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Received: 22 January 2025
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Published: 21 March 2025
Citation: Durán-Rodríguez, O.Y.;
García-Ávila, D.A.; Valencia-Espinosa,
J.A.; Arroyo-Reséndiz, E.; Torres-Olvera,
M.J.; Ramírez-Herrejón, J.P.
Environmental Factors Influencing the
Establishment of the Invasive
Australian Redclaw Crayfish (Cherax
quadricarinatus) in a Biosphere Reserve
on the Central Mexican Plateau. Life
2025,15, 508. https://doi.org/
10.3390/life15040508
Copyright: © 2025 by the authors.
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Article
Environmental Factors Influencing the Establishment of the
Invasive Australian Redclaw Crayfish (Cherax quadricarinatus)
in a Biosphere Reserve on the Central Mexican Plateau
Omar Y. Durán-Rodríguez
1
, Daniel A. García-Ávila
2
, J. Andrés Valencia-Espinosa
3
, Eugenio Arroyo-Reséndiz
4
,
Martín J. Torres-Olvera 5,* and Juan P. Ramírez-Herrejón 6
1Institutional Doctoral Program in Biological Sciences, Facultad de Ciencias Naturales, Campus-Juriquilla,
Universidad Autónoma de Querétaro, Av. de las Ciencias, Juriquilla, Santiago de Querétaro 76230,
Querétaro State, Mexico; oduran22@alumnos.uaq.mx
2Institutional Master’s Program in Biological Sciences, Facultad de Ciencias Naturales, Campus-Juriquilla,
Universidad Autónoma de Querétaro, Av. de las Ciencias, Juriquilla, Santiago de Querétaro 76230,
Querétaro State, Mexico; dagarciabio@gmail.com
3
Facultad de Ciencias Naturales, Campus-Juriquilla, Universidad Autónoma de Querétaro, Av. de las Ciencias,
Juriquilla, Santiago de Querétaro 76230, Querétaro State, Mexico; jose.valencia@uaq.mx
4Escuela de Bachilleres, Concá Campus, Universidad Autónoma de Querétaro, Valle Agrícola, Concá,
Arroyo Seco 76490, Querétaro State, Mexico; eugenio.arroyo@uaq.mx
5Escuela de Bachilleres, Jalpan Campus, Universidad Autónoma de Querétaro, Boulevard Policarpo Olvera,
Fracc. El Coco, Jalpan de Serra 76490, Querétaro State, Mexico
6Water and Soil Quality Laboratory, SECIHTI-Universidad Autónoma de Querétaro, Carretera a
Chichimequillas, Ejido Bolaños, Santiago de Querétaro 76140, Querétaro State, Mexico;
ramirezherrejon@gmail.com
*Correspondence: martin.jonatan.torres@uaq.mx
Abstract: Crustaceans are among the most successful taxonomic groups in invasions world-
wide. Humans can facilitate these invasions through introductions and disturbances in
habitats. The Australian redclaw crayfish (Cherax quadricarinatus) is an invasive species
with significant global ecosystem impacts. This species inhabits the Sierra Gorda Biosphere
Reserve, in the Central Mexican Plateau. We hypothesize that environmental degradation
facilitates the establishment and expansion of invasive crayfish. Seven sites along the Santa
María River, within the reserve buffer zone, were assessed for seven months in 2023. We an-
alyzed the abundance and density of the Australian redclaw crayfish in correlation with the
environmental quality of the habitat. The results confirm that the establishment and spread
of crayfish populations are related to water quality degradation and habitat alteration. The
associated variables include increased total dissolved solids, greater substrate embedment,
and degraded conditions on stream banks. Furthermore, the inverse relationship between
the abundance of Australian redclaw crayfish and macroinvertebrate richness reinforces
the hypothesis that more diverse native communities reduce the success of invaders. This
study highlights the urgent need to implement management strategies focused on habitat
restoration and the control of reproductive populations through the extirpation of mature
individuals as critical measures for controlling the establishment and expansion of the
invasive Australian redclaw crayfish.
Keywords: crustacean; exotic species; environmental degradation; river; protected natural area
1. Introduction
Invasive species pose a significant threat to biodiversity, leading to shifts in community
structure, alterations to ecosystem functioning, and disruptions in the delivery of ecosystem
Life 2025,15, 508 https://doi.org/10.3390/life15040508
Life 2025,15, 508 2 of 23
services [
1
,
2
]. Their impact on ecosystem processes often arises from predation, parasitism,
disease transmission, and habitat modification, while ecosystem services are affected by
public health risks and economic damage [
3
,
4
]. Freshwater ecosystems are highly susceptible
to anthropogenic disturbances that promote biological invasions [
5
–
7
], with the introduction
of non-native species being one of the most critical threats to these habitats [8,9].
Human activities favor biological invasions, not only because of the extirpation of
species from their native range and their introduction in new areas [
6
] but also because
environmental degradation due to human activities can facilitate biological invasions.
Disturbances typically lead to the reconfiguration and homogenization of available space
(habitat) and resources, creating ’new vacancies’ in freshwater ecosystems for alien species
with higher tolerance to environmental stressors and greater adaptability to altered con-
ditions [
10
,
11
]. On the other hand, habitat complexity and heterogeneity can enhance
freshwater ecosystems’ resistance to biological invasions by providing refuge for native
fauna from predation or competition with invasive species [12].
Among freshwater invaders, crustaceans represent one of the most successful taxo-
nomic groups of invasive species globally [
13
]. The Australian redclaw crayfish (Cherax
quadricarinatus von Martens, 1868), a freshwater decapod crustacean, is native to Queens-
land and the Northern Territory of Australia, as well as southern Papua New Guinea [
14
,
15
].
This species has been introduced into more than 10 countries, including Indonesia, South
Africa, Eswatini, China, and Zambezi Basin [
16
–
19
], for cultivation as an alternative food
resource [20,21].
The Australian redclaw crayfish is considered a highly invasive species [
22
] that
significantly impacts invaded ecosystems. It competes with native species for shelter and
food [
14
,
23
–
25
]. Likewise, this species has a euryphagous feeding strategy that targets a
wide range of aquatic organisms, including fish, amphibians, invertebrates, and aquatic
plants [
26
]; thus, as generalist feeders, they can disrupt the ecosystem at all levels of the food
web [
27
]. Additionally, the Australian redclaw crayfish is a potential vector for pathogens,
including fungi, viruses, and bacteria, which pose a threat to native fauna [20,28–32].
The Sierra Gorda Biosphere Reserve (SGBR) stands out as one of Mexico’s most
significant protected areas, hosting a wide variety of habitats that support diverse biotic
communities, including both terrestrial and semi-aquatic vertebrates [
33
]. The SGBR is
divided into different protection zones, such as buffer zones and core areas [
34
,
35
]. The
core zones contain the most well-preserved ecosystems, which remain nearly pristine and
provide refuge for species of flora and fauna that require special protection [
34
,
35
]. In the
Santa Maria River and some of their affluents near a core zone of the SGBR, the Australian
redclaw crayfish has recently been registered, representing a new threat to biodiversity in
this biosphere reserve [36].
We hypothesize that environmental degradation, characterized by altered water qual-
ity and habitat disruption, facilitates the establishment and spread of the invasive redclaw
crayfish (Cherax quadricarinatus) in the river ecosystem within the biosphere reserve. To test
this hypothesis, we analyze the association between the density and abundance of redclaw
crayfish and indicators of environmental degradation, including physicochemical water
variables and indicators of river habitat conditions, biological integrity, and riparian quality.
This knowledge is essential for understanding the Australian redclaw crayfish’s invasion
dynamics and assessing and developing management strategies to reduce the spread and
potential impacts within the SGBR and other regions.
2. Materials and Methods
The SGBR is a protected area in the Central Plateau of Mexico with an approximate
extent of 383,500 ha. The SGBR occupies most of the Sierra Gorda, which is part of the
Life 2025,15, 508 3 of 23
Sierra Madre Oriental and covers the northern half of the state of Querétaro, the west of the
state of Guanajuato, and a small portion of the state of San Luis Potosí. The SGBR belongs
to the Pánuco River Hydrologic Region, which has two basins: Moctezuma River Basin,
which includes the Moctezuma River, Extóraz River, and Axtla River, and Tamuín River
Basin, which includes the Tampaón or Tamuín River, Santa María River, Verde River, and
La Tinaja River [33,35].
