Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August
2019 | 11(10): 14259–14267
The
soft-release of captive-born Kaiser’s Mountain Newt Neurergus
kaiseri (Amphibia: Caudata)
into a highland stream, western
Iran
Tayebe Salehi 1, Vahid Akmali 2 &
Mozafar Sharifi 3
1,2,3 Department
of Biology, Faculty of Science, Razi University, Baghabrisham 6714967346, Kermanshah, Iran.
1 salehi.t643@gmail.com,
2 v_akmali@yahoo.com, 3 sharifimozafar2012@gmail.com (corresponding
author)
Abstract: Captive breeding and reintroduction programs are
important conservation tools and are used for increasing the number of plant
and animal species worldwide. The
endemic Kaiser’s Mountain Newt Neurergus
kaiseri is listed as Vulnerable on the Red List by the International Union for Conservation of Nature (IUCN) and is amended to Appendix I of the
Convention of International Trade on Endangered Species (CITES). In the present study, in order to learn about
the survival ability of captive-born newts of N. kaiseri,
we conducted a trial translocation of 15 two-year-old captive-born N. kaiseri into the highland stream in Sartakht Village, western Iran. The survival rate of these newts
were determined in two stages, involving early acclimatization in mesh bags and
direct release in a highland brook. In 12 surveys to the translocation site, a total of 86 individuals were identified
during spring and summer. The average
survival rate during the acclimatizing phase was 98 ± 0.04 %, while an average survival rate of 12 ± 0.04 % was
obtained when the newts were released in the brook. Applying an average diurnal detection
probability obtained for the Yellow Spotted Mountain Newt Neurergus
derjugini, the overall survival rate in September
when newts began the autumn withdrawal was 13%.
These findings demonstrate that captive-born N. kaiseri
released into the wild in controlled conditions can survive during spring
and summer and provide information for future reintroduction plan of this species.
Keywords:
Captive breeding, conservation, CITES, reintroduction, trial
translocation, threatened species.
doi: https://doi.org/10.11609/jott.4981.11.10.14259-14267
Editor: Anonymity
requested. Date
of publication: 26 August 2019 (online & print)
Manuscript details: #4981 | Received 31 March 2019 | Final received 18
June 2019 | Finally accepted 06 August 2019
Citation: Salehi, T., V. Akmali &
M. Sharifi (2019).
The soft-release of captive-born Kaiser’s Mountain
Newt Neurergus kaiseri
(Amphibia: Caudata) into a highland stream,
western Iran. Journal of
Threatened Taxa 11(10): 14259–14267. https://doi.org/10.11609/jott.4981.11.10.14259-14267
Copyright: © Salehi et al.
2019. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by adequate credit to the author(s)
and the source of publication.
Funding: This study was supported by Department of Biology, Razi University,
Kermanshah, Iran.
Competing interests: The authors
declare no competing interests.
Author details: Tayebe Salehi is currently PhD student of Systematic Zoology at
Department of Biology, Faculty of Science, Razi
University. She earned her MSc from Shahid Beheshti University of Tehran. Her current research focuses
on the conservation biology of two endangered mountain newts (Neurergus kaiseri
and N. derjugini). Vahid Akmali is an Assistant Professor of Zoology in the
Department of Biology, Razi University, Kermanshah,
Iran. He tutors zoology, comparative anatomy, evolution, and biogeography
courses. In recent years his main research interest has focused on
Biospeleology. Mozafar Sharifi is a Senior Lecturer in
ecology in the Department of Biology, Razi
University, Kermanshah, Iran. In recent years, his main research interest
focuses on conservation biology of chiroptera and
amphibians. He has assisted with the conservation assessment of chiroptera and two species of Neurergus
in collaboration with the International Union for the Conservation of Nature.
Author contribution: TS was responsible for field and laboratory works and
preparation of the manuscript. VA reviewed the manuscript. MSH conducted field
surveys and reviewed and approved the manuscript.
Acknowledgements: We thank Razi University for
its support of this study as a part of the PhD Research Project of T. Salehi
(code number 19711). The permission to
collect, breed, and release Kaiser’s Mountain Newts was obtained from the Razi University ethic community under permit number:
3962022.
