First record of the Australian redclaw crayfish Cherax quadricarinatus (von Martens, 1868) in Hong Kong, China

Abstract

Invasive freshwater crayfish are spreading rapidly across the world. Here, we report the first record of Australian redclaw crayfish, Cherax quadricarinatus (von Martens, 1868) in Hong Kong, China. Identification of the captured crayfish was confirmed using external morphological features and molecular analyses. A total of 49 crayfish were captured from a stream pool and a reservoir in Pok Fu Lam Country Park using dip nets and funnel traps. The captured C. quadricarinatus ranged from 17.20 mm to 56.40 mm (mean = 30.70 mm) in carapace length and the sex ratio was 1:1. Since this species is globally recognized as an invasive species, a comprehensive survey on its status and invasion front, an investigation into its potential ecological impacts, as well as the formulation of a monitoring and removal strategy, are warranted.

Full text

BioInvasions Records (2021) Volume 10 Article
in press
Yau and Lau (2021), BioInvasions Records ( in press)
CORRECTED PROOF
Rapid Communication
First record of the Australian redclaw crayfish Cherax quadricarinatus
(von Martens, 1868) in Hong Kong, China
Sze-man Yau1 and Anthony Lau1,2,*
1Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China
2Science Unit, Lingnan University, Hong Kong SAR, China
Author e-mails: 18219594@life.hkbu.edu.hk (SY), antlau1@gmail.com (AL)
*Corresponding author
Abstract
Invasive freshwater crayfish are spreading rapidly across the world. Here, we report
the first record of Australian redclaw crayfish, Cherax quadricarinatus (von Martens,
1868) in Hong Kong, China. Identification of the captured crayfish was confirmed
using external morphological features and molecular analyses. A total of 49 crayfish
were captured from a stream pool and a reservoir in Pok Fu Lam Country Park using
dip nets and funnel traps. The captured C. quadricarinatus ranged from 17.20 mm
to 56.40 mm (mean = 30.70 mm) in carapace length and the sex ratio was 1:1. Since
this species is globally recognized as an invasive species, a comprehensive survey
on its status and invasion front, an investigation into its potential ecological impacts,
as well as the formulation of a monitoring and removal strategy, are warranted.
Key words: invasive crayfish, reservoir, stream, pet release, ornamental trade
Introduction
Introduced alien species have been generally recognized as one of the
greatest threats to global biodiversity (Dudgeon et al. 2006; Pyšek et al.
2020; Tickner et al. 2020). In addition to interacting with native species
through competition and predation, some introduced species can modify
habitats and cause community-level shifts in species assemblages and
associated ecosystem processes (Sanders et al. 2003; Eastwood et al. 2007).
A wide range of animals and plants have been introduced to Hong
Kong, a densely populated metropolitan located on the edge of the tropic.
Relatively wild winters and abundant natural habitats enabled the
establishment of at least 74 invasive species in the city, including mosquito
fish Gambusia affinis, red imported fire ant Sloenopsis invicta, and mile-a-
minute weed Mikania micrantha. Despite recognizing invasive species as a
key threat to the local natural environment, the Hong Kong government
does not maintain a detailed database on invasive species and has put forth
minimal effort to manage these species (GovHK 2015). However, the
success of introduced species management hinges upon early discovery
and quick action (Simberloff et al. 2005). Research on ecological impacts of
Citation: Yau S, Lau A (2021) First record
of the Australian redclaw crayfish
Cherax
quadricarinatus
(von Martens, 1868) in
Hong Kong, China
. BioInvasions Records
10
(in press)
Received:
4 August 2020
Accepted:
13 December 2020
Published:
12 February 2021
Handling editor:
Tatenda Dalu
Thematic editor:
Kenneth Hayes
Copyright:
© Yau and Lau
This
is an open access article distributed under terms
of the Cr eative C ommons At tribut ion Lice nse
(
Attribution 4 .0 Internationa l - CC BY 4.0 ).
OPEN ACCESS.

