Risk assessment for the Mexican freshwater crayfish: the roles of diversity, endemism and conservation status: Risk assessment for the Mexican freshwater crayfish

Abstract

The freshwater fauna has been judged to be one of the most threatened biotic components in the world. In many tropical‐temperate freshwater habitats worldwide the largest invertebrates are crayfish, as is the case with the cambarid crayfish in Mexico. With 98% of endemic species, most of them with reduced distribution ranges, the Mexican crayfish have not been analysed to examine how diversity, endemism and threat are distributed.
A data set was analysed containing 1419 locality records for the 56 species of crayfish occurring in Mexico arranged in a 251 cell grid. Spatial autocorrelation analyses using Moran's I and G* were conducted; species richness, endemism and threat indices were calculated and mapped. An integrated risk score was derived from the two indices.
Spatial autocorrelation analyses revealed a pattern that significantly departs from a random arrangement. Moran's I showed a positive autocorrelation between cells that are less than 800 km apart; while G* analysis identified one hotspot of diversity. Four areas with high endemism and seven areas with intermediate endemism values were recognized. The western portion of the Trans‐Mexican Volcanic Belt, and some areas in the north are of special concern owing to the presence of threatened microendemic species.
The areas where more threatened species occur differ from those with high endemism values. This distinction makes evident that for species with low dispersal capabilities the areas with high endemism are the product of historical and geological events, while the areas with high numbers of threatened species are those where human activities have had a major impact. The integrated risk score, however, resulting from the combination of endemism and threat, peaks along the Trans‐Mexican Volcanic Belt and where it joins the Sierra Madre Oriental.
The integrated risk score proposed in this study, based on well known and frequently used indices in conservation biology, can be used with existing data to determine areas where crayfish species richness, endemism and threat peak to make conservation efforts more cost‐effective.
© 2016 The Authors. Aquatic Conservation: Marine and Freshwater Ecosystems published by John Wiley & Sons, Ltd.

Full text

Risk assessment for the Mexican freshwater crayfish: the roles of
diversity, endemism and conservation status
GEMA ARMENDÁRIZ, BENJAMÍN QUIROZ-MARTÍNEZ and FERNANDO ALVAREZ*
Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, México
ABSTRACT
1. The freshwater fauna has been judged to be one of the most threatened biotic components in the world. In
many tropical-temperate freshwater habitats worldwide the largest invertebrates are crayfish, as is the case with
the cambarid crayfish in Mexico. With 98% of endemic species, most of them with reduced distribution ranges,
the Mexican crayfish have not been analysed to examine how diversity, endemism and threat are distributed.
2. A data set was analysed containing 1419 locality records for the 56 species of crayfish occurring in Mexico arranged
in a 251 cell grid. Spatial autocorrelation analyses using Moran’s I and G* were conducted; species richness, endemism
and threat indices were calculated and mapped. An integrated risk score was derived from the two indices.
3. Spatial autocorrelation analyses revealed a pattern that significantly departs from a random arrangement.
Moran’s I showed a positive autocorrelation between cells that are less than 800 km apart; while G* analysis
identified one hotspot of diversity. Four areas with high endemism and seven areas with intermediate endemism
values were recognized. The western portion of the Trans-Mexican Volcanic Belt, and some areas in the north
are of special concern owing to the presence of threatened microendemic species.
4. The areas where more threatened species occur differ from those with high endemism values. This distinction
makes evident that for species with low dispersal capabilities the areas with high endemism are the product of
historical and geological events, while the areas with high numbers of threatened species are those where human
activities have had a major impact. The integrated risk score, however, resulting from the combination of
endemism and threat, peaks along the Trans-Mexican Volcanic Belt and where it joins the Sierra Madre Oriental.
5. The integrated risk score proposed in this study, based on well known and frequently used indices in
conservation biology, can be used with existing data to determine areas where crayfish species richness,
endemism and threat peak to make conservation efforts more cost-effective.
Copyright #2016 John Wiley & Sons, Ltd.
Received 28 July 2015; Revised 17 March 2016; Accepted 27 March 2016
KEY WORDS: crayfish; cambaridae; endemism; threat; Mexico; risk assessment
INTRODUCTION
The Cambaridae is one of the three families of
crayfish in the infraorder Astacidea, which,
together with the family Astacidae comprise the
superfamily Astacoidea. The family Parastacidae
is placed in its own superfamily (Ahyong et al.,
2011). Cambarid crayfish are strictly freshwater
*Correspondence to: Fernando Alvarez, Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México,
Apartado Postal 70-153, México 04510 D.F., México. Email: falvarez@unam.mx
Copyright #2016 John Wiley & Sons, Ltd.
AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. (2016)
Published online in Wiley Online Library
(wileyonlinelibrary.com). DOI: 10.1002/aqc.2671

crustaceans (Crandall and Buhay, 2008), with a
long history of inhabiting continental bodies of
water (Babcock et al., 1998). The ancestors of
modern-day cambarids already had burrowing
habits and occurred in similar conditions to
present-day ones (Hasiotis and Mitchell, 1993).
Several biogeographic patterns have been
described for cambarids, all founded in a well
accepted hypothesis that considers a centre of
diversity/origin for the group in the south-eastern
United States and a subsequent dispersal and
colonization of areas to the north and south.
Hobbs (1984) and France (1992) described the
progressive decline in the number of species of
crayfish departing from a nuclear area located
around 35° N in Texas, Louisiana, Mississippi,
Alabama and Georgia in the United States. With
a Nearctic origin for all the Cambaridae, the
Mexican crayfish fauna is thought to be the
product of a southward invasion of several
lineages of Procambarus along the Gulf of Mexico
versant and a posterior invasion of one lineage
within the genus Cambarellus through the palaeo-
lakes that existed in northern central Mexico
(Pedraza-Lara et al., 2012). The present
distribution of the Cambaridae in Middle America
also includes Belize, Guatemala, Honduras and
Cuba.
As a result, cambarid crayfish are not evenly
distributed in Mexico; their original distributions,
without considering introductions, are mainly in
three regions: (1) along the Gulf of Mexico
versant and in the Yucatan Peninsula; (2) along
the Trans-Mexican Volcanic Belt (TMVB); and
(3) along the Pacific slope in Jalisco, Nayarit and
Sinaloa, with a disjunct occurrence of one species
in Chihuahua (Villalobos, 1983; Alvarez et al.,
2012) (Figure 1(A)). Taxonomically, the 45 species
of Procambarus occur mostly in the first region,
with only two species in the second region; whereas
the 10 species of Cambarellus are distributed in
regions 2 and 3. Regarding introduced species, the
genus Orconectes is present in Mexico with one
species in Chihuahua, Orconectes virilis (Campos
and Contreras, 1985), whose native distribution is
in south-central Canada and the central United
States; and Procambarus clarkii, which, although
native to north-eastern Mexico and southern Texas
and Louisiana, has been introduced into Baja
California, Chihuahua, Durango, Nuevo León and
Chiapas (Torres and Alvarez, 2012). The two
species are considered in the analyses as their
distributions in Mexico are the result of range
expansions and introductions near the US–Mexico
border, confounding the original distribution
ranges. A third introduced species, the parastacid
Cherax quadricarinatus, which occurs in
Tamaulipas, San Luis Potosí and Morelos
(Bortolini et al., 2007; Alvarez et al., 2014), is not
considered in this study, since its distribution
pattern in Mexico is not related to any of the
biogeographic patterns and processes that are
examined here.
The Mexican crayfish fauna represents 8.7% of
the world’scrayfish diversity and 13.3% of the
total diversity of the family Cambaridae
(Crandall and Buhay, 2008). Fifty-three of the
56 species of crayfish recorded, except for
Orconectes virilis,Procambarus clarkii and
Procambarus pilosimanus, occur only in Mexico,
and most of them have small distribution
ranges with only four species (Cambarellus
montezumae, Procambarus acanthophorus, P.
clarkii, Procambarus llamasi) presenting large
distributions covering several states and basins.
This type of distribution creates a pattern in
which the co-occurrence of several rare species
in a given area can represent a hotspot, a
useful feature for conservation purposes.
Further, the conservation status of each species
can be considered in combination with its type
of distribution to give an idea of what areas
need more research.
The concepts of endemism and of areas of
endemism have generated much discussion, with
different definitions arising depending on the view
and type of analysis that is undertaken.
