A general assessment of the conservation status and decline trends of Mexican amphibians

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A general assessment of the conservation status

and decline trends of Mexican amphibians

Patricia Frı´as-Alvarez•_{J. Jaime Zu´n˜iga-Vega}•_{Oscar Flores-Villela}

Received: 3 August 2009 / Accepted: 21 September 2010 / Published online: 9 October 2010

ÓSpringer Science+Business Media B.V. 2010

Abstract We present a review on the conservation status and population trends of the

372 amphibian species currently recognized for Mexico. We based our analyses on the information gathered by the International Union for the Conservation of Nature-the Global Amphibian Assessment (IUCN-GAA) as well as on available literature about imminent or potential threats to these organisms in Mexico. This country has the fifth largest amphibian fauna in the world and almost 58% of the species that inhabit this country are considered as threatened. We highlight the proportion of species per order, family, and genus that are currently under severe risk in Mexico. In addition, we prepared a detailed list of the main factors that are threatening amphibians in this country. Evidence is provided that the six main mechanisms that are globally leading amphibians to extinction (alien species, over-exploitation, land use change, global changes, pollution, and infectious diseases) are indeed currently operating in Mexico. We discuss the relative importance of each of these causes. We also highlight the paucity of quantitative studies that support the current conservation status of Mexican amphibian species.

Keywords Conservation statusIUCN red listMexican amphibians

Population trendsThreatened species

P. Frı´as-Alvarez

Departamento de Zoologıá, Instituto de Biologıá, Universidad Nacional Autońoma de Me´xico, Ciudad Universitaria, 04510 Mexico, DF, Mexico

J. J. Zu´n˜iga-Vega (&)

Departamento de Ecologı´a y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Auto´noma de Me´xico, Ciudad Universitaria, 04510 Mexico, DF, Mexico

e-mail: [email protected]

O. Flores-Villela

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Worldwide, many amphibian populations are declining (Laurance1996; Houlahan et al.

2000; Lips et al. 2005a, b). Reports about the conservation and status of biodiversity indicate that amphibians are threatened and declining at faster rates than birds and mammals (Stuart et al.2004). Currently 1229 amphibian species are globally reported as endangered and critically endangered, and 39 are considered as extinct in the wild (Stuart et al.2008; IUCN2010).

Mexico is considered a mega-diverse country with a complex geologic history, a unique topography, and greatly diverse vegetation types (Flores-Villela and Gerez1994; Benı´tez-Dı´az and Bellot-Rojas 2003; Ochoa-Ochoa and Flores-Villela 2006). The rich Mexican biodiversity harbors the fifth largest amphibian fauna in the world (Ochoa-Ochoa and Flores-Villela2006; Stuart et al.2008; IUCN2010). Mexico has 372 described amphibian species from which 250 occur only in Mexico (67.2%; Flores-Villela and Canseco-Ma´r-quez2004; Frost2010). Thus, this country is considered as the number three in amphibian endemic species (Stuart et al. 2008). Nevertheless, the current rate of annual species description is increasing: 11.5 and 27.4% of Mexican anurans and salamanders, respec-tively, were described between 1992 and 2007 (Flores-Villela and Canseco-Ma´rquez

2004). Therefore, the actual number of Mexican species appears to be greatly underesti-mated (Frı´as-Alvarez et al.2008).

In the past years some studies have documented declines of Mexican amphibians (Parra-Olea et al.1999; Frı´as-Alvarez et al.2008). Recent field surveys indicate that nowadays it is quite difficult to find salamanders and frogs that were collected by hundreds during the 1970s and 1980s (Parra-Olea et al.1999; Lips et al.2004). Destruction, fragmentation, and modification of their natural habitats are the best-recognized causes of such declines (Parra-Olea et al.1999; Rovito et al.2009). In fact, the highest rates of global habitat loss have occurred in tropical and semi-tropical regions, which correspond to those countries (Mexico included) supporting the richest assemblages of amphibian fauna (Gallant et al.

2007). In addition, diseases (e.g., chytridiomycosis), pollution, increases in UV-B radia-tion, introduction of exotic species, and over-exploitation have been considered as other important causes for the decline of Mexican amphibians (Frı´as-Alvarez et al.2008,2010; Gonza´lez-Bernal2008).

These facts highlight the importance of a general picture that summarizes the Mexican amphibian species that are currently experiencing threats and declines. No synthesis of such information is currently available on the scientific literature (Frı´as-Alvarez et al.

2008). Thus, in this paper we present an evaluation of the current conservation status and trends of the amphibian species that inhabit in Mexico, as well as a summary of the main threats experienced by these organisms in this country. We attempt to create a useful and informative reference for all the future scientific and educational studies focused on the conservation, ecology, and distribution of the Mexican amphibian fauna.

Materials and methods

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that Stuart et al. (2004) used for a global amphibian assessment but we focus only in Mexico.

The GAA-red list of threatened species has included 16 families, 52 genera, and 364 amphibian species that inhabit in Mexico (227 from the order Anura, 135 from Caudata, and 2 from Gymnophiona). The list lacks a few described species (it includes 364 of 372 currently described species for Mexico; Flores-Villela and Canseco-Ma´rquez2004; Frost

2010) as well as several others that still await for formal description. We focused our attention on the three main protection categories of the IUCN, which are those pointing out to species under the highest risks of extinction: Vulnerable (VU), Endangered (EN), and Critically Endangered (CR). Henceforth, we use the term ‘‘threatened’’ to indicate that a species is listed in one of these three conservation categories (as per IUCN2010). In our results, all the percentages of species within particular conservation categories are based on the 364 species included in the GAA data base.