We sampled seven sites: five along the Santa María River, one at Concá Spring, and
another on the Ayutla River. The latter two water bodies are both tributaries of the Santa
María River, which forms the main course of the Tamuín Sub-basin. All of these sites are
located in the Arroyo Seco municipality, in Queretaro State, in the SGBR (Figure 1). These
sites are located within the SGBR buffer zone, less than 10 km upriver from one of the core
zones of the reserve. The seven sampling sites within the Sierra Gorda Biosphere Reserve
represent a gradient of environmental conditions, ranging from minimally impacted natural
areas to highly disturbed habitats. Sites such as Ayutla (AYU), Puente de las Mesas
(PM), and Downstream of Jalpan River (DRJ) exhibit well-preserved riparian corridors
with diverse native vegetation, minimal human impact, and substrates dominated by
larger particles like megalithal and macrolithal materials, providing a complex habitat
structure. In contrast, sites like Concá Manantiales (CM) and El Salitrillo (SAL) are highly
impacted by human activities, including tourism and sand dredging, with severely altered
riparian zones, reduced vegetation cover, and substrates dominated by fine sediments
(e.g., psammal and pelal), reflecting degraded habitat conditions. Intermediate conditions
are observed at sites like El Higuerón (HIG) and Downstream of Adjuntas (DA), where
moderate human impacts coexist with partially fragmented riparian vegetation and a
mixed substrate composition. These environmental differences allowed for the assessment
of the Australian redclaw crayfish distribution across varying habitat conditions (Table 1).
Life 2025, 15, x FOR PEER REVIEW 3 of 25
2. Materials and Methods
The SGBR is a protected area in the Central Plateau of Mexico with an approximate
extent of 383,500 ha. The SGBR occupies most of the Sierra Gorda, which is part of the
Sierra Madre Oriental and covers the northern half of the state of Querétaro, the west of
the state of Guanajuato, and a small portion of the state of San Luis Potosí. The SGBR
belongs to the Pánuco River Hydrologic Region, which has two basins: Moctezuma River
Basin, which includes the Moctezuma River, Extóraz River, and Axtla River, and Tamuín
River Basin, which includes the Tampaón or Tamuín River, Santa María River, Verde
River, and La Tinaja River [33,35].
We sampled seven sites: five along the Santa María River, one at Concá Spring, and
another on the Ayutla River. The laer two water bodies are both tributaries of the Santa
María River, which forms the main course of the Tamuín Sub-basin. All of these sites are
located in the Arroyo Seco municipality, in Queretaro State, in the SGBR (Figure 1). These
sites are located within the SGBR buffer zone, less than 10 km upriver from one of the core
zones of the reserve. The seven sampling sites within the Sierra Gorda Biosphere Reserve
represent a gradient of environmental conditions, ranging from minimally impacted nat-
ural areas to highly disturbed habitats. Sites such as Ayutla (AYU), Puente de las Mesas
(PM), and Downstream of Jalpan River (DRJ) exhibit well-preserved riparian corridors
with diverse native vegetation, minimal human impact, and substrates dominated by
larger particles like megalithal and macrolithal materials, providing a complex habitat
structure. In contrast, sites like Concá Manantiales (CM) and El Salitrillo (SAL) are highly
impacted by human activities, including tourism and sand dredging, with severely altered
riparian zones, reduced vegetation cover, and substrates dominated by fine sediments
(e.g., psammal and pelal), reflecting degraded habitat conditions. Intermediate conditions
are observed at sites like El Higuerón (HIG) and Downstream of Adjuntas (DA), where
moderate human impacts coexist with partially fragmented riparian vegetation and a
mixed substrate composition. These environmental differences allowed for the assess-
ment of the Australian redclaw crayfish distribution across varying habitat conditions
(Table 1).
Figure 1. Geographic location of study area and study sites. SGBR = Sierra Gorda Biosphere Reserve;
1 = Puente de las Mesas; 2 = Concá Manantiales; 3 = El Higueron; 4 = El Salitrillo; 5 = Ayutla; 6 =
Downstream of Adjuntas; 7 = Downstream of Jalpan River.
Figure 1. Geographic location of study area and study sites. SGBR = Sierra Gorda Biosphere Reserve;
1 = Puente de las Mesas; 2 = Concá Manantiales; 3 = El Higueron; 4 = El Salitrillo; 5 = Ayutla;
6 = Downstream of Adjuntas; 7 = Downstream of Jalpan River.
Australian redclaw crayfish specimens were collected using funnel traps with a single
cone-shaped inlet (dimensions: 450 mm height, 300 mm diameter; mesh size: 5 mm) baited
with fish. We set six traps at each site, with three placed in areas with current and three
in pool zones. After 24 h, we collected the captured organisms. Sampling was conducted
Life 2025,15, 508 4 of 23
monthly in April, June, July, August, September, October, and November of 2023. Captured
specimens of Australian redclaw crayfish were euthanized by placing them in slurry ice and
then preserved in an 80% ethyl alcohol solution. Native crustaceans (i.e., Macrobrachium sp.)
were measured, weighed, and released.
Table 1. Habitat description of sampling sites in Sierra Gorda Biosphere Reserve, Central Mexican
Plateau. Sites: PM = Puente de las Mesas; HIG = El Higueron; SAL = El Salitrillo; DA = Downstream
of Adjuntas; DRJ = Downstream of Jalpan River; CM = Concá Manantiales; AYU = Ayutla. Substrate
size: megalithal (>40 cm); macrolithal (20–40 cm); mesolithal (6–20 cm); microlithal (2–6 cm); akal
(small gravel); psammal (sand); pelal (slit, sludge). Habitat description: HMU = hydromorphological
units; HS = hydraulic signature. Characterization of hydraulic signature: shallow (<0.5 m), wading
(0.5–1 m), deep (>1 m); slow (<25 cm/s), flows (25–50 cm/s), fast (>50 cm/s).
Site Shore Line Riparian Vegetation Substrate Habitat Main Impacts
PM Banks significantly
modified by human action.
Average width of riparian
corridor significantly altered
by human action. Riparian
vegetation appears in small
patches covering less than
30% of segment length.
Particle stratification that
provides diversity of
niche space.
Akal (60%), psammal (20%),
macrolithal (10%), mesolithal
(5%), megalithal (3%),
microlithal (2%).
Overhanging vegetation,
canopy cover shading (3%),
submerged vegetation,
woody debris, undercut
banks, and boulders.
HMU:
glide (80%), ruffle (10%), run
(5%), and backwater (5%).
HS:
shallow fast (75%), wading
fast (10%), shallow slow (5%),
wading flows (5%), shallow
flows (3%), and shallow
slow (2%).
Natural area with
moderate human impact
(road, livestock,
and tourism).
HIG Banks moderately
modified by human action
in their form and processes.
Average width of riparian
corridors significantly
reduced by human action,
with average width less than
1 active channel width.
Riparian corridor moderately
fragmented with 50% of
natural coverage including
several strata.
Particles (25–30%)
surrounded by fine sediment.
Mesolithal (40%), psammal
(40%), microlithal (10%),
akal (10%).
Overhanging vegetation,
canopy cover shading (3%),
shallow margins, undercut
banks, boulders, and
woody debris.
HMU:
pool (40%), run (40%), ruffle
(10%), and backwater (10%)
HS:
wading flows (40%), deep
slow (40%), shallow fast
(10%), and shallow
slow (10%).
Natural area with
minimal human impact.
SAL
Banks severely altered by
human action. Channel
margins connected to
urbanized areas and roads.
Average width of riparian
corridors severely reduced
due to human action. Few
riparian woody species;
herbaceous communities
predominate due to
human actions.
Particles (>75%) surrounded
by fine sediment.
Psammal (90%), mesolithal
(5%), macrolithal (5%).
Overhanging vegetation,
canopy cover shading (2%),
undercut banks, and
woody debris.
HMU:
glide (95%) and ruffle (5%).
HS:
shallow slow (90%), shallow
flows (5%), and shallow
fast (5%).
Area impacted by sand
dredging and roads.
DA Banks moderately
modified by human action
in their form and processes.
Moderately restricted by
human action. Average width
of around 3 times active
channel width. Riparian
corridors moderately
fragmented with 60% of
natural coverage including
several strata.
Particles (30–40%)
surrounded by fine sediment.
Megalithal (70%), psammal
(20%), macrolithal (10%).
Overhanging vegetation,
canopy cover shading (5%)
boulders, and
shallow margins.
HMU:
run (50%), rapid (25%), pool
(20%), and backwater (5%).
HS:
wading fast (40%), deep fast
(25%), deep flows (15%),
wading flows (15%), and
shallow slow (5%).
Natural area with
moderate human impact
(tourism, livestock).
DRJ Banks moderately
modified by human action
in their form and processes.
Continuity and coverage of
riparian corridor in natural
conditions including a mix of
species corresponding to
native vegetation associations
of river segment, with
different strata.
Particle stratification that
provides diversity of
niche space.
Mesolithal (70%), macrolithal
(20%), pelal (10%).
Overhanging vegetation,
canopy cover shading (50%),
shallow margin both left and
right, submerged vegetation,
undercut banks, and boulders.
HMU:
run (60%), rapid (20%), pool
(10%), and fast run (10%).
HS:
wading flows (60%), shallow
fast (20%), wading fast (10%),
deep slow (5%), and deep
flows (5%).
Natural area with
minimal human impact.
Life 2025,15, 508 5 of 23
Table 1. Cont.
Site Shore Line Riparian Vegetation Substrate Habitat Main Impacts
CM Banks severely altered by
human action.