Endemism occurs when a taxon is distributed
only in a small area, and nowhere else (Anderson,
1994). In turn, an area of endemism is an area
where the distributions of two or more taxa
overlap regardless of their degree of relatedness
(Morrone, 1994). However, distributional overlap
may become biogeographically interesting if the
taxa involved have reduced distributions, making
the area of special interest for conservation and
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for study of the factors that shaped that
distribution, especially if the co-occurring taxa
are unrelated. The approach of using a grid to
group spatial data has been widely used to
organize species’distributional records, and at the
same time producing data sets that can be
analysed and compared. In this respect, several
spatial attributes of the distribution can be defined
(e.g. species richness, endemism, threat; Orme
et al., 2005) and congruence between these can be
explored in search of patterns that can be used to
construct biogeographical hypotheses.
Risk assessment models in conservation biology
focus mainly on populations not on groups of
species. Through the use of population growth
models that are combined with variables
describing a variety of threats the risk of decline or
extinction is assessed (Burgman et al., 1993). In
the present contribution the risk assessment
identifies areas characterized by high endemism
and threat values, thus involving groups of species
rather than individual populations.
This study had the aim of providing an analysis
of the distributional patterns of the Mexican
cambarid crayfish to define areas of high species
richness and endemism. The conservation status of
each species was included in the analysis to obtain
an integrated risk assessment. As several authors
Figure 1. Distribution of species of the family Cambaridae in Mexico: (a) data points used for the analysis (black circles) and selected geographic
features: TMVB (Trans-Mexican Volcanic Belt), SMO (Sierra Madre Oriental), SMOC (Sierra Madre Occidental); (b) species richness in 1°
latitude × 1° longitude grid, range 0 to 15 species; units of scale are number of species.
RISK ASSESSMENT FOR THE MEXICAN FRESHWATER CRAYFISH
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have suggested, it is becoming increasingly
important to know if hotspots for species diversity
coincide with those for endemism and risk, in
order to be able to plan conservation and research
goals more effectively (Kerr, 1997; Orme et al.,
2005).
METHODS
A database with 1419 locality records for the 56
species of crayfish occurring in Mexico was
compiled from published papers and from the
records in the National Crustacean Collection
(CNCR) of the Institute of Biology, Universidad
Nacional Autonoma de Mexico, in Mexico City.
All the records were checked to correspond to the
correct species and to the correct geographical
location.
A relatively coarse grid of 1° of latitude × 1° of
longitude was used to map the locality records
(Figure 1(B)). This grid size was selected because
it has been widely used to study different
biological groups in Mexico (Contreras-Medina
and Luna-Vega, 2007; Aguilar-Aguilar et al.,
2008; Contreras-MacBeath et al., 2014) and
standardizing grid size will allow future
comparisons. In addition, it gives a good degree
of resolution for the typical geographical range
that crayfish occupy, and because of the
geographical position of Mexico in contrast to
high latitude regions, grid-cell size does not vary
significantly between the southern and northern
portions of the country. The maps presented were
created using SAM software (Rangel et al., 2010).
Spatial autocorrelation
Spatial autocorrelation analysis (SAC) (Ord and
Getis, 1995; Getis and Ord, 1996; Getis, 1999) was
used to test for geographical clustering of cells
with high values of endemism. Spatial
autocorrelation occurs when the values of
variables collected at nearby locations are not
independent from each other (Tobler, 1970). In
order to test whether the geographical pattern of
endemism is essentially random, or whether there
are centres or ‘hotspots’of endemism, two
different SAC statistics, Moran’s I and G* (Getis
and Ord, 1996; Crisp et al., 2001) were used.
Moran’s I coefficient is one of the most commonly
used descriptors of spatial autocorrelation; it
computes the degree of autocorrelation (positive
or negative) between values of a variable as a
function of spatial lags. It varies from 1
(negative autocorrelation) to +1 (positive
autocorrelation), with values closer to zero in the
absence of autocorrelation or when there is a
random pattern (Legendre, 1993; Fortin et al.,
2002; Rangel et al., 2010). In this study, Moran’sI
was first calculated to test for any unusual pattern
of positive vs. negative autocorrelation using SAM
software (Rangel et al., 2010); G* was then
calculated to diagnose and rank hotspots (Getis,
1999). G* measures the degree of deviation of the
neighbourhood from the mean, irrespective of
whether this is positive or negative, and is
alternatively known as ‘hotspot analysis’(Getis
and Ord, 1996).