We conducted a comparison of the conservation categories of Mexican amphibians as considered by the Mexican environmental agency with the conservation categories pro-posed by the IUCN red list. This Mexican official list of species at risk was issued originally in 1994 and updated in 2001 (Norma Oficial Mexicana, NOM-059-ECOL-2001, Secretarı´a de Medio Ambiente y Recursos Naturales 2002). With this comparison we aimed to evaluate how the Mexican government currently considers the conservation status of the native amphibian fauna. Four conservation categories are defined by this Mexican official list, which according to this document are partially coincident with the IUCN categories. (1) Probably Extinct in the Wild (E). This category coincides with the IUCN Extinct (EX) and Extinct in the Wild (EW) categories. (2) Threatened with Extinction (P), partially coincident with the IUCN CR and EN categories. (3) Threatened (A), partially coincident with the VU category. (4) Under Special Protection (Pr). This category can include the low-risk categories of the red list: Near Threatened (NT), Least Concern (LC), and Data Deficient (DD).

In addition to the information available from the GAA, we conducted an extensive search for literature containing evidence of declining populations of amphibians in Mexico. We surveyed several sources of reliable information: peer-reviewed journals, unpublished academic theses and dissertations, and books. Our aim was to find formal experimental or empirical studies that evaluated the demographic or genetic trends of amphibian popula-tions anywhere throughout Mexico. We also considered reports that compared past and present abundances of amphibians in the wild and those that document imminent threats to focal populations.

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Mexican amphibians are more threatened than any other vertebrate group as indicated by a larger proportion of amphibian species that are included in one of the three main protection categories of the IUCN red list (57.97%, 211 species), in comparison with Mexican mammals (19.35%), Mexican birds (5.01%) or Mexican reptiles (14.07%; Table1). In addition, given the high rates of habitat deterioration all throughout Mexico (Challenger

2003), it is not surprising that 21 species (5.77%) are currently listed as Near Threatened (NT; Table1).

From the 246 amphibian species that according to the GAA data base are endemic to Mexico, a disturbing 69.5% are considered as threatened (171 species). From these, 27 species are categorized as VU, 67 as EN, and 77 as CR.

The families with more threatened species are (percentage of species listed as threa-tened by the IUCN-GAA; Table2): Plethodontidae (73.04%), Ambystomatidae (64.71%), Eleutherodactylidae (60.87%), Craugastoridae (59.46%), Hylidae (58.95%), Ranidae (42.30%), Bufonidae (31.25%), and Microhylidae (20%). The single species of the family Salamandridae that occurs in Mexico (Notophthalmus meridionalis) is EN. Similarly, one of the two species of the family Caeciliidae (Dermophis mexicanus) inhabiting in this country is listed as VU.

Several genera experience severe conservation problems as indicated by their high percentages of threatened species:Thorius (95.65%),Plectrohyla (87.88%),

Chiroptero-triton(83.33%),Pseudoeurycea(77.55%),Ecnomiohyla(66.67%),Ambystoma(64.71%),

Eleutherodactylus(60.87%),Craugastor(59.46%), andExerodonta(55.56%). All species

(100%) in the following genera, which only have a few representatives in Mexico (from 1 to 5 species), are considered as threatened: Bromeliohyla, Charadrahyla, Cryptotriton,

Dendrotriton, Duellmanohyla, Megastomatohyla, Notophthalmus, Nyctanolis, and

Par-vimolge. The generaAgalychnis,Dermophis,Hypopachus, andRanaare each represented

in Mexico by only two species, for a total of eight species. Of these pairs, one species in each genus is listed as either VU, EN, or CR (Table2).

The threat to Mexican amphibians is quite alarming in the order Caudata (newts, sal-amanders, and axolotls), which has 96 species (71.11%) listed as threatened by the IUCN. Eleven of these species are considered as VU (8.15%), 40 as EN (29.63%), and 45 as CR (33.33%). At least 114 members of the order Anura that inhabit Mexico (50.22%) are threatened, with 32 species in the category of VU (14.10%), 39 EN (17.18%), and 43 CR (18.94%). Knowledge about the only two Mexican species of the order Gymnophiona is drastically poor even though one of them is endemic to Mexico (Dermophis oaxacae). The latter species is listed as DD whereas the other species, Dermophis mexicanus, is con-sidered as VU (Tables1,2).

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(6)

(7)

(8)

ble

2

continu

ed

rder

Family

G

enus

Total

EX

D

LC

NT

VU

EN

CR

TH

ta

Si

renidae

Siren

2

0

2

00

0

hio

na

Caec

iliidae

Derm

ophis

2

0

1

0

01

00

1

(5

0

Total

364

0

3

8

9

4

2

1

4

7

9

8

211

(5

7.97)

ata

are

shown

by

Ord

er,

Family,

and

Genus.

Red

list

categories

VU,

EN,

an

d

C

R

indicat

e

species

that

are

curren

tly

threatened

in

th

e

wild.

We

show

ber

and

pe

rcentage

(with

in

pa

renthes

es)

of

species

of

each

genus

that

are

listed

in

the

three

latter

cate

gories

(

TH

threat

ened

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present in the Mexican territory. These species areAmbystoma mavortium,A. subsalsum,

Charadrahyla tecuani, Craugastor galacticorhinus, C. saltator, Lithobates brownorum,

and Ptychohyla macrotympanum (Frost 2010). In addition, Incilius campbelli, which is

listed as NT, was not considered to be present in Mexico by the IUCN (2010). However, this species is currently recognized as occurring in southeastern Mexico (Frost2010).