Average width of riparian
corridor significantly altered
by human action. Riparian
vegetation is reduced to
isolated trees or shrubs,
leaving large open areas),
including only one stratum.
Particles (>75%) surrounded
by fine sediment.
Microlithal (50%), debris
(20%), pelal (15%), psammal
(5%), akal (5%),
mesolithal (5%).
Overhanging vegetation,
canopy cover shading (70%),
undercut banks, and
submerged vegetation.
HMU:
pool (55%), glide (40%), and
riffle (5%).
HS:
wading slow (55%), wading
flows (40%), and shallow
fast (5%).
Highly impacted by
tourism activities.
AYU Banks moderately
modified by human action
in their form and processes.
Moderately restricted by
human action. In valley
surrounded by vegetation.
Particle stratification that
provides diversity of
niche space.
Megalithal (60%), macrolithal
(20%), mesolithal (15%),
microlithal (5%).
Overhanging vegetation,
canopy cover shading (20%),
shallow margin left, boulders,
and woody debris.
HMU:
glide (60%), pool (20%), rapid
(10%), and run (10%).
HS:
wading flows (60%), wading
slow (20%), wading fast
(10%), and deep slow (10%).
Natural area with
moderate human
impact (tourism).
The identification of the specimens was determined using the diagnosis described by
Arias-Rodríguez and Torralba-Burrial (2021) [
37
]. All specimens were weighed, measured,
and sexed before preservation in a solution of 80% alcohol. The total length (TL) and
carapace length (CL) were measured. The crayfish were placed on filter paper for several
minutes to remove excess water and then weighed to the nearest 0.01 g, and we measured
the total length (TL) and carapace length (CL) with calipers to the nearest 0.01 cm, following
Rodriguez et al. (2014) and Sedik et al. (2019) [
38
,
39
]. The density of Cherax quadricarinatus
was estimated using two complementary approaches: Global Density and Average Density.
Global Density represents the total number of individuals captured per trap-day across
the entire sampling period (7 months). Considering that six traps were deployed per site
during each sampling event and each sampling lasted 24 h, the total trapping effort per
site was 42 trap-days (6 traps
×
7 sampling events). It was calculated as follows: total
abundance (all sampling events)/42 trap-days. This metric reflects the overall capture rate
standardized per day of trapping. Average Density refers to the mean density per sampling
event by sampling. It was calculated by dividing the number of crayfish captured during
each 24 h sampling event by the 42 trap-days used, then averaging these values across
the seven sampling events at each site. The formula was as follows: average (abundance
per sampling event/42 trap-days). This provides an estimation of the average number of
crayfish captured per day.
Spawning-capable individuals were identified based on a combination of morphologi-
cal and reproductive characteristics. Females carrying visible eggs were directly classified
as spawning-capable. For individuals without visible eggs, maturity was assessed using
weight thresholds and the presence of secondary sexual characteristics. Juveniles were
defined as individuals weighing between 6 and 49 g, following commercial aquaculture
classifications [
40
], while individuals weighing approximately 90 g or more were consid-
ered mature, consistent with the sexual maturity range reported for Cherax quadricarinatus
(56.69–85.04 g) [
41
]. In males, secondary sexual characteristics included the presence of a
distinctive red soft patch on the outer surface of the propodus of the claw, genital open-
ings (gonopores) at the base of the fifth pereiopods, and the presence of the appendix
masculina [
42
]. In females, maturity was confirmed by the presence of genital openings
at the base of the third pereiopods. Additionally, intersex individuals, which may dis-
play mixed characteristics (e.g., one or two appendix masculina and both pairs of genital
openings), were identified but categorized separately due to their ambiguous reproduc-
Life 2025,15, 508 6 of 23
tive status [
36
]. This combination of morphological characteristics and weight thresholds
allowed for reliable identification of spawning-capable individuals in the field.
We evaluated the physical, chemical, and biological conditions in April 2023 during
the dry season when conditions were more stable [
43
]. This evaluation was conducted for
each study site on a river section to standardize the sampling effort. The river section was
equivalent to five times the river width, following the criteria of Mexican Standard NMX-
AA-159-SCFI-2012 [
44
], which establishes the procedure for the determination of ecological
flow in river basins. The physical condition of the habitat was assessed using a Visual-Based
Habitat Assessment (VBHA) following the methodology of Barbour et al. (1999) [
45
], which
includes 10 variables related to physical elements and processes, such as sinuosity, substrate
and bank materials (epifaunal substrate/available cover, embeddedness, velocity/depth
combinations), sediment retention areas (sediment deposition, channel flow status, channel
alterations, frequency of riffles), riparian vegetation conditions (bank vegetative protection),
riparian zone conditions (bank stability), and floodplain status (riparian vegetative zone
width) (Table 2).
Table 2. Environmental variables of sampling sites in the Sierra Gorda Biosphere Reserve, Central
Mexican Plateau. For variable values, the RQI (values of 1–150) is the sum of the variables RW*, LC*,
CS*, ADR, BC, LAC, and VC. Each variable is evaluated on a scale of “1 to 15”, where “1” represents
bad quality and “15” very good quality. For variables marked with “*”, each margin is assessed
separately, representing the condition of each side, and their combined score reflects the total score
(values of 1–30). The VBHA (values of 1–200) is the sum of the variables EPS, EMB, V/D, SD, CFS,
CA, FR, BS*, and VP*, and is equivalent to RW*. Additionally, it includes the score of another variable
(riparian width), which is not included to avoid redundancy. Each variable is evaluated on a scale
of “0 to 20”, where “0” represents the poorest or most altered condition of the variable and “20”
the most optimal or healthy condition. For variables marked with “*”, each margin is evaluated
separately (values of 1–10), and their combined score reflects the total score (values of 1–20). The
IIBAMA (values of 0–24) is the sum of the variables RT, EPT, II, IT, MT, and FT. The resulting value of
each variable is assigned a value between 1 and 4, depending on the point category.
Index Variable Acronym Variable Description
RQI
Riparian Quality Index (González-del-Tánago
and García-de-Jalón, 2011) [46]
An index developed to assess and characterize
the ecological status of riparian systems.
Riparian width RW *
Assesses restrictions to the riparian corridor caused by
human influence. When there are no restrictions, the riparian
width has its natural borders, and vegetation covers all land
that is between the channel and adjacent slopes.
Longitudinal continuity LC *
An estimation of the intensity of fragmentation of the riparian
vegetated area based on the size and frequency of open areas
created by human actions (i.e., land-use).
Composition and structure of
riparian vegetation CS * This variable helps assess the condition of riparian
composition by evaluating the vegetation’s natural
succession stages.
Age diversity and regeneration ADR This variable refers to the age classes of woody species in the
riparian zone. It helps to evaluate the regeneration of
woody species.
Bank condition BC This variable helps to assess the heterogeneity of the water
shoreline, stability of banks, and changes in erosion
and sedimentation.
Lateral connectivity LAC
The variable assesses how much the flow regulation has been
altered by morphological changes in the margins of the river
or by channelization works that prevent the occurrence of
natural bank flooding.
Vertical connectivity VC
The level of alterations to the soil surface that reduce natural
infiltration and alterations to substrata that reduce alluvial
permeability, subsurface flows, and
groundwater connectivity.
Life 2025,15, 508 7 of 23
Table 2. Cont.
Index Variable Acronym Variable Description
VBHA
Visual-Based Habitat Assessment
(Barbour et al., 1999) [45]
A qualitative index to visually evaluate the
environmental condition of rivers and streams by
assessing their physical and
ecological characteristics.
Epifaunal substrate EPS
The abundance and diversity of submerged structures in a
stream (such as cobbles, rocks, logs, and undercut banks) that
shape habitat complexity. These features provide refuge,
feeding grounds, and spawning sites for macrofauna.
Substrate embedment EMB
The degree to which rocks and snags are buried in streambed
sediments. Higher embeddedness reduces the surface area
for shelter, spawning, and egg incubation.
Velocity and depth
regime variations V/D The presence of diverse flow patterns (slow–deep,
slow–shallow, fast–deep, and fast–shallow) enhancing
habitat complexity.
Sediment deposition SD The accumulation of sediment in pools and the alteration of
river bottoms. Excessive deposition indicates instability and
reduces habitat suitability.
Channel flow status CFS
Refers to the degree to which the stream channel is filled with
water. Changes in flow,caused by factors such as channel
widening or flow reduction, limit suitable habitats for
aquatic organisms.
Channel alteration CA
Refers to significant changes in the stream’s shape, often due
to human activities like straightening, deepening, or
diverting for flood control or irrigation.
Riffle frequency FR
Measures the occurrence of riffles, which contribute to habitat
diversity and fauna richness. More frequent riffles enhance
habitat quality.
Bank stability BS *
Assesses the degree of bank erosion and potential for collapse.
Steep, unstable banks with crumbling soil, exposed roots, or
lack of vegetation indicate sediment movement issues and
reduced habitat quality.
Vegetation protection VP *
Refers to the extent of vegetation on stream banks and the
adjacent riparian zone. The presence of native vs. exotic
plants and the impact of grazing or urbanization on
vegetation are also considered.