Species richness and endemism
Species richness was taken as the number of species
in each grid-cell. Endemism was assessed through a
simple index that considers in how many grid-cells a
species occurs; that is, a species occurring in only
one grid-cell will have a score of 1 for that cell. If
it occurs in two cells the score will be 0.5 for each
of the two cells, and so on (Crisp et al., 2001). If
several species co-occur in one grid-cell the scores
are added and the index of endemism (IE) is
obtained. If several (2–4) or many (>5) species co-
occur in one grid-cell then the index of endemism
can be very high and could be misrepresenting the
data; for example, if many widely distributed
species co-occur in one grid-cell. To correct for
this artefact a mean was calculated to get the
corrected weighted index of endemism (CWEI)
(Crisp et al., 2001; Linder, 2001). The implications
of variable spatial scale (grid size) and range size
(number of cells in which a species occurs) have
been discussed in detail (Hijmans and Spooner,
2001; Kier and Barthlott, 2001) with a general
conclusion that the level of endemism increases
with increasing scale, as more species with
restricted ranges tend to be included when cell size
increases (Laffan and Crisp, 2003).
ARMENDÁRIZ G. ET AL.
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Conservation status
The conservation status of the Mexican crayfish
available in the IUCN Red List of Threatened
Species (www.iucnredlist.org) was used. The
assessments were made in 2009 and represent the
most recent resource for this fauna. The Mexican
crayfish fall into one of seven categories. The
dwarf crayfish species Cambarellus alvarezi and
Cambarellus chihuahuae were declared extinct
(Alvarez et al., 2010a, b); however, they were
included in the analyses in order to maintain the
biogeographic information they represent. The
seven categories were assigned a numerical value:
0, data deficient (DD); 1, Least Concern (LC); 2,
Near Threatened (NT); 3, Vulnerable (VU); 4,
Endangered (EN); 5, Critically Endangered (CR);
6, Extinct (EX). Data Deficient species (16, 28.5%)
could not be assessed, so a value of 0 was
assigned to avoid increasing grid-cell scores when
defining areas of high risk. To avoid
overestimating the importance of one grid-cell
owing to the presence of many species with low
conservation categories, the scores were corrected
for number of species.
Integrated risk
The CWEI data and the conservation scores were
added to obtain an integrated risk assessment in
which the areas with rare and endangered species
could be identified. In contrast to previous
measures, the sum was not corrected for number
of species in each grid-cell.
RESULTS
Spatial autocorrelation
The SAC analysis using Moran’s I shows a positive
autocorrelation for pairs of points separated by up
to 800 km (Figure 2). Pairs of points separated by
800 km show no correlation, with a random
pattern, and as distances increase a negative
autocorrelation is found indicating more data
dispersion (Figure 2(A)).
The graphical representation of the analysis
based on the G* statistic shows the presence of a
hotspot of diversity, or an area of intense
clustering of species, in central Veracruz and
eastern Puebla. This tendency decreases in all
directions from the hotspot; however, areas of
intermediate intensity persist along the TMVB and
in central Chiapas (Figure 2(B)).
Species richness and endemism
The 56 species of crayfish from Mexico occur in 29
of the 32 states, being absent from Aguascalientes,
Tlaxcala and Guerrero; however, P. clarkii is an
introduced species in Baja California, Baja
California Sur, Sonora, Durango and Chiapas,
and O. virilis in Chihuahua. The results show
that crayfish are present in 94 (37.5%) of the 251
grid-cells. The highest number of species in one
grid-cell was 15 in an area located in central
Veracruz and north-eastern Puebla (20° N, 97°
W) (Figure 1(B)). Following this hotspot are
three grid-cells with eight species, two of which
are adjacent to the 15-species’grid-cell; in the
same geographic area, southern Veracruz, are two
grid-cells with seven species each (Figure 1(B)).
An area of intermediate species richness is
located along the TMVB where three grid-cells
have five species, two have four and two have
three species (Figure 1(B)). For the rest of the
distribution, 55 grid-cells have one species and 22
have two; that is one species or two species occur
in 82% of the total area occupied by crayfish in
Mexico.
Taxonomically, the 10 species of Cambarellus
are present in 31 grid-cells, 12.3% of the total for
Mexico and 33% of the total occupied by
crayfish; for Procambarus the numbers are 74 or
29.5% of the total for Mexico and 78.7% for the
total grid-cells occupied by crayfish. Species of
Cambarellus occur exclusively in 20 grid-cells,
while those of Procambarus occur in 63; both
genera co-occur in 11 grid-cells. The species with
the widest distribution is P. clarkii which occurs
in nine states occupying 25 grid-cells; while the
second most widely distributed species is
Cambarellus montezumae occurring in 11 states
and 19 grid-cells.