In comparison with the 364 taxa listed by the IUCN red list, the Mexican list of species at risk (NOM-059-ECOL-2001, Secretarı´a de Medio Ambiente y Recursos Naturales2002) only includes 197 amphibian species (Table3). However, after the recent taxonomic changes (e.g., Frost et al. 2006) only 194 actual species are listed by the Mexican gov-ernment. According to the Mexican list, there are no extinct (E) amphibians, 6 species are threatened with extinction (P), 39 are threatened (A), and 149 are under special protection (Pr). From those species missed by the NOM-059-ECOL-2001, 25 are listed by the IUCN as CR, 28 as EN, and 20 as VU (i.e., 73 threatened species). When comparing the 194 species listed by the NOM-059-ECOL-2001 with those listed by the IUCN red list we found that only 59 taxa are in coincident categories. From such 59 species, six are listed as P by the NOM-059-ECOL-2001 and as EN or CR by the IUCN, six are considered as A by the 059-ECOL-2001 and as VU by the IUCN, and 47 are listed as Pr by the NOM-059-ECOL-2001 and as NT, LC or NT by the IUCN red list (Table3).

We must highlight the fact that 126 amphibian species listed by the Mexican govern-ment are in lower-risk conservation categories in comparison with those assigned by the IUCN (Table3). From such 126 species, 49 and 59 are considered by the red list as EN and CR, respectively, whereas in the NOM-059-ECOL-2001 these are listed as either A (26 taxa) or Pr (82 taxa). The remaining 18 taxa are listed by the IUCN as VU, whereas the NOM-059-ECOL-2001 lists them as Pr. In contrast, only seven amphibian species are included in a higher-risk conservation category according to the Mexican authorities in comparison with their status on the IUCN red list. Such seven amphibians are listed by the IUCN as either NT (four species), LC (two species) or DD (one species), whereas in the NOM-059-ECOL-2001 all them appear as A. Additionally, two species (Craugastor

sal-tatorandLithobates brownorum) are listed as Pr in the NOM-059-ECOL-2001 and do not

appear on the IUCN red list (Table3).

In Table3 we also show the factors that are apparently threatening to every single Mexican amphibian species. Notice that the information contained in this table comes from both the GAA assessment and our additional extensive literature survey. The most com-mon threat to Mexican amphibians is land use change. A total of 322 species out of the 372 recognized for Mexico by the IUCN (86.56%) suffer from the consequences of the human activities that modify their natural habitat. Emerging infectious diseases represent the second most conspicuous threat. A total of 87 species (23.39%) have been suggested as actual or at least potential victims of pathogens. Pollution is also impacting a relatively high number of species: 76 Mexican amphibians (20.43%) are threatened by toxic chemicals. The introduction of alien species is currently damaging 41 species (11.02%), whereas global changes and over-exploitation each affects 36 (9.68%) species (Table3).

Discussion

(10)