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
non-marine invasive species in Hong Kong has focused mainly on primary
and secondary consumers such as Pomacea canaliculata (Fang et al. 2010;
Karraker and Dudgeon 2014) and S. invicta (Chan and Guénard 2020), but
less attention has been paid to higher level consumers such as predacious
fish and decapods.
Hong Kong has several species of native freshwater decapods, but there
is no native crayfish (Dudgeon 1999). However, unidentified feral crayfish
have been observed in Pok Fu Lam Country Park since the early 2000s (Lee
Wing Ho pers. comm.) and again in 2016 (A. Lau pers. observation). Feral
populations of freshwater crayfish may be introduced after intentional
release, unintentional introduction through escape from aquaculture, bait-
bucket release, and release after being imported for educational purposes
(Hobbs et al. 1989; Gherardi 2010). Crayfish are generalist omnivores and
ecosystem engineers, and when introduced, generally have negative effects
on recipient ecosystems. These effects can include reduction in the biomass
and abundance of macrophytes, benthic invertebrates, fish, and amphibians
(Twardochleb et al. 2013). Introduced crayfish species also tend to have a
wider environmental tolerance than native species, which allows them to
survive in extreme temperature conditions and low dissolved oxygen levels
(Reynolds and Souty-Grosset 2011).
To date, no study has been conducted to confirm the identity of the
reported crayfish species in Hong Kong. The objective of this study is to
confirm the identity of this unidentified crayfish species and collect basic
ecological information regarding this crayfish in the recipient ecosystem.
Materials and methods
Study site
This study was conducted in a stream pool (22°15′59.6″N; 114°08′23.2″E)
and a section of a reservoir (22°15′58.8″N; 114°08′21.5″E) in Pok Fu Lam
Country Park in the Hong Kong Special Administrative Region, China
(Figure 1). Small stream pools with low flow rates or nearly stagnant water
are often formed along the stream length during the dry season (i.e.
October to March). The stream pool sampled had a surface area of 5.17 m2
with a maximum depth of 0.62 m, and the reservoir’s surface area was
30565.46 m2. The stream pool substrate was mainly large cobbles with
some boulders, while the reservoir substrate was mainly sand and clay with
many boulders located along the shore. Riparian vegetation at the stream
pool comprised mainly small trees and shrubs; the reservoir was
surrounded by tall grasses and a few shrubs. Emergent vegetation at the
stream pool was dominated by Acorus gramineus.
Sampling
Sampling was conducted from December 2019 to February 2020. Initially,
aliquots of canned cat food, minced chicken, or rice mixed with shrimp food,

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
Figure 1. Map of Hong Kong SAR, China indicating the location of the study sites.
each weighing approximately 30 g, were placed in separate mesh bags as
bait to attract crayfish. Since canned cat food appeared to be the most
attractive to the crayfish (S-M Yau pers. obs.), all subsequent sampling used
only canned cat food as bait. Some crayfish were captured using hand-held
dip nets when they approached bait, and some were captured with baited
funnel traps (30 cm diameter, 60 cm long, 1 cm mesh size). The duration of
the dip net capture period was around 6 man-hour per sampling occasion,
while the funnel traps (two in the stream pool and two in the reservoir)
were placed at the sampling sites for around 10 hours (overnight) per
sampling occasion. In total, we surveyed two sampling sites for four occasions.
At the time of sampling, the water temperature was between 16.1 °C and
19.1 °C (mean = 18.15 °C, SD = 0.86). Average pH was 6.67 for the stream
pool and 6.91 for the reservoir; and average dissolved oxygen was 8.84 and
9.22 mg/L for the stream pool and the reservoir, respectively.
Standard morphological measurements were conducted for each
crayfish captured. The total length, carapace length, and chela length of the
crayfish were measured to the nearest millimetre with a vernier caliper.
The mass (g) of the captured crayfish was measured with a scale. The sex of
each crayfish was identified based on the position of the genital openings.
The genital openings of males and females are located at the base of the
fifth and third pair of pereiopods, respectively (Parnes et al. 2003). If the
genital opening was located at the base of the fifth and the third pair of the
walking legs, that individual was classified as intersex (Parnes et al. 2003).
All crayfish captured were not released back into the sampling site, but by-
catch was immediately released back into the water. The captured crayfish
were transported to the laboratory using a cooler filled with ice.