IIBAMA
Index of biological integrity based on aquatic
macroinvertebrate assemblages (Pérez-Munguía
and Pineda-López, 2005; Torres-Olvera, et al.,
2018) [47,48]
This index was developed to estimate the
environmental condition of rivers and streams in
central México. The index is based on families of
aquatic macroinvertebrates as indicators of
degradation in river ecosystems.
Taxon richness RT
The number of aquatic macroinvertebrate families in a
sample. Higher taxa richness may indicate habitat
heterogeneity, which is related to refuge availability and an
increased speciation likelihood.
Ephemeroptera, Plecoptera, and
Trichoptera richness EPT
Families in these Orders (excluding Baetidae) are associated
with the transformation of organic matter into nutrients and
are sensitive to
environmental stress.
Intolerant insects II
Aquatic insect families that are sensitive to environmental
degradation. The absence of sensitive insects is an indicator
of alterations in environmental conditions (i.e., dissolved
oxygen, temperature, water level).
Intolerant taxa IT Refers to variables such as variable II plus other taxa of
macroinvertebrates that are not tolerant.
Mean tolerance MT
Corresponds to the average of the tolerance values present in
the sample.
Fixed taxa FT Corresponds to the number of taxa that have life habits fixed
to the substrate.
The condition of the riparian vegetation was evaluated following González del Tánago
and García de Jalón (2011) [
46
], assessing qualitative attributes of the riverine zone of the
river, including the space available for riparian functions (i.e., the longitudinal continuity
of natural riparian vegetation, width dimension of the floodplain with riparian vegetation,
and composition and structure of riparian vegetation variables) and indicators of the
temporal evolution of the present structure (i.e., variables related to the natural regeneration
of woody vegetation, bank conditions, and lateral connectivity, permeability, and soil
profile conditions) (Table 2). These variables were scored on a numerical scale from 0 to
15 and added to provide a final habitat category. González del Tánago and García de
Jalón (2011) [
46
] included descriptions of the characteristics and relative criteria to ensure
consistency in the evaluation procedure, and the scores increased as the habitat quality
increased. The actual riparian assessment process involved classifying the seven variables
as very good (scored from 13 to 15), good (scored from 10 to 12), moderate (scored from 7
Life 2025,15, 508 8 of 23
to 9), poor (scored from 4 to 6), or bad (scored from 1 to 3) based on the criteria described
by González del Tánago and García de Jalón (2011) [
46
]. The data supporting the reported
results are publicly archived on the Science Data Bank data storage platform, as stated in
the Data Availability Statement.
We determined the chemical condition by measuring the water’s chemical and physical
properties with a multimeter (Hach Hydromet Quanta, Loveland, CO, USA), including the
pH, dissolved oxygen (mg/L), total dissolved solids (ppm), electrical conductivity (mS),
and temperature (◦C).
We assessed the biological condition by evaluating the index of biological integrity
based on aquatic macroinvertebrate assemblages (IIBAMA) created by Pérez-Munguía
and Pineda-López (2005) and validated by Torres-Olvera et al. (2018) [
47
,
48
]. This index
includes six attributes that change with habitat degradation (here, we mention the attributes
and ecological meanings taken directly from Torres-Olvera et al. (2018)) [
48
]. The attributes
include the following: (I) The richness of taxa (RT) is limited by the heterogeneity of ecologi-
cal process; high taxa richness can highlight habitat heterogeneity and is associated with an
increased speciation likelihood. (II) Ephemeroptera, Plecoptera, and Trichoptera richness
(EPT) is associated with the transformation of organic matter into available nutrients for
superior trophic levels, and these groups are considered a good indicator of water quality.
(III) The richness of sensitive insects (II) is included because aquatic insects can fly between
freshwater ecosystems during adult stages as a survival strategy. The absence of sensitive
insects is related to limiting conditions of temperature, dissolved oxygen, alkalinity, salinity,
water flow rate, water level, and aquatic vegetation cover. For these reasons, sensitive
insects offer current and long-term information about environmental conditions. (IV) The
richness of sensitive taxa (IT) (not insects), which generally spend no part of their lifecycle
out of the water, can indicate an ecosystem where the habitat quality has been optimal for a
long time. (V) The mean tolerance value (MT) refers to the average value of tolerance of
the sample. Tolerance represents the capability of aquatic macroinvertebrates to survive
under environmental degradation. The values of tolerance show a relationship between
anthropic stress and the presence of aquatic organisms in a spatiotemporal way. For this
reason, they indicate the condition of freshwater systems. (VI) The number of fixed taxa
to a substrate (FT) is moderately sensitive to water pollution and depends on biotope
diversity and the heterogeneity of flow patterns. FT depletion can indicate the loss of
aquatic habitat heterogeneity and availability, caused by the riverbank’s degradation. Also,
land use changes in the catchment, which can increase fine sediment deposition, can reduce
the available habitat and food resources for clinger organisms. The values of each attribute
were used as response variables (not the value of the index) for data analyses (Table 2).
Macroinvertebrate samples were collected from all available habitats using a D-net
(300 mm diameter, 300
µ
m mesh size) with a total sampling effort of 90 min. Macroin-
vertebrates were separated from detritus by placing the collected samples in a white tray,
then picking the macroinvertebrates from the substrate with entomological tweezers. They
were preserved directly in the field with 80% alcohol and transported to the Biotic Integrity
Lab at UAQ-Campus Aeropuerto. Taxonomic identification of the macroinvertebrates was
carried out at the family level using specialized keys (e.g., [49,50]).
The true diversity of aquatic macroinvertebrate assemblages was also estimated using
the approach proposed by Jost (2006, 2007) through an assessment of the effective numbers
of elements at the family level, which refers to the number of taxa equally probable and
necessary to obtain a diversity value [
51
,
52
]. This method offers advantages over con-
ventional indices, such as Shannon’s index, as it has mathematical properties that align
more closely with what biologists intuitively expect from a diversity measure [
52
]. True
diversity was estimated using the SPADE (2009) program. We calculated the first-order
Life 2025,15, 508 9 of 23
diversity to emphasize the influence of abundant species, given that aquatic macroinver-
tebrate communities often display a pattern of rare and abundant species, resulting in an
uneven taxonomic distribution. The Jackknife estimator was employed. This estimator
works by systematically recalculating diversity after removing one observation at a time,
thereby generating an estimate that accounts for sample variability and rare taxa. It is well
suited for macroinvertebrate assemblages due to its ability to reduce bias associated with
under-sampling and provide more accurate estimates of true diversity [53,54].
We performed a principal component analysis (PCA) to elucidate patterns within
the physical and chemical variables and identify the variables that explain the greatest
variance with statistical significance [
55
]. Prior to the analysis, environmental variables
were standardized by transforming them logarithmically to ensure comparability and
prevent variables with larger scales from dominating the results. The PCA was based on
a correlation matrix, which is suitable when variables are measured on different scales.
Eigenvalues greater than five were considered to identify significant principal components.
The PCA was conducted using data from all sampling sites to identify general patterns and
key environmental gradients influencing the distribution of the Australian redclaw crayfish.
A biplot was generated to illustrate the influence of environmental variables at each site
and highlight the degradation gradient among them. The analysis included the pH, water
temperature, electrical conductivity, total dissolved solids, dissolved oxygen, and index
scores (IIBAMA, VBHA, and RQI). Additionally, we carried out a Spearman correlation
analysis to examine the relationships between the abundance of the Australian redclaw
crayfish and the environmental variables (physical, chemical, and biological) independently,
in order to identify those most closely associated with species establishment. Additionally,
we conducted a non-metric multidimensional scaling (NMDS) analysis to rank the data
and identify patterns and associations between aquatic macroinvertebrate assemblages, the
Australian redclaw crayfish, and environmental variables (including habitat, water quality,
and community stability) [
56
]. These analyses were performed with PAST (version 3.07)
software [57].
3. Results
A total of 760 Australian redclaw crayfish specimens were collected. The site with
the highest abundance of this species was Concá Manantiales, a spring that feeds into the
Santa Maria River. No individuals of the Australian redclaw crayfish were collected at
the Ayutla site, a tributary of the Santa Maria River. Along the Santa Maria River, from
upstream to downstream, 1 individual was collected at the upper site (Puente de las Mesas),
96 individuals at El Higuerón, 164 at El Salitrillo, 70 at Downstream of Adjuntas, and 12 at
Downstream of Jalpan River (Table 3).
We found spawning-capable individuals at almost all study sites except Ayutla. We
captured the largest and heaviest individuals at the most downstream site on the Santa
María River (Downstream of Jalpan River), with an average weight of 103.64 g, including
five mature individuals and four spawning-capable specimens; however, no juveniles were
collected at this site (Figure 2). The site with the highest abundance of this species (Concá
Manatiales) was dominated by juveniles (94%), with no mature individuals found. At
Puente de las Mesas, the single individual collected was spawning-capable. In El Higuerón,
62.5% of individuals were juveniles, 32.3% were spawning-capable, and 5.2% were mature.