ble

3

Lis

t

o

f

the

conservat

ion

cate

gories

and

main

threat

s

affecting

the

372

Mexi

can

amp

hibian

species

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

Alien species Over- exploita

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Bufoni

dae

Anaxyr

us

borea

s

NT

x

Anaxyr

us

californ

icus

EN

x

*x

x

1

Anaxyr

us

cognat

us

LC

x

*

x

2

Anaxyr

us

compact

ilis

LC

x

*

x

2,

3

Anaxyr

us

bebi

lis

LC

Pr

x

Anaxyr

us

kelloggi

LC

x

Anaxyr

us

me

xicanus

NT

x

Anaxyr

us

punct

atus

LC

x

Anaxyr

us

retifo

rmis

LC

Pr

x

Anaxyr

us

specio

sus

LC

x

Anaxyr

us

woodhou

sii

LC

x

4

Incilius

alva

rius

LC

xx

*1

,

4

Incil

ius

bocou

rti

LC

x

Incil

ius

campbe

lli

a

NT

x

Incil

ius

canal

iferus

LC

x

Incil

ius

cavif

rons

EN

Pr

x

Incil

ius

cocc

ifer

LC

Pr

x

Incilius

crist

atus

CR

Pr

x

*x

x

5,

6

Incil

ius

cycladen

VU

x

Incil

ius

gemm

ifer

EN

Pr

x

(11)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Incil

ius

luetk

enii

LC

x

Incil

ius

macrocri

status

VU

x

Incilius

m

a

rmoreu

s

LC

x

7

Incil

ius

mazatla

nensis

LC

x

Incil

ius

nebul

ifer

LC

x

Incil

ius

occid

enta

lis

LC

x

Incil

ius

perpl

exus

EN

x

Incil

ius

pis

innus

DD

x

Incil

ius

spi

culatus

EN

x

Incil

ius

taca

nensis

EN

x

Incil

ius

tutela

rius

EN

x

Incilius

valliceps

LC

xx

8,

9,

10

Rhine

lla

marina

LC

x

7,

9,

10,

12

Centrol

enida

e

Hya

linobat

rachiu

m

fleischmanni

LC

x

13

Craug

astoridae

Crauga

sto

r

alfredi

VU

x

Crauga

sto

r

amniscol

a

DD

x

Crauga

sto

r

augusti

LC

x

Crauga

sto

r

batrachyl

us

DD

Pr

x

(12)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Craug

astor

berkenbu

schii

NT

Pr

x

*x

x

5,

13

Crauga

sto

r

brocchi

VU

x

Crauga

sto

r

decoratus

VU

Pr

x

Crauga

sto

r

galacticorh

inu

s

x

Crauga

sto

r

glaucus

CR

Pr

x

Craug

astor

gregg

i

CR

Pr

x

13

Craug

astor

guerreroe

nsis

b

CR

Pr

x

13,

14

Craug

astor

hobartsm

ithi

EN

x

*1

5

Craug

astor

laticep

s

NT

Pr

x

13

Craug

astor

li

neatus

CR

Pr

x

13

Crauga

sto

r

loki

LC

x

Crauga

sto

r

matudai

VU

Pr

x

Crauga

sto

r

megalotymp

anum

CR

Pr

x

Craug

astor

mexicanu

s

LC

Pr

x

*

x

13

Crauga

sto

r

montanu

s

EN

Pr

x

Craug

astor

occidentalis

DD

x

15

Crauga

sto

r

omiltema

nus

EN

Pr

x

(13)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Crauga

sto

r

palenque

DD

x

Crauga

sto

r

pelorus

DD

x

Craug

astor

polymni

ae

b

CR

Pr

x

13,

14

Crauga

sto

r

pozo

CR

x

Crauga

sto

r

pygmaeu

s

VU

x

Crauga

sto

r

rhod

opis

VU

x

Craug

astor

rugulosu

s

LC

x

13

Crauga

sto

r

rupini

us

LC

x

Crauga

sto

r

saltator

Pr

x

Crauga

sto

r

silvicola

EN

Pr

x

Craug

astor

spatulat

us

EN

Pr

x

*5

Crauga

sto

r

stuart

i

EN

Pr

x

Crauga

sto

r

tarahuma

raensis

VU

Pr

x

Craug

astor

tayl

ori

c

DD

Pr

x

16

Craug

astor

un

o

c

EN

Pr

x

*1

6

Crauga

sto

r

vocal

is

LC

x

Crauga

sto

r

vulca

ni

EN

x

Crauga

sto

r

yucatanensis

NT

Pr

x

(14)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Eleuth

erodac

tylidae

Eleutheroda

ctylus

angusti

digitoru

m

VU

Pr

x

*

x

17

Eleu

therodact

ylus

cystignathoides

LC

x

Eleu

therodact

ylus

dennisi

EN

Pr

x

Eleu

therodact

ylus

dilatus

EN

x

Eleu

therodact

ylus

dixoni

CR

Pr

x

Eleu

therodact

ylus

grandis

CR

Pr

x

Eleu

therodact

ylus

guttila

tus

LC

x

Eleu

therodact

ylus

interorbitalis

DD

Pr

x

Eleu

therodact

ylus

leprus

VU

x

Eleu

therodact

ylus

longipe

s

VU

x

Eleu

therodact

ylus

maurus

DD

Pr

x

Eleutheroda

ctylus

modest

us

VU

Pr

x

*1

5

Eleu

therodact

ylus

nitidus

LC

x

(15)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Eleu

therodact

ylus

nivicol

imae

VU

Pr

x

Eleu

therodact

ylus

pallidus

DD

Pr

x

Eleu

therodact

ylus

pipilans

LC

x

Eleu

therodact

ylus

rubrimaculatus

VU

x

Eleutheroda

ctylus

rufescen

s

CR

Pr

x

*

x

17

Eleu

therodact

ylus

saxatilis

EN

x

Eleu

therodact

ylus

syristes

EN

Pr

x

Eleu

therodact

ylus

teretistes

DD

Pr

x

Eleu

therodact

ylus

verrucipes

VU

Pr

x

Eleu

therodact

ylus

verrucul

atus

DD

Pr

x

Hylidae Acri

s

crepitans

LC

x

Agalyc

hnis