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
Species identification
Crayfish were identified by their morphological characteristics and DNA.
Muscle tissues were extracted from the chelae and walking legs of eight
crayfish using sterile scissors (Scalici et al. 2009). Genomic DNA was extracted
by using the DNeasy Blood and Tissue Kit (QIAGEN, Hilden, Germany).
The universal primers HCO2198 (5’-TAAACTTCAGGGTGACCAAAAA
ATCA-3’) and LCO1490 (5’-GGTCAACAAATCATAAAGATATTGG-3’)
were used to amplify the mitochondrial cytochrome c oxidase subunit I
(COI) gene by conducting polymerase chain reaction (PCR) (Folmer et al.
1994). Identical COI gene fragments with approximately 650 base pairs
were amplified after PCR (Scalici et al. 2009). The confirmed PCR product
was sent to the laboratory company (Tech Dragon Limited) to conduct DNA
sequencing. Basic Local Alignment Search Tool (BLAST) (https://blast.
ncbi.nlm.nih.gov/Blast.cgi) was used to confirm the crayfish species by
comparing the 624 bps obtained sequences to sequences in the BLAST
GenBank nucleotide database.
Results
A total of 49 crayfish were captured from 4 sampling occasions
(Supplementary material Table S1). The captured crayfish were identified
as Australian redclaw crayfish, Cherax quadricarinatus (von Martens, 1868),
(Figure 2) based on morphological characteristics and DNA barcoding. All
eight sequences matched with the C. quadricarinatus sequences in
Genbank, with similarity values ranging from 99% to 100% (Genbank
Accession number: KY745779.1 and KX377348.1).
Total length of captured C. quadricarinatus was between 33 mm and
119 mm (mean = 65.06, SD = 21.28 mm). Carapace length ranged from
17.20 mm to 56.40 mm (mean = 30.70, SD = 10.13 mm), while length of
chela was between 8.60 mm and 43.40 mm (mean = 20.78, SD = 9.06 mm)
(Figure 3). A total of 29 males and 19 females and 1 intersex were captured;
the sex ratio was not significantly different from 1:1 (χ 2 = 1.653, p = 0.199).
We captured 33 crayfish from the stream pool and 16 crayfish from the
reservoir. The catch per unit effort (CPUE) for baited traps was 0.50 crayfish
per trap night for both the stream pool and the reservoir.
Discussion
Here we provide evidence of the presence of Cherax quadricarinatus in a
stream and a reservoir in Pok Fu Lam Country Park in the Hong Kong
Special Administrative Region, China. Cherax quadricarinatus is a large
and conspicuously coloured crayfish native to south-eastern Papua New
Guinea and northern Australia (Jones 2011). Cherax quadricarinatus has
been introduced to many countries around the world for aquaculture,
fisheries and ornamental pet trade (Ackefors 2000; Belle et al. 2011; Lodge

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
Figure 2. Lateral (A) and dorsal (B) views of a male Cherax quadricarinatus captured in Pok
Fu Lam Country Park, Hong Kong SAR, China.
Figure 3. Carapace length distribution of Cherax quadricarinatus (n = 49) captured in Pok Fu
Lam Country Park, Hong Kong SAR, China.
0
2
4
6
8
10
12
14
16
18
<10 10-20 20-30 30-40 40-50 50-60 >60
Number of Individuals
Carapace length (mm)
Female
Male
Intersex

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
et al. 2012; Faulkes 2015; Madzivanzira et al. 2020). Escape from captivity
and deliberate release by pet owners has resulted in the establishment of
feral populations globally (Lodge et al. 2012; Madzivanzira et al. 2020).
The most likely introduction pathway of C. quadricarinatus to Hong
Kong is the deliberate release by pet owners. Live C. quadricarinatus, along
with several other non-native crayfish species, can be found for sale in several
shops in the popular “Goldfish Street” pet market in Hong Kong. Although
Hong Kong imports up to 30% of all the aquacultured C. quadricarinatus
from Australia (Jones 2011), this species is rarely consumed as food within
Hong Kong. We suspect that most C. quadricarinatus are imported as
frozen “seafood” and re-exported to China where consumption of crayfish
is common. Pok Fu Lam Country Park is an apparent “dumping ground”
for unwanted pets, probably due to its location and ease-of-access. Over
the course of this study, several other introduced species were also observed
in Pok Fu Lam Country Park Reservoir and stream pools, which included:
the red-eared slider Trachemys scripta elegans, Chinese stripe-necked turtle
Mauremys sinensis, goldfish Carassius auratus, an unidentified species of
jewel cichlid Hemichromis sp., and a breeding population of Chinese water
dragons Physignathus cocincinus.
This study observed C. quadricarinatus of multiple size classes as well as
a berried female with hatchlings in July 2020, indicating that the population of
C. quadricarinatus in Pok Fu Lam Country Park is reproducing. Most of
the C. quadricarinatus captured were small (< 40 mm carapace length).
However, this may not reflect the overall size distribution of the population.
Based on our observations, most crayfish were hiding in shelters when we
first arrived at the sampling sites. Individuals attracted by the bait would
emerge from their shelters and thus were more likely to be captured. In
contrast, the majority of C. quadricarinatus captured by Nunes et al. (2017)
using baited crayfish traps ranged between 40 to 70 mm in carapace length.
This may reflect a bias towards smaller individuals in our study. However,
the South African population sampled in Nunes et al. (2017) is a long-
established invasion, and the individuals sampled are likely to be larger
than in recently introduced populations. Continuous monitoring is
required to confirm this suspected discrepancy.
Cherax quadricarinatus may threaten native species through interspecific
competition for food and shelter. For example, Zeng et al. (2019)
demonstrated that C. quadricarinatus outcompetes the native freshwater
crab Parathelphusa maculata for shelter and that this interaction leads to
an overall displacement of the native species from areas with more
crayfish. A study in South Africa demonstrated that biotic resistance to
C. quadricarinatus by native, trophically analogous, freshwater crabs was
size and sex-dependent. For example, the female Potamonautes perlatus
native to Southern Africa, have significantly stronger maximum chela force
than female C. quadricarinatus and both sexes of another introduced

