from theAtlantic Forest of Sao Paulo State, Brazil. Zootaxa 1795,4656.

BICKFORD, D., LOHMAN, D.J., SODHI, N.S., NG, P.K.L., MEIER, R.,WINKER, K., INGRAM, K.K. & DAS, I. 2007. Cryptic speciesas a window on diversity and conservation. Trends in Ecologyand Evolution 22, 148155.

BOISTEL, R., MASSARY, J.-C. DE & ANGULO, A. 2006. Descriptionof a new species of the genus Adenomera (Amphibia, Anura,Leptodactylidae) from French Guiana. Acta Herpetologica 1,114.

CALVO, M., TEMPLADO, J., OLIVERIO, M. & MACHORDOM, A. 2009.

Hidden Mediterranean biodiversity: molecular evidence for acrypticspecies complex within thereef buildingvermetid gas-tropodDendropoma petraeum (Mollusca: Caenogastropoda).Biological Journal of the Linnean Society 96, 898912.

CAMARGO, A., DE SA, R.O. & HEYER, W.R. 2006. Phylogeneticanalyses of mtDNA sequences reveal three cryptic lineages inthe widespreadneotropicalfrogLeptodactylus fuscus (Schnei-der, 1799) (Anura, Leptodactylidae).Biological Journal of theLinnean Society 87, 325341.

COCROFT, R.B. & RYAN, M.J. 1995. Patterns of advertisement callevolution in toads and chorus frogs. Animal Behaviour 49,283303.

COLBORN, J. , CRABTREE, R.E., SHAKLEE, J.B., PFEILER, E . &BOWEN, B.W. 2001. The evolutionary enigma of Bonefishes(Albula spp.): Cryptic species and ancient separations in a

globally distributed shorefish. Evolution 55, 807820.COMISKEY, J.A., CAMPBELL, J.P., ALONSO, A., MISTRY, S.,

DALLMEIER, F., NU NEZ, P., BELTRAN, H., BALDEON, S., NAU-RAY, W., DE LA COLINA, R., ACURIO, L. & UDVARDY, S. 2001.The vegetation communities of the Lower Urubamba Re-gion, Peru. In: ALONSO, A., DALLMEIER, F. & CAMPBELL, P.,Eds., Urubamba: The Biodiversity of a Peruvian Rainforest.SI/MAB Series # 7, 932.

COPREN, K.A., NELSON, L.J., VARGO, E.L. & HAVERTY, M.I. 2005.Phylogenetic analyses of mtDNA sequences corroborate tax-onomic designations based on cuticular hydrocarbons in sub-

terranean termites. Molecular Phylogenetics and Evolution35, 689700.

CUERVO, A.M., CADENA, C.D., KRABBE, N. & RENJIFO, L.M. 2005.Scytalopus stilesi, a new species of tapaculo (Rhinocrypti-dae) from the cordillera central of Colombia. The Auk 122,445463.

DE LA RIVA, I. 1996. The specific name of Adenomera (Anura:Leptodactylidae) in the Paraguay River Basin.Journal of Her-

petology 30, 556557.DSP DEVELOPMENT CORPORATION. 1998. DADiSP. Cambridge,

MA.ELMER, K.R., DAVILA, J.A. & LOUGHEED, S.C. 2007. Cryptic di-

versity and deep divergence in an upper Amazonian leaflitterfrog, Eleutherodactylus ockendeni. BMC Evolutionary Biol-ogy 7, 247.

EWING, A.W. 1989. Arthropod Bioacoustics: Neurobiology andBehaviour. Comstock Publishing Associates, Cornell Univer-sity Press, Ithaca.

FINER, M., JENKINS, C.N., PIMM, S.L., KEANE, B. & ROSS, C.2008. Oil and gas projects in the western Amazon: Threats towilderness, biodiversity, and indigenous peoples. PLoS ONE3, e2932. doi:10.1371/journal.pone.0002932.

FOUQUET, A. , GILLES, A. , VENCES, M. , MARTY, M. , BLANC,

M . & GEMMELL, N.J. 2007. Underestimation of speciesrichness in Neotropical frogs revealed by mtDNA anal-yses. PLoS ONE 2, e1109. doi:10.1371/journal.pone.0001109.

FROST, D.R. 2009. Amphibian Species of the World: an OnlineReference. Version 5.3 (12 February 2009). American Mu-seum of Natural History, New York. http://research.amnh.org/herpetology/amphibia/.

FU, J. & ZENG, X. 2008. How many species are in the genusBatrachuperus? A phylogeographical analysis of the streamsalamanders (family Hynobiidae) from southwestern China.Molecular Ecology 17, 14691488.

FUNK, W.C., ANGULO, A., CALDWELL, J.P., RYAN, M.J. & CAN-NATELLA, D.C. 2008. Comparison of morphology and callsof two cryptic species of Physalaemus (Anura: Leiuperidae).