callidryas

LC

x

Agalych

nis

moreletii

CR

x

*

x

13,

18

Anothec

a

spinosa

LC

(16)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Bromel

iohyla

bromelia

cia

EN

x

Brom

eliohyl

a

dendroscarta

b

CR

Pr

x

13,

14

Chara

drahy

la

altipot

ens

b

CR

Pr

x

13,

14

Charad

rahyl

a

chaneq

ue

EN

Pr

x

Chara

drahy

la

nephila

VU

x

*1

3

Chara

drahy

la

taeniopu

s

VU

A

x

*

x

*

5

,

10,

19

Charad

rahyl

a

tecuani

x

Chara

drahy

la

trux

b

CR

A

x

13,

14

Dendro

psop

hus

ebraccatus

LC

x

Dendro

psop

hus

microcephalus

LC

x

Dendro

psop

hus

robertme

rtensi

LC

x

Dendro

psop

hus

sartori

LC

A

x

Diag

lena

spat

ulata

LC

x

Duellm

anohy

la

chamulae

EN

Pr

x

(17)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Duel

lmanoh

yla

ignicolo

r

EN

Pr

x

*1

3

Duellm

anohy

la

schmidto

rum

VU

Pr

x

Ecnom

iohyla

echinata

b

CR

Pr

x

13,

14

Ecnom

iohyla

miotym

panum

NT

x

*

x

10,

19

Ecnomiohy

la

valancife

r

CR

Pr

x

Exerod

onta

abdi

vita

DD

x

Exerod

onta

bivo

cata

DD

x

Exerod

onta

chimalap

a

EN

x

Exerod

onta

jua

nitae

VU

A

x

Exer

odont

a

melanom

ma

VU

Pr

x

*

13,

18

Exerod

onta

orum

VU

Pr

x

Exer

odont

a

smarag

dina

LC

Pr

x

*

x

15

Exerod

onta

sumichrast

i

LC

x

Exerod

onta

xer

a

VU

x

Hyla

arbo

ricola

DD

x

Hyla

aren

icolor

LC

x

2

Hyla

euph

orbiacea

NT

x

(18)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Hyla

eximi

a

LC

x

xx

2,

7,

18

Hyla

plicat

a

LC

A

x

Hyla

wa

lker

VU

x

Hyla

wrigh

torum

LC

x

Megast

omatohyl

a

mixe

CR

Pr

x

Mega

stoma

tohyla

mixoma

culata

EN

A

x

*5

Megast

omatohyl

a

nubicol

a

EN

A

x

Mega

stoma

tohyla

pellita

b

CR

x

13,

14

Pach

ymedusa

dacnicolor

LC

x

x7

,

1

2

Plectroh

yla

acanthod

es

CR

Pr

x

Plectroh

yla

ameiboth

alame

DD

x

Plectroh

yla

arboresc

andens

EN

Pr

x

*x

x

5

Plectroh

yla

avia

CR

Pr

x

Plectroh

yla

bistinct

a

LC

Pr

x

*

x

x1

7

Plectroh

yla

calthu

la

CR

x

*x

2

0

Plectroh

yla

calvicollina

b

CR

x

13,

(19)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Plectroh

yla

celata

b

CR

x

13,

14

Plectroh

yla

cemb

ra

b

CR

A

x

13,

14

Plectroh

yla

charadri

cola

EN

A

x

Plectroh

yla

chryse

s

CR

Pr

x

Plectroh

yla

crassa

CR

Pr

x

Plectroh

yla

cyanomma

b

CR

A

x

13,

14

Plectroh

yla

cyclada

EN

x

*1

3

Plectroh

yla

ephemera

b

CR

x

*

14,

21,

22

Plectroh

yla

guatemal

ensis

CR

x

13

Plectroh

yla

hartwegi

CR

Pr

x

13

Plectroh

yla

hazelae

b

CR

Pr

x

13,

14

Plectroh

yla

ixil

CR

x

*2

1

Plectroh

yla

labedact

yla

c

DD

x

*1

6

Plectroh

yla

lacertosa

EN

Pr

x

Plectroh

yla

ma

tudai

VU

x

*1

3

Plectroh

yla

miahuat

lanensi

s

DD

x

Plectroh

yla

mykter

EN

A

x

(20)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Plectroh

yla

pachyde

rma

c

CR

Pr

x

*x

1

6

Plectroh

yla

pentheter

EN

x

Plectroh

yla

psarosem

a

CR

x

Plectroh

yla

pycnochila

CR

A

x

Plectroh

yla

robertsor

um

EN

A

x

Plectroh

yla

sabrin

a

CR

A

x

*1

3

Plectroh

yla

sagorum

EN

x

*1

3

Plectroh

yla

siopela

b

CR

x

14

Plectroh

yla

thorect

es

b

CR

Pr

x

13,

14

Pseud

acris

cadaverina

LC

x

Pseud

acris

clarkii

LC

x

Pseu

dacris

regil

la

LC

xx

4,

23

Ptych

ohyla

acrochorda

DD

x

Ptychoh

yla

erythromm

a

EN

Pr

x

*1

3

Ptych

ohyla

euthysano

ta

NT

A

x

(21)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Ptychoh

yla

leonhardsch

ultzei

EN

Pr

x

13

Ptych

ohyla

macroty

mpanum

x

Ptychoh

yla

zophodes

DD

x

*1

3

Scin

ax

stauffe

ri

LC

x

Smili

sca

baudi

nii

LC

x

7

Smili

sca

cya

nostic

ta

NT

x

13

Smili

sca

dentat

a

EN

A

x

*

x

2,

24

Smilis

ca

fodiens

LC

x

Tlalo

cohyla

godmani

VU

A

x

Tlalo

cohyla

loq

uax

LC

x

Tlalo

cohyla

pict

a

LC

x

5

Tlalo

cohyla

sm

ithii

LC

x

*1

5

Trac

hycephalus

venulosus

LC

x

Tripri

on

petasat

us

LC

Pr

x

Leiuper

idae

Engys

tomops

pustulosus

LC

x

Leptodac

tylidae

Lept

odactylus

fragilis

LC

x

(22)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Lept

odactylus

melanon

otus

LC

x

x1

5

Micro

hylidae

Gast

rophry

ne

elegans

LC

Pr

x

Gast

rophry

ne

olivacea

LC

Pr

x

Gast

rophryn

e

usta