INTRODUCTION
The list of species categorized
as Vulnerable, Endangered, or Critically Endangered has nearly doubled in the
past two decades, and 20,000 species are estimated as endangered species on the
verge of extinction (Estrada 2014). The
release of captive-born individuals is being increasingly used as an important
tool for the restoration of endangered and threatened species around the world
(Seddon et al. 2007; Okuyama et al. 2010). The reintroduction of captive-bred animals
for establishing a viable population often fails due to a range of reasons
(Mathews et al. 2005), such as inability to avoid predators, a lack of
searching for food and inability to process food, inability to find shelter,
lack of predatory abilities, loss of social interactions with conspecifics and
orientation in a complex environment (Okuyama et al.
2010).
Various studies conducted on
reintroduced species have shown that different environmental and biological
factors contribute to the success of reintroduction projects. One of these factors is the type of release;
hard (direct) or soft (indirect) release (Serangeli
et al. 2012). Based on the hypothesis that soft-release methods will improve the
success of reintroduction, they are often included in reintroduction protocols
(Moehrenschlager & Macdonald 2003). A common soft-release method is delayed
release (or acclimatization) that prevents high rates of mortality that often
occur immediately after release (Dickens et al. 2010). In this technique, individuals are placed in
a protective enclosure at the release site, so that they can acclimatize to the
new environment gradually before the release (Sutherland 2000). In addition, long-term food availability,
habitat suitability and the season of release are other factors for the success
of reintroduction (Jule et al. 2008; Serangeli et al. 2012).
Over 32% of amphibian species
have been known as globally threatened species since the 1970s
(Stuart et al. 2004). Different factors including pollution, over-consumption,
habitat loss, climate change, and disease (both fungal and viral) play a role
in these declines. Therefore, captive
breeding programs are used increasingly to counter extinctions of wild
populations of frogs and salamanders (Gascon et al. 2007; Bodinof
et al. 2012). The drawbacks associated
with captive breeding may be less important in amphibian species due to several
life history attributes such as small body size with low space requirements,
rapid growth and high fecundity (Kinne 2004; Sharifi & Vaissi 2014). There are several reasons to translocate
animals that could generally be assigned to experimental research, to mitigate
human-wildlife conflict and conservation or population
re-establishment (Germano & Bishop 2009). The aim of the experimental reintroduction or
research is to survey the best conditions for captive-bred survival in a
release site and to improve reintroduction programs in the future (Liu et al.
2016). As a result, an experimental
approach can help to provide appropriate guidelines for the success of the reintroduction
program (Griffiths & Pavajeau 2008; Santos et al.
2009; Roe et al. 2010).
Kaiser’s Mountain Newt Neurergus kaiseri is a
species that is endemic to the southern Zagros Mountains with a restricted
distribution in the Lorestan and Khuzestan provinces. Rapid declines due to its highly fragmented
breeding habitat and also because it occupies a small range during its
reproductive period implied the extinction of this newt in the wild and is
pointed out to be one of the threatened species in Iran (Sharifi
et al. 2009). Until recently, studies
showed that localities from only four streams (in a single catchment area)
increased to 40 new geographical localities.
Therefore, this species was listed as Vulnerable by IUCN in 2017 (Mobaraki et al. 2014). Furthermore, this species has
been listed in Appendix I of the Convention of International Trade on
Endangered Species (CITES, https://www.cites.org/eng/app/appendices.php, Sharifi et al. 2009).
A conservation management plan
funded by the Mohamed bin Zayed Species Conservation Fund was initiated for The
Yellow Spotted Mountain Newt Neurergus derjugini (= Neurergus
microspilotus) in 2010. Part of this plan included the development of
a captive breeding facility (CBF) at Razi University,
Kermanshah, Iran (Vaissi & Sharifi
2015). Several laboratory studies in the
CBF on N. derjugini provided information on
growth and development (Vaissi & Sharifi 2016a,b), cannibalism (Vaissi
& Sharifi 2016b), ontogenetic changes in spot
configuration (Vaissi & Sharifi
2017), a trial reintroduction of captive-bred newts (Sharifi
& Vaissi 2014; Vaissi
& Sharifi 2018), and comparing the predatory
impact of captive-bred and free-living newts (Salehi & Sharifi
2019). Also, this project initiated a
program for captive breeding and field studies of the Kaiser’s Mountain Newt
(Image 1A) aiming to provide critical information for a conservation management
plan. These studies included sexual size
dimorphism (Sharifi et al. 2012), histomorphological
study (Parto et al. 2013; Parto
et al. 2014b), reporting chytridiomycosis (Sharifi et
al. 2014), and red-leg syndrome (Parto et al. 2014a),
delimiting the species range (Sharifi et al. 2013),
ageing and growth of species (Farasat & Sharifi 2016), reproductive morphology and sperm storage (Parto et al. 2015), and population genetic structure (Farasat et al. 2016).