At El Salitrillo, 65.6% were juveniles and 34.6% were spawning-capable. Downstream of
Adjuntas, 54.3% were juveniles, 38.6% were spawning-capable, and 7.2% were mature
(Figure 2).
Life 2025,15, 508 10 of 23
Table 3. The number of individuals, relative abundance, and density (Global Density = total abun-
dance (all sampling events)/42 trap-days, Average Density = average (abundance per sampling
event/42 trap-days)) of the Australian redclaw crayfish (Cherax quadricarinatus) by site in the Sierra
Gorda Biosphere Reserve, Central Mexican Plateau. NI = number of individuals; RA = relative
abundance; AYU = Ayutla; DA = Downstream of Adjuntas; HIG = El Higuerón; SAL = El Salitrillo;
CM = Concá Manantiales; PM = Puente de las Mesas; DRJ = Downstream of Jalpan River.
Study Site NI RA Global Density Average Density
AYU 0 0 0 0
DA 10 ±14.3 5.7 1.67 0.24 ±0.3
HIG 13.7 ±12.5 9.4 2.29 0.33 ±0.29
SAL 23.4 ±19.6 24.5 3.9 0.56 ±0.47
CM 59.6 ±47.5 58.5 9.92 1.4 ±1.1
PM 0.14 ±0.38 0 0.02 0.003 ±0.009
DRJ 1.7 ±1.4 1.9 0.29 0.04 ±0.03
The PCA indicated that the weight of the included variables was generally moderate
and relatively balanced across components 1 and 2 (Table 4), which together explain 78% of
the total variance in the set of environmental variables. As a result, the analysis did not
provide elements for eliminating any environmental variables from the correlation with the
abundance of the Australian redclaw crayfish. The variables with the highest coefficients in
component 1 were the number of families of aquatic macroinvertebrates that live attached
to the substrate (fixed taxa, FT) (0.2196), the true diversity of aquatic macroinvertebrate
assemblages (D1) (0.2199), the number of families of aquatic macroinvertebrates intolerant
to organic pollution (intolerant taxa, IT) (0.2178), the number of families of aquatic insects
intolerant to organic pollution (intolerant insects, II) (0.2151), and the condition or stability
of the stream banks (bank stability, BS) (0.2138). These variables represent biological and
habitat quality factors related to the community structure and physical characteristics
of the environment. The variables with the highest loadings in component 2 were the
channel flow status (CFS) (0.3645), sediment deposition (SD) (0.3559), and the epifaunal
substrate or available cover, which serves as refugia, feeding sites, or sites for spawning
and nursery functions for aquatic macrofauna (epifaunal substrate, EPS) (0.3090). These
variables are associated with the physical characteristics of the streambed and water flow,
reflecting current conditions and the sediment structure. Collectively, these components
capture the key environmental gradients influencing the distribution and establishment
of the Australian redclaw crayfish in the study area. As shown in the PCA biplot of
environmental variables, Ayutla (AYU) and Downstream of Jalpan River (DRJ) exhibit the
lowest disturbance, followed by DA, HIG, PM, and SAL with intermediate values, while
Conca Manantiales (CM) shows the highest disturbance (Figure 3).
The Spearman rank order correlations revealed some significant relationships between
environmental variables and the abundance of the Australian redclaw crayfish (Table 5).
The total dissolved solids (TDS) showed a strong positive correlation with Australian
redclaw crayfish abundance (rs = 0.75, p= 0.0522), suggesting that higher levels of dissolved
solids may favor the establishment of the species. The substrate embedment (EMB) was
negatively correlated with abundance (rs =
−
0.7857, p= 0.0362), indicating that greater
substrate embedment can favor the presence of the Australian redclaw crayfish due to
the nature of the variable, since a higher rating of this variable showed a better condition
or a lower degree of embedding. The taxon richness (RT) exhibited a perfect negative
correlation (rs =
−
1, p< 0.0001), suggesting that more diverse communities are less likely
to support a high abundance of the Australian redclaw crayfish. Although not statistically
significant, bank stability (BS, rs =
−
0.7092, p= 0.0743) and the Visual-Based Habitat
Assessment (VBHA, rs =
−
0.6786, p= 0.0938) also showed strong negative correlations,
Life 2025,15, 508 11 of 23
showing a potential trend where more stable and well-preserved habitats may reduce the
success of the establishment of the Australian redclaw crayfish. These findings highlight
the importance of water quality, biotic resistance, and habitat conditions in influencing the
distribution and establishment of the Australian redclaw crayfish.
Life 2025, 15, x FOR PEER REVIEW 11 of 25
abundance; AYU = Ayutla; DA = Downstream of Adjuntas; HIG = El Higuerón; SAL = El Salitrillo;
CM = Concá Manantiales; PM = Puente de las Mesas; DRJ = Downstream of Jalpan River.
Study Site NI RA Global Density Average Density
AYU 0 0 0 0
DA 10 ± 14.3 5.7 1.67 0.24 ± 0.3
HIG 13.7 ± 12.5 9.4 2.29 0.33 ± 0.29
SAL 23.4 ± 19.6 24.5 3.9 0.56 ± 0.47
CM 59.6 ± 47.5 58.5 9.92 1.4 ± 1.1
PM 0.14 ± 0.38 0 0.02 0.003 ± 0.009
DRJ 1.7 ± 1.4 1.9 0.29 0.04 ± 0.03
We found spawning-capable individuals at almost all study sites except Ayutla. We
captured the largest and heaviest individuals at the most downstream site on the Santa
María River (Downstream of Jalpan River), with an average weight of 103.64 g, including
five mature individuals and four spawning-capable specimens; however, no juveniles
were collected at this site (Figure 2). The site with the highest abundance of this species
(Concá Manatiales) was dominated by juveniles (94%), with no mature individuals found.
At Puente de las Mesas, the single individual collected was spawning-capable. In El Hi-
guerón, 62.5% of individuals were juveniles, 32.3% were spawning-capable, and 5.2%
were mature. At El Salitrillo, 65.6% were juveniles and 34.6% were spawning-capable.
Downstream of Adjuntas, 54.3% were juveniles, 38.6% were spawning-capable, and 7.2%
were mature (Figure 2).
Figure 2. The number of individuals by maturation phase (light gray bar) and weight (dark gray
bar) of the Australian redclaw crayfish (Cherax quadricarinatus) for each study site in the Sierra Gorda
Biosphere Reserve, Central Mexican Plateau. PM = Puente de las Mesas; CM = Concá Manantiales;
HIG = El Higuerón; SAL = El Salitrillo; DA = Downstream of Adjuntas; DRJ = Downstream of
Jalpan River.
The non-metric multidimensional scaling (NMDS) analysis provided a clear ordination
of sites based on environmental gradients (Figure 4). The first axis (r
2
= 0.75) explained
most of the variation, while the second axis (r
2
= 0) did not contribute significantly. The
environmental variables most strongly correlated with axis 1 were TDS (positively), DO,
VBHA, IIBAMA, and pH (negatively), reflecting a gradient of water quality and habitat
conditions influencing the distribution and density of the Australian redclaw crayfish.
Concá Manantiales (CM) had a higher density and abundance of the Australian redclaw
crayfish and showed a strong association with higher total dissolved solids (TDS). In
contrast, the site Ayutla (AYU), with no presence of Australian redclaw crayfish, had the
most negative score on axis 1, corresponding to higher dissolved oxygen (DO), lower
temperatures (TEMP), and better habitat and integrity conditions (VBHA and IIBAMA).
The sites Downstream of Jalpan River (DRJ) and Puente de las Mesas (PM) were positioned
in the left zone closer to the center of the ordination, reflecting intermediate environmental
Life 2025,15, 508 12 of 23
conditions, and these sites showed the presence of the Australian redclaw crayfish but at
a low density. On the other hand, the sites Downstream of Adjuntas (DA), El Salitrillo
(SAL), and El Higuerón (HIG) were also closer to the center but on the right side of the
ordination, reflecting more degraded conditions than DRJ and PM, and these sites showed
higher densities of the Australian redclaw crayfish.
Life 2025, 15, x FOR PEER REVIEW 13 of 25
EMB 0.1593 0.1572
V/D 0.2079 −0.0577
SD −0.0067 0.3559
CFS 0.0278 0.3645
CA 0.2098 −0.1047
FR 0.2134 −0.0821
BS 0.2138 0.0690
VP 0.0628 0.1302
VBHA 0.2075 0.1048
RW 0.1485 0.1704
LC 0.1423 0.1356
CS 0.1445 0.1773
ADR 0.1752 −0.2115
BC 0.2030 0.0774
LAC 0.1214 −0.2405
VC 0.1996 0.0009
RQI 0.1947 0.1637
RT 0.1841 0.1378
EPT 0.1857 −0.1912
II 0.2151 −0.0181
IT 0.2178 0.0024
MT −0.1757 0.2107
FT 0.2196 −0.0109
IIBAMA 0.2132 0.0313
D1 0.2199 0.0157
Figure 3. A principal component analysis biplot of environmental variables of sampling sites in the
Sierra Gorda Biosphere Reserve, Central Mexican Plateau. SAL = El Salitrillo; PM = Puente de las
Mes as; HIG = El Hig uerón ; DA = D ownstre am of A djuntas; DRJ = Downstream of Jalpan River; AYU
= Ayutla; CM = Concá Manantiales. TEMP = water temperature; CE = electrical conductivity; pH =
hydrogen potential; IIBAMA = index of biological integrity based on aquatic macroinvertebrate as-
semblages; DO = dissolved oxygen; D1 = first-order alpha diversity; VBHA = Visual-Based Habitat
Assessment; RQI = Riparian Quality Index; TDS = total dissolved solids.