Herpetologica 64, 290304.GOWER, D.J., DHARNE, M., BHATTA, G., GIRI, V., VYAS, R., GOVIN-DAPPA, V., OOMMEN, O.V., GEORGE, J. ,SHOUCHE, Y. & WILKIN-SON, M. 2007. Remarkable genetic homogeneity in unstriped,long-tailedIchthyophis along 1500 km of the Western Ghats,India. Journal of Zoology 272, 266275.

HEYER, W.R. 1973. Systematics of the marmoratus group of thefrog genus Leptodactylus (Amphibia, Leptodactylidae). Con-tributions in Science, Natural History Museum, Los AngelesCounty 251, 150.

HEYER, W.R. 1975. Adenomera lutzi (Amphibia: Leptodactyli-dae), a new species of frog from Guyana. Proceedings of theBiological Society of Washington 88, 315318.

HEYER, W.R. 1984. The systematic status of Adenomera griseigu-laris Henle, with comments on systematic problems in thegenus Adenomera (Amphibia: Leptodactylidae). Amphibia-Reptilia 5, 97100.

HEYER, W.R., GARCIA-LOPEZ, J.M. & CARDOSO, A.J. 1996. Adver-tisement call variation in theLeptodactylus mystaceus speciescomplex (Amphibia: Leptodactylidae) with a description of anew sibling species. Amphibia-Reptilia 17, 731.

HEYER, W.R., RAND, A.S., CRUZ, C.A.G., PEIXOTO, O.L. & NEL-SON, C.E. 1990. Frogs of Boraceia. Arquivos de Zoologia 31,230410.

ICOCHEA, J., QUISPITUPAC, E., PORTILLA, A. & PONCE, E. 2001. As-sessment of amphibians and reptiles of the Lower Urubamba
http://research.amnh.org/herpetology/amphibia/http://research.amnh.org/herpetology/amphibia/http://research.amnh.org/herpetology/amphibia/http://research.amnh.org/herpetology/amphibia/


15/15


region, Peru. In ALONSO, A., DALLMEIER, F. & CAMPBELL, P.,Eds., Urubamba: The Biodiversity of a Peruvian Rainforest.SI/MAB Series # 7, 129142.

INGER, R.F., STUART, B.L. & ISKANDAR, D.T. 2009. Systematics ofa widespread Southeast Asian frog, Rana chalconota (Am-phibia: Anura: Ranidae). Zoological Journal of the LinneanSociety 155, 123147.

IUCN. 2001.IUCN Red List Categories and Criteria: Version 3.1.

IUCN Species Survival Commission. IUCN, Gland, Switzer-land and Cambridge, UK.

IUCN. 2009. IUCN Red List of Threatened Species. Version2009.2. www.iucnredlist.org (accessed 14 February 2010).

IUCN STANDARDS AND PETITIONS WORKING GROUP. 2008.Guidelines for using the IUCN Red List Categoriesand Criteria. Version 7.0. Prepared by the Standardsand Petitions Working Group of the IUCN SSC Bio-diversity Assessments Sub-Committee in August 2008.http://intranet.iucn.org/webfiles/doc/SSC/RedList/RedList-Guidelines.pdf.

KELLER, E. 1994. Signalyze. Version 3.12. Infosignal Inc, Lau-sanne.

KOK, P.J.R., KOKUBUM, M.N.C., MACCULLOCH, R.D. & LATH-ROP, A. 2007. Morphological variation in Leptodactylus lutzi

(Anura, Leptodactylidae) with description of its advertise-ment call and notes on its courtship behavior. Phyllomedusa6, 4560.

KOKUBUM, M.N.C. & GIARETTA, A.A. 2005. Reproductive ecol-ogy and behaviour of a species of Adenomera (Anura, Lep-todactylinae) with endotrophic tadpoles: Systematic implica-tions. Journal of Natural History 39, 17451758.

KWET, A. 2007. Bioacoustic variation in the genus Adenomerain southern Brazil, with revalidation of Leptodactylus nanusMuller, 1922 (Anura: Leptodactylidae).Mitteilungen aus demMuseum fur Naturkunde in Berlin, Zool. Reihe 83 (S1) 5668.

KWET, A. & ANGULO, A. 2002. A new species of Adenomera(Anura, Leptodactylidae) from the Araucaria forest of RioGrande do Sul (Brazil), with comments on the systematicstatus of southern populations of the genus. Alytes 20, 2843.

KWET, A., STEINER, J. & ZILLIKENS, A. 2009. A new species ofAdenomera (Amphibia: Anura: Leptodactylidae) fromthe At-lantic rain forest in Santa Catarina, southern Brazil. Studieson Neotropical Fauna and Environment44, 93107.

MARQUEZ, R., DE LA RIVA, I. & BOSCH, J. 1995. Advertisementcalls of Bolivian Leptodactylidae (Amphibia, Anura).Journalof Zoology, London 237, 313336.

PADIAL, J.M. & DE LA RIVA, I. 2009. Integrative taxonomy revealscryptic Amazonian species of Pristimantis (Anura: Strabo-mantidae). Zoological Journal of the Linnean Society 155,97122.