LC

Pr

x

*1

5

Hypopa

chus

barb

eri

VU

x

Hyp

opachu

s

variolo

sus

LC

x

15

Ranidae Lith

obates

berland

ieri

LC

Pr

xx

1,

9,

10,

25,

26

Lith

obates

brownoru

m

Pr

x

27,

28,

29

Litho

bates

catesbe

ianus

LC

x

Litho

bates

chichicuahutla

CR

x

Litho

bates

chiricahuensis

VU

A

x

Litho

bates

dunn

i

EN

Pr

x

Lith

obates

forre

ri

LC

Pr

xx

7,

11,

17,

31,

32

Litho

bates

joh

ni

EN

P

x

(23)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Litho

bates

lemosespinal

i

DD

x

Litho

bates

maculatu

s

LC

x

Lith

obates

magnaocu

lar

is

LC

x

x3

2

Lith

obates

megapod

a

VU

Pr

x

xx

*x

x

*

x

10,

17,

18,

26,

31,

Lith

obates

montezu

mae

LC

Pr

x

*

x

*

xx

7,

10,

17,

31,

34

Lith

obates

neovolcan

icus

NT

A

x

*x

xx

2,

17,

18

Lith

obates

omilteman

us

b

CR

P

x

*

xx

13,

14,

35

Lith

obates

psilonot

a

c

DD

x

*

x

2,

16

Lith

obates

puebla

e

b,c

CR

P

x

*

x

14,

16

Litho

bates

pustulosus

LC

Pr

x

Lith

obates

sierram

adrensi

s

VU

Pr

x

*1

3

Lith

obates

spectabilis

LC

x

*

12,

18

Lith

obates

tarahum

arae

VU

x

*

36,

(24)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Lith

obates

tlalo

ci

b

CR

P

x

*

x

*

x

14,

38,

39,

40

Lith

obates

vailla

nti

LC

x

*

x

27,

28,

29

Lith

obates

yavapa

iensis

LC

Pr

x

*

x

*

x

1,

4,

41,

Litho

bates

zwei

feli

LC

x

Rana

boyl

ii

NT

Pr

x

*1

Rana

drayt

onii

VU

x

*x

x

1

Rhino

phryn

idae

Rhinop

hrynu

s

dorsalis

LC

Pr

x

Scaph

iopodida

e

Scaph

iopus

couchi

i

LC

x

Spea

bombi

frons

LC

x

Spea

hammon

dii

NT

x

Spea

multi

plicata

LC

x

x7

Ambyst

omati

dae

Ambystoma altami

rani

EN

A

x

*

x

*x

x

10,

18,

30,

43,

44

Ambystoma amblycephalu

m

CR

Pr

x

*

x

*1

7

Ambystoma anderson

i

CR

Pr

x

*

xx

*1

(25)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Ambyst

oma

bombyp

ellum

CR

Pr

x

Ambystoma dumerilii

CR

Pr

x

*

x

*

x

*

10,

17,

30,

45

Ambyst

oma

flavipip

eratum

DD

Pr

x

Ambystoma granulos

um

CR

Pr

x

18

Ambystoma

leora

e

CR

A

x

xx

*

x

30,

44

Ambystoma lermaen

se

CR

Pr

x

*

x

*

x

*

10,

30,

46,

44

Ambyst

oma

mavortiu

m

x

Ambystoma mexicanu

m

CR

Pr

x

*

x

*

x

*

x

*

x

*

10,

34,

47,

48

Ambystoma ordinariu

m

EN

Pr

x

*

x

*1

7

Ambystoma

rivula

re

DD

A

x

*

x

*x

x

18,

30,

44

Ambyst

oma

rosaceu

m

LC

Pr

x

Ambyst

oma

silvense

DD

x

Ambyst

oma

subsalsu

m

x

Ambystoma

taylori

CR

Pr

x

10,

30

Ambystoma tigrinum

LC

Pr

x

*

xx

*

xx

x

2,

17,

(26)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Ambystoma

velasci

LC

Pr

x

xx

*x

x

10,

18,

30,

44

Pletho

dontida

e

Anei

des

lugubri

s

LC

Pr

x

Batracho

seps

m

ajor

LC

x

Bolitogl

ossa

alberchi

LC

x

Bolitogl

ossa

engelhard

ti

EN

Pr

x

Bolitogl

ossa

flavime

mbris

EN

Pr

x

Bolitogl

ossa

flaviventris

EN

x

Bolitogl

ossa

franklini

EN

Pr

x

Boli

toglossa

hartwegi

NT

x

49

Bolitogl

ossa

hermosa

NT

Pr

x

Bolitogl

ossa

lincol

ni

NT

x

Bolitogl

ossa

macrinii

NT

Pr

x

Bolitogl

ossa

mexicana

LC

Pr

x

Bolitogl

ossa

mulleri

VU

(27)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Bolitogl

ossa

oaxacensis

DD

x

Bolitogl

ossa

occidentalis

LC

Pr

x

Bolitogl

ossa

platyda

ctyla

NT

Pr

x

Bolitogl

ossa

riletti

EN

Pr

x

Boli

toglossa

rostrata

VU

Pr

x

xx

50

Bolitogl

ossa

rufescens

LC

Pr

x

Bolitogl

ossa

stuart

i

DD

Pr

x

Bolitogl

ossa

veracrucis

EN

Pr

x

Bolitogl

ossa

yucatana

LC

Pr

x

Bolitogl

ossa

zapoteca

DD

x

Chiro

pterotriton

arboreus

CR

Pr

x

Chiro

pterotriton

chiropt

erus

CR

Pr

x

Chiro

pterotriton

chondrost

ega

EN

Pr

x

Chiro

pterotriton

cracens

EN

x

(28)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Chir

opterot

riton

dimidi

atus

EN

Pr

x

xx

34,

49,

50

Chiro

pterotriton

lavae

CR

Pr

x

Chir

opterot

riton

magnipes

b

CR

Pr

x

14

Chir

opterot

riton

mosaue

ri

b

DD

Pr

x

14

Chir

opterot

riton

multident

atus

EN

Pr

x

*x

x

14,

34,

49,

50

Chiro

pterotriton

orculus

VU

x

Chiro

pterotriton

priscus

NT

Pr

x

Chiro

pterotriton

terrestris

CR

x

Cryp

totriton

adelos

EN

Pr

x

Cryp

totriton

alvarezdeltoroi

EN

Pr

x

Dendro

trito

n

megarh