The Spearman rank order correlations revealed some significant relationships be-
tween environmental variables and the abundance of the Australian redclaw crayfish
Figure 3. A principal component analysis biplot of environmental variables of sampling sites in the
Sierra Gorda Biosphere Reserve, Central Mexican Plateau. SAL = El Salitrillo; PM = Puente de las
Mesas; HIG = El Higuerón; DA = Downstream of Adjuntas; DRJ = Downstream of Jalpan River;
AYU = Ayutla; CM = Concá Manantiales. TEMP = water temperature; CE = electrical conductivity;
pH = hydrogen potential; IIBAMA = index of biological integrity based on aquatic macroinvertebrate
assemblages; DO = dissolved oxygen; D1 = first-order alpha diversity; VBHA = Visual-Based Habitat
Assessment; RQI = Riparian Quality Index; TDS = total dissolved solids.
Table 4. A principal component analysis of environmental variables of sampling sites in the Sierra
Gorda Biosphere Reserve, Central Mexican Plateau. pH = hydrogen potential; CE = electrical
conductivity; TEMP = water temperature; TDS = total dissolved solids; DO = dissolved oxygen;
EPS = epifaunal substrate; EMB = substrate embedment; V/D = velocity and depth regime varia-
tions; SD = sediment deposition; CFS = channel flow status; CA = channel alteration; FR = riffle
frequency; BS = bank stability; VP = vegetation protection; VBHA = Visual-Based Habitat Assessment;
RW = riparian width; LC = longitudinal continuity; CS = composition and structure; ADR = age
diversity and regeneration; BC = bank condition; LAC = lateral connectivity; VC = vertical connec-
tivity; RQI = Riparian Quality Index; RT = taxon richness; EPT = Ephemeroptera, Plecoptera, and
Trichoptera richness; II = intolerant insects; IT = intolerant taxa; MT = mean tolerance;
FT = fixed
taxa; IIBAMA = index of biological integrity based on aquatic macroinvertebrate assemblages;
D1 = first-order alpha diversity.
PC 1 PC 2
Eigenvalue 19.5955 6.3525
Percentage variance 59.38 19.25
pH 0.1775 −0.2208
CE −0.0199 −0.3479
TEMP −0.0798 −0.2378
TDS −0.2030 −0.0157
DO 0.1806 −0.0281
EPS 0.0641 0.3090
EMB 0.1593 0.1572
V/D 0.2079 −0.0577
SD −0.0067 0.3559
CFS 0.0278 0.3645
CA 0.2098 −0.1047
Life 2025,15, 508 13 of 23
Table 4. Cont.
PC 1 PC 2
FR 0.2134 −0.0821
BS 0.2138 0.0690
VP 0.0628 0.1302
VBHA 0.2075 0.1048
RW 0.1485 0.1704
LC 0.1423 0.1356
CS 0.1445 0.1773
ADR 0.1752 −0.2115
BC 0.2030 0.0774
LAC 0.1214 −0.2405
VC 0.1996 0.0009
RQI 0.1947 0.1637
RT 0.1841 0.1378
EPT 0.1857 −0.1912
II 0.2151 −0.0181
IT 0.2178 0.0024
MT −0.1757 0.2107
FT 0.2196 −0.0109
IIBAMA 0.2132 0.0313
D1 0.2199 0.0157
Table 5. Spearman correlations between the abundance of Australian redclaw crayfish (Cherax
quadricarinatus) and environmental and biological variables in the Sierra Gorda Biosphere Re-
serve, Central Mexican Plateau. rs = Spearman rank order correlation; pH = hydrogen potential;
CE = electrical conductivity; TEMP = water temperature; TDS = total dissolved solids; DO = dis-
solved oxygen; EPS = epifaunal substrate; EMB = substrate embedment; V/D = velocity and depth
regime variations; SD = sediment deposition; CFS = channel flow status; CA = channel alteration;
FR = riffle
frequency; BS = bank stability; VP = vegetation protection; VBHA = Visual-Based Habitat
Assessment; RW = riparian width; LC = longitudinal continuity; CS = composition and struc-
ture; ADR = age diversity and regeneration; BC = bank condition; LAC = lateral connectivity;
VC = vertical
connectivity; RQI = Riparian Quality Index; RT = taxon richness; EPT = Ephemeroptera,
Plecoptera, and Trichoptera richness; II = intolerant insects; IT = intolerant taxa; MT = mean tolerance;
FT = fixed taxa; IIBAMA = index of biological integrity based on aquatic macroinvertebrate assem-
blages; D1 = first-order alpha diversity. The superscript “a” next to the p-values indicates that the
marked variables are statistically significant at the established significance level (p< 0.05).
Variable rs p
pH −0.0541 0.9084
CE 0.2143 0.6445
TEMP 0.3214 0.4821
TDS 0.75 0.0522
DO −0.3929 0.3833
EPS −0.6667 0.1019
EMB −0.7857 0.0362 a
V/D −0.4364 0.3276
SD −0.1081 0.8175
CFS −0.3368 0.4601
CA −0.5455 0.2053
FR −0.393 0.3832
BS −0.7092 0.0743
VP −0.4491 0.3121
VBHA −0.6786 0.0938
RW −0.5455 0.2053
LC −0.3143 0.5441
CS −0.4505 0.3104
ADR 0.0741 0.8745
BC −0.393 0.3832
Life 2025,15, 508 14 of 23
Table 5. Cont.
Variable rs p
LAC 0 1
VC −0.2594 0.5742
RQI −0.7027 0.0782
RT −1 <0.0001 a
EPT 0 1
II −0.4364 0.3276
IT −0.593 0.1605
MT 0 1
FT −0.6365 0.1243
IIBAMA −0.4546 0.3054
D1 −0.70273 0.089683
Life 2025, 15, x FOR PEER REVIEW 15 of 25
LAC 01
a
VC −0.2594 0.5742
a
RQI −0.702
7
0.0782
a
RT −1<0.0001
EPT 01
a
II −0.4364 0.3276
a
IT −0.593 0.1605
a
MT 01
a
FT −0.6365 0.1243
a
IIBAMA −0.4546 0.3054
a
D1 −0.70273 0.089683
a
The non-metric multidimensional scaling (NMDS) analysis provided a clear ordina-
tion of sites based on environmental gradients (Figure 4). The first axis (r² = 0.75) explained
most of the variation, while the second axis (r² = 0) did not contribute significantly. The
environmental variables most strongly correlated with axis 1 were TDS (positively), DO,
VBHA, IIBAMA, and pH (negatively), reflecting a gradient of water quality and habitat
conditions influencing the distribution and density of the Australian redclaw crayfish.
Concá Manantiales (CM) had a higher density and abundance of the Australian redclaw
crayfish and showed a strong association with higher total dissolved solids (TDS). In con-
trast, the site Ayutla (AYU), with no presence of Australian redclaw crayfish, had the most
negative score on axis 1, corresponding to higher dissolved oxygen (DO), lower tempera-
tures (TEMP), and beer habitat and integrity conditions (VBHA and IIBAMA). The sites
Downstream of Jalpan River (DRJ) and Puente de las Mesas (PM) were positioned in the
left zone closer to the center of the ordination, reflecting intermediate environmental con-
ditions, and these sites showed the presence of the Australian redclaw crayfish but at a
low density. On the other hand, the sites Downstream of Adjuntas (DA), El Salitrillo
(SAL), and El Higuerón (HIG) were also closer to the center but on the right side of the
ordination, reflecting more degraded conditions than DRJ and PM, and these sites showed
higher densities of the Australian redclaw crayfish.