The areas of endemism defined by the IE
(Figure 3(A)), without considering the number of
species occurring per cell, coincide with the species
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richness distribution (Figure 1(B)). However, the
CWEI defines four areas, different from the
previous ones, as having the highest endemicity
values because one exclusive species occurs in
each of those grid-cells (Figure 3(B)). The species
involved in generating this pattern are, from north
to south: C. chihuahuae, recently declared extinct
(Alvarez et al., 2010c), which occupied a small
drainage system in central Chihuahua, south west
from the town of Villa Ahumada; Cambarellus
areolatus, from the environs of Parras, Coahuila;
Procambarus maya, known only from a few sites
inside the Sian Ka’an Nature Reserve in Quintana
Roo (Alvarez et al., 2007); and Procambarus
oaxacae, a stygobitic species from northern
Oaxaca.
Other areas with high levels of endemism, defined
by the presence of one to three species with reduced
ranges are in southern Nuevo León, where P.
clarkii is present in several sites and Cambarellus
alvarezi, also declared extinct (Alvarez et al.,
2010a), occurred in one spring at El Potosí; eastern
San Luis Potosí with the presence of Procambarus
cuevachicae,Procambarus toltecae and Procambarus
xilitlae; central Veracruz, where there are 10 species
of Procambarus in three grid-cells (P. hoffmanni,P.
contrerasi, P. erichsoni, P. caballeroi, P. xochitlanae,
P. ortmanni, P. riojai, P. cuetzalanae, P.
teziutlanensis, P. tlapacoyanensis); southern Sinaloa
and central Nayarit, where Cambarellus occidentalis
and C. montezumae occur; and the border region
between southern Veracruz and northern Oaxaca,
Figure 2. Graphical representation of the spatial autocorrelation analyses performed with the distributional data of Mexican cambarid crayfish: (a)
Moran’s I values estimated across a distance scale, see text for explanation; (b) G* shows significant spatial clustering of high values that identifiya
statistically significant hotspot; units of scale are G* values, low values = no association of neighbouring grid-cells, high values = strong association of
neighbouring grid-cells.
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with four species of Procambarus:P. citlaltepetl, P.
cavernicola, P. acanthophorus and P. veracruzanus.
Conservation status
Similar to the results obtained for endemism, one
grid-cell in central Veracruz has the highest
conservation value because 15 species occur in
that area (Figure 4(A)). Another two areas with
high incidence of threatened species are the border
area between Michoacán and Jalisco, where five
species occur (Cambarellus chapalanus, NT;
Cambarellus patzcuarensis, EN; Cambarellus
prolixus, CR; Procambarus bouvieri, EN;
Procambarus digueti, EN); and southern Veracruz
and northern Oaxaca, where another five species
of Procambarus are threatened (P. atemacoensis,
CR; P. cavernicola, VU; P. citlaltepetl, VU; P.
vazquezae, NT; P. zapoapensis, NT) (Figure 4(A)).
However, if conservation scores are corrected for
number of species, then the areas of high
importance change (Figure 4(B)). A hotspot for
conservation appears in southern Coahuila where
C. areolatus has been assessed as CR. Other areas
with high importance for crayfish conservation
are: southern Nuevo León where C. alvarezi, now
extinct, occurred; the border area between
Michoacán and Jalisco remains as an important
region for crayfish conservation; and southern San
Luis Potosí, where Procambarus roberti (EN) is
distributed (Figure 4(B)).
Integrated risk
The combined analysis of CWEI and corrected
conservation status –that is the integrated risk
Figure 3. Endemism of the Mexican cambarid crayfish: (a) values of the simple endemism index, scale range 0–7.5; (b) corrected weighted endemism
index, scale range 0–1.
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assessment –identifies a hotspot in southern
Coahuila, a large area along the TMVB from
Michoacán to Hidalgo and Puebla, and a third
area in southern Nuevo León (Figure 5). In these
areas species with reduced geographic ranges
occur, that are also of conservation concern.