inus

VU

Pr

x

Dendro

trito

n

xolocalcae

VU

Pr

x

Ensa

tina

eschscholtzii

LC

Pr

x

Nyct

anolis

pernix

EN

Pr

x

Oedip

ina

elon

gata

LC

Pr

(29)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Parvim

olge

townsend

i

CR

A

x

xx

49,

50

Pseud

oeurycea

ahuitzotl

CR

x

Pseud

oeurycea

altamo

ntana

EN

Pr

x

Pseud

oeurycea

amuzga

DD

x

Pseud

oeurycea

anitae

CR

A

x

Pseu

doeuryc

ea

aquatica

b

CR

x

*

x

14,

51

Pseud

oeurycea

aurantia

VU

x

Pseu

doeuryc

ea

bellii

VU

A

x

xx

*x

x

34,

49

Pseud

oeurycea

boneti

VU

x

Pseud

oeurycea

brunnat

a

CR

Pr

x

Pseu

doeuryc

ea

cephali

ca

NT

A

x

*

x

49

Pseud

oeurycea

cochranae

EN

A

x

Pseud

oeurycea

conanti

EN

A

x

(30)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Pseud

oeurycea

firscheini

EN

Pr

x

Pseud

oeurycea

gadovii

EN

Pr

x

Pseud

oeurycea

galeanae

NT

A

x

Pseud

oeurycea

gigante

a

CR

x

Pseud

oeurycea

goebeli

CR

A

x

Pseu

doeuryc

ea

juarezi

CR

A

x

49

Pseu

doeuryc

ea

leprosa

VU

A

x

*

x

49

Pseu

doeuryc

ea

lineola

EN

Pr

x

49

Pseud

oeurycea

longica

uda

EN

Pr

x

Pseud

oeurycea

lynchi

CR

x

Pseud

oeurycea

maxima

DD

x

Pseud

oeurycea

melanom

olga

EN

Pr

x

Pseud

oeurycea

mixcoa

tl

DD

x

(31)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Pseud

oeurycea

mixteca

LC

x

Pseud

oeurycea

mystax

EN

x

Pseu

doeuryc

ea

naucampa

tepet

l

b

CR

A

x

14

Pseud

oeurycea

nigra

CR

P

x

Pseu

doeuryc

ea

nigroma

culata

b

CR

Pr

x

xx

14,

50

Pseud

oeurycea

obesa

DD

x

Pseud

oeurycea

orchileucos

EN

x

Pseud

oeurycea

orchime

las

EN

x

Pseud

oeurycea

papenfus

si

NT

x

Pseu

doeuryc

ea

parva

b

CR

A

x

14

Pseu

doeuryc

ea

praecel

lens

b,c

CR

A

x

*

x

14,

16,

49

Pseud

oeurycea

quetzal

anens

is

DD

x

Pseu

doeuryc

ea

rex

CR

Pr

x

xx

50

Pseud

oeurycea

robertsi

CR

A

x

(32)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Pseud

oeurycea

ruficauda

DD

x

Pseud

oeurycea

saltator

CR

A

x

Pseud

oeurycea

scandens

VU

Pr

x

Pseu

doeuryc

ea

smithi

CR

A

x

*

xx

49,

50

Pseud

oeurycea

tenchalli

EN

x

Pseud

oeurycea

teotepec

EN

x

Pseud

oeurycea

tlahcuil

oh

CR

x

Pseud

oeurycea

tlilicxitl

DD

x

Pseu

doeuryc

ea

unguiden

tis

CR

A

x

*

x

49,

50

Pseud

oeurycea

werleri

EN

Pr

x

Thoriu

s

arbo

reus

EN

x

Thoriu

s

aureu

s

CR

x

Thoriu

s

borea

s

EN

x

Thori

us

dubitus

EN

Pr

x

xx

50

Thoriu

s

gran

dis

EN

x

Thori

us

infer

nalis

b,c

CR

x

*

x

14,

(33)

ble

3

cont

inue

d

IUCN category

Mexica

n

official list

Endemi

c

to

Mexi

co

tion

Land use change

Globa

l

changes

Pollu

tion

Emergin

g

infectious diseases

Lack

of

recent

observa

tions

Lack

of

informat

ion

Refer

ences

Thoriu

s

inspe

ratus

DD

x

Thoriu

s

lunari

s

EN

x

Thoriu

s

macdou

galli

VU

Pr

x

Thori

us

magn

ipes

b

CR

x

xx

14,

50

Thoriu

s

minutissi

mus

CR

Pr

x

Thori

us

minyde

mus

c

CR

x

*x

1

6

Thoriu

s

muni

ficus

CR

x

Thori

us

narismag

nus

b

CR

x

14

Thori

us

nariso

valis

b

CR

Pr

x

*

x

14,

49

Thoriu

s

omiltemi

EN

x

Thoriu

s

papa

loae

EN

x

Thori

us

pennatul

us

CR

Pr

x

xx

49,

50

Thori

us

pulmon

aris

EN

Pr

x

*

x

49

Thoriu

s

schmidti

EN

x

Thoriu

s

smithi

CR

Pr

x

Thoriu

s

spilog

aster

CR

x

Thori

us

troglody

tes

EN

Pr

x

xx

49,

50

Salaman

dridae

Notop

hthalm

us

meridion

alis

EN

P

x

Sirenid

ae

Siren

intermedi

a

LC

Pr

(34)

ble 3 cont inue d IUCN category Mexica n official list Endemi c to Mexi co Alien species Over- exploita tion

Land use change

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2010). According to global data, Mexico is considered as number two within the list of countries with the greatest numbers of threatened species (Stuart et al. 2008). It is important to notice that the number of Mexican amphibian species currently considered as threatened is underestimated because 38 of them (10.44%) are included in the DD cate-gory. Moreover, seven Mexican amphibian species are not included in the GAA red list and nothing is known about their conservation status or population trends. Future con-servation assessments will thus raise the proportion of amphibian species that in Mexico are experiencing serious threats.