Figure 4. Non-metric multidimensional scaling ordination based on macroinvertebrate assemblages
at the study sites in the Sierra Gorda Biosphere Reserve, Central Mexican Plateau, with environ-
mental and biological variables as response variables. Values in parentheses indicate the density of
the Australian redclaw crayfish. Stress: 0.06, r2 axis 1 = 0.75, r2 axis 2 = 0. AYU = Ayutla; DA =
Downstream of Adjuntas; HIG = El Higuerón; SAL = El Salitrillo; CM = Concá Manantiales; PM =
Figure 4. Non-metric multidimensional scaling ordination based on macroinvertebrate assemblages
at the study sites in the Sierra Gorda Biosphere Reserve, Central Mexican Plateau, with environmental
and biological variables as response variables. Values in parentheses indicate the density of the Aus-
tralian redclaw crayfish. Stress: 0.06, r2 axis 1 = 0.75, r2 axis 2 = 0. AYU = Ayutla;
DA = Downstream
of Adjuntas; HIG = El Higuerón; SAL = El Salitrillo; CM = Concá Manantiales; PM = Puente de
las Mesas; DRJ = Downstream of Jalpan River. DO = dissolved oxygen; pH = hydrogen potential;
TEMP = water
temperature; TDS = total dissolved solids; RQI = value obtained for the Riparian
Quality Index; VBHA = value obtained in the Visual-Based Habitat Assessment; IIBAMA = value
obtained for the index of biological integrity based on aquatic macroinvertebrates assemblages;
D1 = first-order alpha diversity.
4. Discussion
This study demonstrated the successful establishment of the Australian redclaw cray-
fish (Cherax quadricarinatus) across multiple sites within the Santa María River and Concá
Spring, in the Sierra Gorda Biosphere Reserve. The findings showed that the Australian
redclaw crayfish is particularly abundant in degraded environments, so we cannot reject
our hypothesis that environmental degradation, characterized by altered water quality
and habitat disruption, facilitates the establishment and spread of this species in the river
ecosystem. The environmental variables associated with higher densities of the Australian
redclaw crayfish include increased total dissolved solids (TDS), greater substrate embed-
ment, and degraded conditions of the stream banks, suggesting that the Australian redclaw
crayfish thrives in habitats where the water quality and structural habitat features are com-
promised. These results contribute to identifying the environmental factors that facilitate
Life 2025,15, 508 15 of 23
the establishment and proliferation of invasive crayfish species and provide important
insights into the mechanisms driving biological invasions in freshwater ecosystems.
Sites with higher densities of the Australian redclaw crayfish, such as El Salitrillo
and El Higuerón, presented degraded environmental conditions. These conditions were
reflected in variables such as substrate embedment, high TDS levels, and degraded stream
banks. This pattern is consistent with previous findings that invasive species, such as the
snail Melanoides tuberculata, and fishes such as the twospot livebearer (Pseudoxiphophorus
bimaculatus) and the common carp (Cyprinus carpio), thrive in disturbed or human-impacted
habitats [
58
–
60
]. In particular, the presence of egg-bearing females of the Australian redclaw
crayfish in degraded areas, as observed in Indonesia, confirms the successful establishment
of populations in impacted environments [
18
]. The ability of the Australian redclaw crayfish
to accumulate heavy metals, as shown in previous studies [
61
], probably explains its success
in these degraded environments. The species appears to have efficient detoxification
mechanisms, allowing it to survive in habitats with high concentrations of contaminants
(e.g., metals). Additionally, it is a useful bioindicator of substrate contamination due to its
capacity to accumulate metals in its hepatopancreas [61].
The adaptability of the Australian redclaw crayfish to various environmental con-
ditions, such as fluctuations in pH, temperature, and dissolved oxygen levels, enhances
its ability to establish itself in diverse habitats [
62
,
63
]. In our study, this adaptability
is supported by the presence of the Australian redclaw crayfish in sites with different
physicochemical conditions. Specifically, the species was found in habitats with a range
of dissolved oxygen levels (ranging within 5.81–12.27 mg/L), pH values (7.31–8.42), and
temperatures (26.4–37.4
◦
C). These findings suggest that the Australian redclaw crayfish
can tolerate environmental variability, which likely contributes to its invasive potential.
Moreover, its reproductive potential is bolstered by increased sperm production at temper-
atures above 27
◦
C [
64
], which may explain its high reproductive success in warmer waters
(i.e., >28
◦
C) within the study area. This is of particular interest in the context of climate
change as the general temperature increases of 2–4
◦
C projected under the IS92 scenario for
central–eastern Mexico may increase the risk of Australian redclaw crayfish establishment.
The inverse relationship between the abundance of the Australian redclaw crayfish
and the richness of aquatic macroinvertebrate families found in our study suggests that
ecosystems with greater biodiversity may be more resistant to the establishment of inva-
sive species. This pattern may align with the biotic resistance hypothesis, where diverse
native communities reduce the success of invaders [
65
]. This inverse correlation can reflect
that such environments are less suitable for native species, reducing biotic resistance and
facilitating the establishment of invasive species. Additionally, higher macroinvertebrate
diversity is often associated with better water quality and habitat conditions [
66
]. Moreover,
sites with elevated levels of total dissolved solids (TDS) and habitat degradation, where
macroinvertebrate diversity is reduced, appeared to support higher Australian redclaw
crayfish densities. This pattern suggests that human-induced disturbances, such as pol-
lution and sedimentation, create ecological conditions where invasive species can thrive
due to reduced competition and ecological niches that invasive species are well suited to
exploit (cf. [67]).
These findings can help predict the presence and abundance of the Australian redclaw
crayfish and contribute to its management in biological invasions. The negative correlation
observed between Cherax quadricarinatus density and macroinvertebrate diversity suggests
that habitat degradation may play a key role in facilitating the establishment of this invasive
species. This pattern likely reflects habitat quality rather than direct biotic interactions, such
as resource competition. Cherax destructor, for example, thrives in eutrophic, canopy-free
habitats where autochthonous resources dominate [
68
]. Similarly, C. quadricarinatus may
Life 2025,15, 508 16 of 23
benefit from the high productivity of eutrophic systems, where easily digestible resources
are abundant. This is consistent with laboratory studies showing that the species achieves
greater growth and survival rates when fed low-fiber diets, reflecting its limited capac-
ity to digest structural plant material [
69
]. These findings suggest that the presence of
C. quadricarinatus in degraded habitats may be linked to its ability to exploit high-
productivity environments, which often have reduced macroinvertebrate diversity. Addi-
tionally, despite its flexible trophic niche, C. quadricarinatus tends to occupy lower trophic
levels in the food web [
70
]. Abiotic factors such as total dissolved solids (TDS), substrate em-
bedment, and shoreline degradation appear to be stronger predictors of Cherax abundance.
However, macroinvertebrate richness may serve as an indirect indicator of habitat quality
and should be further explored as a potential predictor of invasive species abundance.
Our findings align with studies on other invasive crayfish species, such as Procambarus
clarkii, which also thrive in eutrophic and degraded habitats. In these conditions, eutrophi-
cation, riparian canopy removal, and lower flow velocities decrease habitat suitability for
native species, thereby reducing biotic resistance and indirectly facilitating the establish-
ment of invaders [
71
]. In such environments, other invasive crayfish like Austropotamobius
pallipes and Procambarus clarkii can exploit altered ecological conditions such as increased
availability of organic matter, reduced competition, and lower predation pressure, which
may enhance their growth and establishment [
72
]. These species exhibit physiological
and ecological plasticity, allowing them to tolerate fluctuating environmental conditions,
including low dissolved oxygen levels and higher nutrient concentrations, which often
limit native species survival and reproduction.
Although this study focused on the environmental conditions influencing the establish-
ment of the Australian redclaw crayfish, the observed differences in population structure
across sites suggest underlying population dynamics that require further investigation.
Higher densities of the Australian redclaw crayfish were recorded in more disturbed sites;
however, body size did not appear to be significantly affected by environmental degrada-
tion. The lower densities observed in less degraded sites, without compromising individual
growth, suggest that the species can adapt to these environments, albeit at reduced popu-
lation densities. Additionally, differences in the proportions of juveniles and adults were
observed among sites, which may be related to ontogenetic dietary shifts. Juveniles, with
higher protein requirements, tend to rely on zooplankton and small macroinvertebrates,
which may favor their proliferation in areas with high organic matter loads and degraded
habitat conditions [
68
,
73
]. This aligns with the higher proportion of juveniles recorded in
more degraded sites, such as Concá Manantiales (CM) and El Salitrillo (SAL). In contrast,
adults, whose diet is more dependent on detritus and macrophytes, may be better suited
to a broader range of habitats, including less degraded sites where resource diversity and
habitat complexity are greater [
73
]. While these patterns provide valuable insights, it is
premature to draw definitive conclusions. Factors such as fishing pressure, predator pres-
ence, and specific environmental conditions could be more important for the population
dynamics of the Australian redclaw crayfish in invaded ecosystems.