Concordance between endemism and threat
Correlation analysis was used to test if hotspots for
endemism and threat were concordant
geographically. Species richness in each grid cell
was used as a surrogate for geographical
distribution. The correlation of species richness vs.
endemism was significant (Pearson, r = 0.37,
P<0.0001) while that of species richness vs.
threat was not (Pearson, r = 0.05, P>0.05).
DISCUSSION
Distribution pattern and species richness
In contrast to highly vagile animals (i.e. fishes,
birds, mammals), the distribution patterns shown
by crayfish are relatively fixed spatially and may
reflect historical processes of speciation and
colonization. Pedraza-Lara et al.(2012)found
the phylogenetic structure of the Mexican
Cambarellus to be congruent with their
geographic distribution, indicating that geological
events have had an important role in shaping
their current distribution ranges. Mexican
crayfish are distributed primarily along the Gulf
of Mexico slope, occupying an area delimited by
the Sierra Madre Oriental and along the TMVB,
producing, where the two physiographic features
Figure 4. Threat values derived from the IUCN assessments of the Mexican cambarid species: (a) individual species scores added, scale range 0–40; (b)
threat scores corrected for number of species present in each grid-cell, scale range 0–6.
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join, a hotspot of species richness (Figure 1(B)).
While the Sierra Madre Oriental may have
served as the invasion route for crayfish from the
southern United States to Mexico, through
intense vicariance events that can be seen in the
latitudinal succession of genera and species from
north to south, the TMVB represents at different
times both a corridor that connects the Gulf of
Mexico and Pacific lowlands and a barrier.
Alvarez et al. (2012) discussed the hypothesis
(Rodríguez, 1986) on the competitive exclusion of
crayfish by pseudothelphusid crabs in central
Mexico, in border areas between the Neotropical
and the Neartic regions, by which freshwater crabs
would have outcompeted and excluded crayfish in
areas where they co-occur. Alvarez et al. (2012)
showed that both distribution patterns, of crayfish
and crabs, are the result of independent processes,
mainly geological events, that have occurred at
different times, and that both coexist in a number
of areas throughout central Mexico.
Another important consequence of the relatively
reduced mobility of crayfish and absence of
migrations and dispersing larval stages, is that
they are more vulnerable to disturbances since
typically they are established over reduced ranges
encompassing one or two grid-cells. In several
instances, where the species is known only from
the type locality, the distribution area could be less
than 100 km
2
(Alvarez et al., 2010c). Only four
species present in Mexico have large distribution
ranges, while the remaining 52 species can be
considered as ‘rare’with very restricted
distribution ranges. This type of distribution could
contribute to the fact that already two species
have been declared extinct.
Using drainage basins as the units for analysis
Quiroz-Martínez et al. (2014) found concordant
distribution patterns of freshwater taxa in Mexico
including helminth parasites of freshwater fishes,
fishes (Poecilidae) and crustaceans (Palaemonidae
and Pseudothelphusidae) which defined two
different faunas, one for the Pacific slope and one
for the Gulf of Mexico slope. Although the groups
analysed by Quiroz-Martínez et al. (2014) are
mainly Neotropical, in contrast to cambarid
crayfish which have a Neartic origin, the Gulf of
Mexico slope created by the Sierra Madre Oriental
represents an important corridor for the
diversification of freshwater organisms.
Despite the fact that almost all crayfish species
occurring in Mexico are endemic to the country
and that many of them have reduced distribution
ranges, only one species, Procambarus regiomontanus,
is listed in the Nom-059-Semarnat-2010 as
Critically Endangered, which is the official
Mexican Red List (Alvarez and Villalobos, 2015).
Although Mexico has a nature reserve system
composed of 174 reserves, only 17 (30%) species of
crayfish occur in 21 (12%) of them showing that
freshwater fauna, especially invertebrates, have not
been considered in their selection. In light of this
Figure 5. Integrated risk scores for the Mexican cambarid species, obtained by combining endemism and threat, scale range 0–7.
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precarious situation, new proposals based on the
analysis of distribution patterns should be put
forward to improve the conservation of this fauna.
Endemism
Endemism is a scale-dependent concept that needs
to be defined for every study. Fifty-three out of the
56 species (95%) distributed in Mexico are
endemic to the country. The use of the 1°
longitude × 1° latitude grid, that creates cells each
covering approximately 11 500 km
2
in central
Mexico, is useful to interpret general patterns at a
country-wide scale, although the distribution
ranges of several species of crayfish are smaller.