Even though the IUCN does not formally consider any Mexican amphibian as extinct in the wild (i.e., no species listed as EX or EW), a recent assessment of the Mexican bio-diversity reports 29 species as extinct (Baena et al.2008; these species are indicated in Table3). Most of these 29 amphibian taxa are in the CR category of the IUCN (2010). The only exception isChiropterotriton mosaueriwhich is listed as DD. The main criteria for considering these amphibians as extinct by Baena et al. (2008) are the deep disturbance of habitat structure along with the lack of recent observations in spite of extensive field work (e.g., Pseudoeurycea aquatica; Wake and Campbell 2001). Nevertheless, these authors recognize that these extinctions have been suggested but not yet confirmed. Additionally, Ochoa-Ochoa et al. (2009) state that 9 microendemic taxa represent possible extinctions (also indicated in Table3). These species are considered as DD, EN, or CR by the IUCN (2010). Baena et al. (2008) and Ochoa-Ochoa et al. (2009) coincide in three species

(Lithobates pueblae, Pseudoeurycea praecellens, and Thorius infernalis) which gives a

total of 35 presumably extinct amphibians in Mexico. Without a doubt, these species are among those that deserve urgent attention. Biological surveys are needed to determine the existence and viability of their natural populations.

Clearly, the taxonomic pattern on the number and proportion of threatened species is not random. Certain families are experiencing higher rates of declines. For instance, more than 73% of the species in the family Plethodontidae (84 species) are considered as either VU, EN or CR. This fact is greatly significant, given that this family is widespread throughout much of the country and represents a large proportion of the Mexican fauna. Most of the threatened species in the Plethodontidae have very restricted geographic distributions and exhibit very specific micro-habitat requirements. As an example consider the species in the generaThoriusandChiropterotriton, which have 95.65 and 83.33% of threatened species, respectively (Parra-Olea et al.1999; Rovito et al.2009).

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agency (NOM-059-ECOL-2001, Secretarı´a de Medio Ambiente y Recursos Naturales

2002), we realized that the latter misses an important large number of species: 170 taxa from which 73 are threatened according to the IUCN. Also disturbing are the 126 amphibian species that are included into lower-risk conservation categories by the Mexican authorities in comparison with those assigned by the IUCN, as well as the low level of coincidence between the two lists (only 59 species are in coincident categories). These facts reflect two main issues. First, in Mexico the conservation status of amphibians is considered to be way better than their actual situation. Second, the official knowledge about the amphibian fauna in this country is markedly out of date. This is noticeable because in 1994 the number of species in Mexico recognized as threatened by the IUCN was strikingly low in comparison with the Mexican official list (Flores-Villela and Gerez

1994). Obviously, this is not the case anymore. The consequence is clear cut: within Mexico several threatened amphibians can be officially ignored, traded, and exploited.

Among the six factors that Collins and Storfer (2003) proposed as the main causes of amphibian declines, land use change is by far the most important affecting Mexican species (322 affected species; Table3). Agriculture, aquaculture, cattle breeding, logging, wood harvesting, and urban development are the most common activities in Mexico that promote habitat destruction and fragmentation (Merino-Pe´rez 2003). This has seriously impacted the diversity and abundance of amphibian populations. In several well-studied neotropical regions in Mexico, where habitat destruction has been evident, nowadays it is difficult to find a single amphibian, even though 30–35 years ago many plethodontid salamanders were encountered by hundreds (Parra-Olea et al. 1999; Lips et al. 2004; Rovito et al.2009). The xeric habitats in northern Mexico have also suffered from intense land use change, negatively affecting amphibian populations. For example, human development in the Baja California region is depleting freshwater and associated native habitats, critically threatening species such asAnaxyrus californicus andRana draytonii

(Lovich et al.2009). Similarly, increasing urbanization in the dry plains of Aguascalientes has reduced drastically the distribution range ofSmilisca dentata, a micro-endemic species considered as EN (Va´zquez-Dı´az and Quintero-Dı´az2005; Sigala-Rodrı´guez and Greene

2009). In fact, Ochoa-Ochoa et al. (2009) demonstrated that all amphibians endemic to Mexico have suffered the effects of habitat loss and 36 of such species have lost more than 50% of their original area of distribution.

Emerging infectious diseases represent the second most important threat to Mexican amphibians. It has long been recognized that new diseases caused by infectious agents such as bacteria, viruses, and fungi can cause the decline and extinction of amphibian popu-lations (Collins and Storfer 2003). One of the major pathogens presently known as responsible for several cases of decline of amphibians in the wild and in captivity is the fungusBatrachochytrium dendrobatidis(Bd; Berger et al.1998). Research on the presence and effects of this disease (chytridiomycosis) in Mexico is only starting. Nevertheless, a few studies have documented the presence ofBdin Mexican amphibian species, either by indirect evidence such as the loss of keratinized mouthparts in tadpoles (Lips et al.2004) or by direct examination of specimens (both adults and larvae) using real-time PCR assays (Frı´as-Alvarez et al. 2008). Several species (almost all endemic to Mexico) have been found positive withBd(e.g.,Agalychnis moreletii,Ambystoma altamirani,A. granulosum,

A. mexicanum,A. rivulare,A. velasci,Craugastor saltator,Hyla euphorbiacea,H. eximia,

Exerodonta melanomma, Lithobates megapoda, L. montezumae, L. neovolcanicus,