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
crayfish species Procambarus clarkii (South et al. 2020). In Hong Kong,
C. quadricarinatus may compete with functionally similar native decapods
such as Macrobrachium hainanense, M. nipponense, and Nanhaipotamon
hongkongense. Unfortunately, outside of the South African studies,
information on the ecological impacts of C. quadricarinatus is limited
(Madzivanzira et al. 2020; Morningstar et al. 2020). Pinder et al. (2019)
suggested that this species may deplete macrophyte cover and alter
invertebrate communities in Western Australia, while Williams et al.
(2001) suggested it may out compete and replace freshwater shrimp in
Puerto Rico. Further studies on the potential impacts of C. quadricarinatus
on native species are warranted.
Because of the potential negative impacts presented by C. quadricarinatus,
it is necessary to conduct a comprehensive survey of C. quadricarinatus in
Hong Kong in order to determine the extent of invasion to other streams
and reservoirs. In South Africa and Swaziland, C. quadricarinatus has been
shown to be capable of spreading at a rate of 8 km/year downstream and
4.7 km/year upstream (Nunes et al. 2017). Since most of the streams in Pok
Fu Lam Country Park are connected through the reservoir, it is highly
likely that C. quadricarinatus will colonize all the streams draining into the
basin. In Singapore, C. quadricarinatus was first reported in 2007 and has
spread to at least 3 of 13 reservoirs (Ahyong and Yeo 2007; Belle and Yeo
2010; Belle et al. 2011). Therefore, to detect new invasion fronts of this
species, the local authority in Hong Kong should consider employing
environmental DNA (eDNA) techniques, which have been demonstrated
to be feasible and reliable elsewhere (Cai et al. 2017).
Targeted plans to manage this invasive species are needed to control
their population size. Since pet abandonment is one likely reasons leading
to the occurrence of the feral crayfish population in Hong Kong,
strengthening public education is suggested to raise conservation awareness
in order to solve the problem from the root. Additional legislation (with
fines) that prohibits the release of animals and resources to enable
enforcement of the legislation should also be considered to further
discourage people from releasing animals into the wild.
Acknowledgements
We thank Hau Ka Ki Anthony and Au Ming-Fung Franco for assistance with field work. We
thank the scientific officers at Hong Kong Baptist University Department of Biology for
logistical support. We thank the Agriculture, Fisheries and Conservation Department for issuing
a permit to collect crayfish for this study. We thank the anonymous reviewers for providing
helpful comments on earlier drafts of this manuscript. We thank Ackley Lane for editing.
Ethics and Permits
The Agriculture, Fisheries and Conservation Department granted permission to possess funnel
traps for ecological surveys within Pok Fu Lam Country Park.

First record of Cherax quadricarinatus in Hong Kong
Yau and Lau (2021), BioInvasions Records ( in press)
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Supplementary material
The following supplementary material is available for this article:
Table S1. Details of surveys conducted in December 2019 to February 2020 in Pok Fu Lam Country Park: species captured, locality
and coordinates, water temperature, and air temperature.