Thus, a finer scale will be needed in future studies
to define the extension of the areas of endemism
for this group. The results of this study show that
primary areas of endemism are produced by rare
species occurring alone in one grid-cell (Figure 3
(B)) and secondary areas have two or three rare
species co-occurring in one grid-cell, except for the
outstanding regions in central Veracruz and
eastern Puebla where the hotspots of species
richness are located.
An important advantage of the use of a grid to
describe distributions is that several other studies
covering Mexico have used the same approach
and grid size allowing for direct comparisons
between studies. The areas of endemism for
crayfish coincide partially with those for
freshwater fishes (Contreras-MacBeath et al.,
2014), especially in northern Mexico in
Chihuahua, southern Coahuila and southern
Nuevo León, where dry conditions prevail and
both groups tend to use the same bodies of water.
Freshwater fishes also represent hotspots for
endemism in southern Oaxaca and central Baja
California Sur where crayfish do not occur, and
have areas of endemism of secondary importance
along the TMVB as crayfish do (Contreras-
MacBeath et al., 2014). Helminth parasites of
freshwater fishes have two areas of high
endemism, one in central Durango and a second
one in central Mexico, including the Valley of
Mexico, and the State of Mexico, which are not
concordant with those of crayfish (Aguilar-Aguilar
et al., 2008).
Conservation and distribution
Based on the IUCN assessments, the areas with
high importance for crayfish conservation in
Mexico agree partially with the results obtained
here for species richness and endemism (Figures 1
(B), 3(B), 4(B)). The species richness hotspot in
central Veracruz and eastern Puebla remains as an
important area that has to be considered for future
biogeographic studies and the establishment of
nature reserves; however, southern Coahuila and
the TMVB are relevant also since both areas have
high endemism and conservation values. The
central Veracruz and eastern Puebla diversity
hotspots were also identified by Richman et al.
(2015), who analysed the major threats for crayfish
worldwide.
The identification of areas that represent
hotspots for both diversity and endemism in a
given group of organisms is relevant since there
are opposing views about the frequency and
causes of occurrence of this phenomenon,
particularly in vagile organisms (Jetz et al., 2004;
Orme et al., 2005). For the Mexican freshwater
crayfish the congruence of these criteria is
important for assigning conservation priorities,
but also point to a historical perspective, rather
than a contemporary one, to explain the observed
distribution patterns. Thus, intense speciation in
the confluence of the Sierra Madre Oriental and
the TMVB might have occurred from the late
Miocene onwards, when ancestral stocks were
already present in the area and the orogenesis in
the region caused by intense vulcanism was under
way (Velasco-de León et al., 2007; Pedraza-Lara
et al., 2012).
Hotspots for endemism and threat are not
concordant geographically, as can be seen in
Figures 3(B) and 4(B). The fact that species
richness is correlated with endemism suggests that
historical or geological events have created areas of
high endemism through intense vicariance events in
areas of complex orography. In turn, the lack of
correlation between species richness and threat
points to human induced changes as the factor that
has had an impact on crayfish populations.
Crayfish are threatened in many parts of the
world mainly because of the presence of invasive
ARMENDÁRIZ G. ET AL.
Copyright #2016 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2016)

alien species, pathogens and habitat modification
(Whiterod et al., 2015; Alvarez and Villalobos,
2015; Chucholl and Schrimpf, 2016; Füreder,
2015). A variety of conservation and restocking
strategies have been devised to help stop the
decline of crayfish populations in many parts of
the world; although of prime importance, these
studies and practices target individual species,
many of which have been assessed in regional and
global red lists (Kozák et al., 2011). However, at
the other end of the spectrum is the need to
identify regions or basins containing as many rare
and threatened crayfish species as possible to make
conservation efforts cost-effective. Even when
more studies are needed to validate this approach,
we have devised a risk score that could be used
easily to define areas with high diversity,
endemism and conservation value.
ACKNOWLEDGEMENTS
The first author gratefully acknowledges the
support of a CONACYT scholarship for her
Master’s studies. We thank CONACYT for
funding the postdoctoral fellowship of B. Quiroz-
Martínez held in the National Crustacean
Collection of the Institute of Biology, UNAM,
under grant 155644 (546) awarded to F. Alvarez.
Comments made by the editor and two reviewers
greatly improved the final version of the
manuscript.
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