PADIAL, J.M., KOHLER, J., MU NOZ, A. & DE LA RIVA, I. 2008. As-sessing the taxonomic status of tropical frogs through bioa-coustics: geographical variation in the advertisement calls inthe Eleutherodactylus discoidalis species group (Anura). Zo-ological Journal of the Linnean Society 152, 353365.

PAREDES-ESQUIVEL, C., DONNELLY, M.J., HARBACH, R.E. & TOWN-SON, H. 2009. A molecular phylogeny of mosquitoes in theAnopheles barbirostris subgroup reveals cryptic species: im-plications for identification of disease vectors.Molecular Phy-logenetics and Evolution 50, 141151.

PATERSON, H.E.H. & MCEVEY, S.F., Ed. 1993. Evolution andthe Recognition Concept of Species. Collected Writings. TheJohns Hopkins University Press, Baltimore.

PFENNINGER, M. & SCHWENK, K. 2007. Cryptic animal species arehomogeneously distributed among taxa and biogeographicalregions. BMC Evolutionary Biology 7, 121.

PONSSA, M.L. & HEYER, W.R. 2007. Osteological characteriza-tion of four putative species of the genus Adenomera (Anura:

Leptodactylidae), with comments on intra- and interspecificvariation. Zootaxa 1403, 3754.

PRINGLE, A., BAKER, D.M., PLATT, J.L., WARES, J.P., LATGE, J.P.& TAYLOR, J.W. 2005. Cryptic speciation in the cosmopolitanand clonal human pathogenic fungus Aspergillus fumigatus.Evolution 59, 18861899.

READING, C.J. & JOFRE, G.M. 2003. Reproduction in the nestbuilding vizcacheras frog Leptodactylus bufonius in centralArgentina. Amphibia-Reptilia 24, 415427.

RON, S.R., SANTOS, J.C. & CANNATELLA, D.C. 2006. Phylogeny ofthe tungara frog genus Engystomops ( = Physalaemus pus-tulosus species group; Anura: Leptodactylidae). MolecularPhylogenetics and Evolution 39, 392403.

SCHICK, S., VEITH, M. & LOTTERS, S. 2005. Distribution patternsof amphibians from the Kakamega Forest, Kenya. African

Journal of Herpetology 54, 185190.SIMPSON, G.G. 1961. Principles of Animal Taxonomy. Columbia

University Press, New York.STUART, B.L., INGER, R.F. & VORIS, H.K. 2006. High level of

cryptic species diversity revealed by sympatric lineages ofSoutheast Asian forest frogs. Biology Letters 2, 470474.

STUART,S.N.,CHANSON, J.S., COX,N.A.,YOUNG,B.E.,RODRIGUES,A.S.L., FISCHMAN, D.L. & WALLER, R.W. 2004. Status andtrends of amphibian declines and extinctions worldwide. Sci-ence 306, 17831786.

SUMIDA, M., KOTAKI, M., ISLAM, M.M., DJONG, T.H., IGAWA,T., KONDO, Y., MATSUI, M., DE SILVA, A., KHONSUE, W. &NISHIOKA, M. 2007. Evolutionary relationships and reproduc-tive isolating mechanisms in the Rice Frog (Fejervarya lim-nocharis) species complex from Sri Lanka, Thailand, Taiwan

and Japan, inferred from mtDNA gene sequences, allozymes,and crossing experiments. Zoological Science 24, 547562.TORRES-PEREZ, F., MENDEZ, M.A., BENAVIDES, E., MORENO, R.A.,

LAMBOROT, M., PALMA, R.E. & ORTIZ, J.C. 2009. Systematicsand evolutionary relationships of the mountain lizard Liolae-mus monticola (Liolaemini): how morphological and molec-ular evidence contributes to reveal hidden species diversity.Biological Journal of the Linnean Society 96, 635650.

TRONTELJ, P. & FISER, C. 2009. Cryptic species diversityshould not be trivialised. Systematics and Biodiversity 7,13.

VALENCIA, G. & ALONSO, A. 1998. Biodiversity assessment of thediurnal butterflies of the Lower Urubamba region, Peru. In:ALONSO, A. , DALLMEIER, F. & CAMPBELL, P., Eds., Urubamba:The Biodiversity of a Peruvian Rainforest. SI/MAB Series #7, 95109.

VIEITES, D.R., WOLLENBERG, K.C., ANDREONE, F., KOHLER, J.,GLAW, F. & VENCES, M. 2009. Vast underestimation of Mada-gascars biodiversity evidenced by an integrative amphibianinventory. Proceedings of the National Academy of Sciences,USA 106, 82678272.
http://http//www.iucnredlist.orghttp://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pdfhttp://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pdfhttp://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pdfhttp://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pdfhttp://http//www.iucnredlist.org

Date post:	04-Apr-2018
Category:	Documents
Upload:	danramosgutierrez
View:	218 times
Download:	0 times

Crypic Species Complexes Widespreadspecies Leptodactylus Mormaratus Group

Documents