On the other hand, the impact of the Australian redclaw crayfish on native biodiversity
could extend beyond competition for shelter and resources. The presence of invasive
crayfish species is linked to a decline in benthic macroinvertebrate biodiversity in aquatic
ecosystems [
74
], as we observed in sites with higher abundance of the Australian redclaw
crayfish in our study. The population establishment of the Australian redclaw crayfish in
degraded habitats of the Sierra Gorda Biosphere Reserve may lead to significant changes
in the aquatic community structure, such as shifts in community composition, reductions
in functional diversity, and alterations in trophic interactions, including the disruption
of predator–prey dynamics and nutrient cycling processes, through mechanisms such
Life 2025,15, 508 17 of 23
as bioturbation and selective predation on native macroinvertebrates. Competition for
resources and shelter with native crustaceans, as documented in other invasions, could
reduce the abundance and diversity of these native species [
75
,
76
], potentially leading
to local population declines or shifts in species dominance. Interestingly, our results
showed that sites with higher macroinvertebrate diversity, such as Ayutla (AYU), had
no Australian redclaw crayfish presence, while sites with lower diversity, like Concá
Manatiales (CM) and El Salitrillo (SAL), supported higher densities of the species. This
pattern suggests that reduced native biodiversity may facilitate the establishment of the
Australian redclaw crayfish; in turn, its presence could exacerbate biodiversity loss, creating
synergistic effects that allow its successful establishment. These ecological processes alter
community structure and ecosystem processes, such as organic matter decomposition and
nutrient cycling [77].
The Australian redclaw crayfish threatens the integrity of the aquatic ecosystems
in the Sierra Gorda Biosphere Reserve and poses a risk to native species, particularly
Macrobrachium sp., a native crayfish in the same river systems and habitats. The presence
of the invasive Australian redclaw crayfish increases the risk of competitive displacement
of Macrobrachium sp., which is already facing pressure from habitat degradation. The
Australian redclaw crayfish is known for its aggressive behavior and ability to outcompete
native species for essential resources (e.g., macrophytes and detritus) [
78
]. This competitive
pressure may lead to reduced access to food and shelter for Macrobrachium sp. While
Macrobrachium sp. is a robust species, with adult specimens possessing physical strength
and resistance that may allow them to defend against aggressive interactions with the
Australian redclaw crayfish, juvenile Macrobrachium sp. are more vulnerable due to their
smaller size, making them more susceptible to predation or displacement by mature
Australian redclaw crayfish.
The presence of the Australian redclaw crayfish can exacerbate habitat degradation,
which can directly affect Macrobrachium sp. and other native species. Invasive crayfish
species are known to alter the physical structure of the environment by burrowing and
disturbing the substrate, leading to increased turbidity and sedimentation [
71
]. These
changes can degrade the quality of habitats that are critical for the survival of native species,
particularly in areas with already lower water quality and limited shelter. The loss of critical
habitats and increased predation pressure by the invasive Australian redclaw crayfish can
lead to the decline of native populations.
As Rodríguez-Cruz et al. (2023) [
36
] emphasized, understanding the distribution and
invasion dynamics of the Australian redclaw crayfish is crucial for developing effective
management strategies to mitigate its spread and impact within the Sierra Gorda Biosphere
Reserve. Restoring habitats, replanting riparian vegetation, improving water quality by
reducing pollution and eutrophication, and managing local dredging could reduce the
invasion success. Additionally, managing reproductive populations (egg-bearing females,
mature individuals, and intersex males) may be a key action to limiting the population’s
success. This management could involve targeted removal efforts focused on these repro-
ductive individuals during breeding seasons, such as the use of baited traps designed to
capture larger, mature crayfish. By reducing the reproductive potential of the population,
this strategy can decrease recruitment rates and slow the spread of the Australian redclaw
crayfish in invaded ecosystems [
16
,
79
]. However, it is essential to consider the reproductive
characteristics associated with crayfish, which could represent a challenge for the success
of management strategies. On the one hand, crayfish have different reproductive mor-
photypes that are essential for understanding the fine reproductive period [80,81]. On the
other hand, it is necessary to locate females and intersexual individuals who tend to act
like males, since these are the ones who tend to have a higher proportion of females in
Life 2025,15, 508 18 of 23
their litter [
6
]. The capture of these organisms is recommended as part of a control plan,
especially at the beginning of invasions, to reduce propagule pressure [79].
This study provides the principal environmental factors that facilitate the establish-
ment and proliferation of the invasive Australian redclaw crayfish, including elevated
levels of total dissolved solids (TDS), reduced substrate embedment, lower macroinver-
tebrate taxon richness, and degraded habitat conditions, such as poor bank stability and
reduced riparian vegetation cover; however, the relatively short sampling period may not
capture the population dynamics of the species. Additionally, some biotic factors that could
influence the distribution of the species, such as the presence of predators or competitors,
were not considered. Future studies should address these variables to provide a more
comprehensive understanding of the relationships between the Australian redclaw crayfish
and local biodiversity. We suggest long-term studies to assess how the Australian redclaw
crayfish populations evolve in response to habitat improvements. Experimental research
evaluating the effectiveness of different management strategies, such as species removal
or riparian restoration, could provide valuable insights for controlling this invasion and
understanding the invasion dynamics. It is also significant to monitor the long-term effects
on native biodiversity and main ecosystem processes, such as primary productivity and
organic matter decomposition. There is an urgent need for further studies and management
measures for improving habitat quality and limiting the spread of this species to protect
native biodiversity.
Author Contributions: Conceptualization, O.Y.D.-R. and M.J.T.-O.; methodology, O.Y.D.-R.,
E.A.-R.
and M.J.T.-O.; validation, O.Y.D.-R.; formal analysis, O.Y.D.-R. and D.A.G.-Á.; investigation, O.Y.D.-R.
(lead), M.J.T.-O. (lead), E.A.-R. (lead), D.A.G.-Á. and J.A.V.-E.; resources, J.P.R.-H.; data curation,
M.J.T.-O.; writing—original draft preparation, O.Y.D.-R. and J.A.V.-E.; writing—review and editing,
O.Y.D.-R., J.A.V.-E. and J.P.R.-H.; visualization, O.Y.D.-R. and D.A.G.-Á.; supervision, J.P.R.-H.,
O.Y.D.-R. and E.A.-R.; project administration, O.Y.D.-R.; funding acquisition, J.P.R.-H. and O.Y.D.-R.
All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the FONDEC-UAQ-2022 (Fondo para el Desarrollo del
Conocimiento—Universidad Autónoma de Querétaro, grant number FNB-2023-01).
Institutional Review Board Statement: We declare that the manuscript adheres to the publisher’s
Ethical Guidelines; all research related to this article had the necessary research permits and was
evaluated by the ethics committee of the Faculty of Natural Sciences of the Autonomous University
of Querétaro, who, in turn, referred it to SEMARNAT (Secretaría de Medio Ambiente y Recursos
Naturales: No.22/K4-0179/08/22) and CONANP (Comisión Nacional de Áreas Naturales Protegidas:
No.0201/RBSC/2022) for project authorization.
Informed Consent Statement: Not applicable.
Data Availability Statement: The data supporting the reported results are publicly archived on
the Science Data Bank data storage platform, which can be accessed through the following link:
https://doi.org/10.57760/sciencedb.14208.
Acknowledgments: We thank all those who collaborated on the project ‘Invasion dynamics of the
Australian Redclaw Crayfish, Cherax quadricarinatus (Von Martens, 1868) in the Sierra Gorda Biosphere
Reserve, Querétaro’ supported by Fondo para el Desarrollo del Conocimiento (FONDEC-UAQ-2022).
This research was also supported by PRONAII 318956 ‘Ecohidrología para la sustentabilidad y
gobernanza del agua y cuencas para el bien común’ (PRONACES- SECIHTI). We thank Eduardo
Tello Guillén (local fisherman) for making the traps, MSC Ulises Torres García for data curation, Biol.
Diana Stephanie Angeles and Juan Manuel Camacho for field work, and Delia Reséndiz and Calixto
López for logistical support. O.Y.D.-R. and J.P.R.-H. are grateful to SECIHTI for the facilities provided
for the development of this investigation.
Conflicts of Interest: The authors declare no conflicts of interest.
Life 2025,15, 508 19 of 23
Abbreviations
The following abbreviations are used in this manuscript:
SGBR Sierra Gorda Biosphere Reserve
TL Total length
CL Carapace length
VBHA Visual-Based Habitat Assessment
PCA Principal component analysis
NMDS Non-metric multidimensional scaling
PC Principal component
DO Dissolved oxygen
TDS Total dissolved solids
TEMP Water temperature
CE Electrical conductivity
EPS Epifaunal substrate
EMB Substrate embedment
V/D Velocity and depth regime variations
SD Sediment deposition
CFS Channel flow status
CA Channel alteration
FR Riffle frequency
BS Bank stability
VP Vegetation protection
RW Riparian width
LC Longitudinal continuity
CS Composition and structure
RQI Riparian Quality Index
ADR Age diversity and regeneration
BC Bank condition
LAC Lateral connectivity
VC Vertical connectivity
RT Taxon richness
EPT Ephemeroptera, Plecoptera, and Trichoptera richness
II Intolerant insects
IT Intolerant taxa
FT Fixed taxa
MT Mean tolerance
IIBAMA Index of biological integrity based on aquatic macroinvertebrate assemblages
D1 First-order alpha diversity
NI Number of individuals
RA Relative abundance
AYU Ayutla
DA Downstream of Adjuntas
HIG El Higuerón
SAL El Salitrillo
CM Concá Manantiales
PM Puente de las Mesas
DRJ Downstream of Jalpan River
Rs Spearman rank order correlation
Life 2025,15, 508 20 of 23
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