Here we will use translocation
as a term referring to the release of individuals from captive origins to areas
without conspecifics into the wild for experimental evaluation of post-release
survival of captive-reared Kaiser’s Mountain Newts. Much of our discourse on translocation here
will focus on the captive breeding management and therefore on captive-release
programs. However, there was no
monitoring work on the survival of the captive-born Kaiser’s Mountain Newts
into the wild so, here we describe a trial translocation of this species. For this purpose, the experimental release
was carried out in two stages during spring and summer. The first stage involved the indirect release
of individuals into the environment for acclimatization, and in the second
stage, the newts were released directly into the environment.
The main aims of our trial
translocation were: (i) whether captive-born newts
could survive in the natural habitat during the acclimatization phase, (ii) to
determine whether acclimatized newts would be observed at the release site
after free release, and (iii) whether reintroduction of captive-born newts
could be an effective conservation strategy for the recovery of a viable
population in the future.
MATERIALS
AND METHODS
Captive breeding
The previous ex situ conservation
program on N. derjugini and their
reintroduction provided relevant experience and information for the current
work. In the spring of 2014, the first
gravid females (SVL: 173.9–174.2 mm) from Bozorgab
Stream (32.9330N & 48.4660E) in the southern Zagros
Mountains were transported to CBF. The
gravid females were detectable by their swollen bodies. They were introduced together in one aquarium
(75 × 45 × 35 cm) with a water level of about 9cm and with small pebbles. Also, the aquaria were filled with mosses and
some aquatic plants for egg attachment.
Immediately after egg laying, we introduced the eggs (due to
cannibalism) into separate rearing aquaria with aerated water. The egg stage lasted 2–3 weeks and then in
the first phase of their life they were motionless and attached their mouth
regions to plants, stones or other solid objects. In this life cycle, they consumed their
internal nutrient reserves and then were fed with Artemia
egg and shredded blood worms Glycera
dibranchiate. The larval period
lasted 8–9 months, reaching metamorphosis (loss of gills) and in this stage the
young postmetamorphs (mean SVL was 30 ± 0.59 mm and
mean body mass was 1.53 ± 0.05 g) left the water and they stayed more in the
terrestrial component of their habitat.
They were fed with a series of gradually larger food items including
blood worms, earthworm Lumbricus terrestris, and live mealworms Teneberio molitor
until they reached the scheduled release size.
Selecting newts for release
We released 15 two-year-old
individuals (Image 1B, mean SVL was 35.71 ± 2.46 mm and mean body mass was 1.61
± 0.48 g) in 2016 because individuals of smaller sizes are vulnerable to
predators and environmental factors. In
addition, larger individuals acclimatize themselves to the captive condition
and likely lose their normal behavior and
function. Prerelease
protocols included testing for diseases, normal behaviors,
and responsiveness to stimulus.
Selecting of the release site
The selected site in the present
study was a highland brook in Sartakht Village (34.7660N
& 47.1500E) in western Iran (Figure 1, Image 1C), a small
highland (1,600m) stream with permanent water discharge. This was partly selected because it was close
to a private property to which we had easy and regular access.
Acclimatization and free release
We performed a soft-release
reintroduction involving a period of acclimatization in the highland stream to
allow the newts to adjust to the environmental conditions and avoid the impact
of native predators such as crabs (Potamon bilobatum). The newts
were placed in mesh bags (46 × 30 × 36 cm) and hid under plants in release site
on three occasions (5 individuals per occasion) in 2016: 29 April, 6 May, and
13 May (Image 1D). Periods of
acclimatization were 9, 10 and 11 weeks for three occasions. We fed newts with mealworms in the first
week of acclimatization to the environmental conditions. The remaining newts from acclimatization
period were directly released into the highland brook on 15 July 2016 (Image
1E).
Visual monitoring and detection probability
The newts were monitored
on seven occasions when they were in their mesh bags until we made sure of
their relative survival during the acclimatization period. Following 70 days of acclimatization, the
newts were released in the stream and monitored by visual counts on five
occasions until 16 September 2016 when the newts began the autumn withdrawal
from the stream. Visual counts conducted
by two observers walking along the stream banks between 10.00h and 13.00h where
vegetation cover in the stream was dense and the search involved pursuing them
under plants and rocks. Visual counts
were conducted on 6 May, 13 May, 20 May, 3 June, 17 June, 1 July, 15 July, 22
July, 5 August, 19 August, 2 September and 16 September. For identification using coloration pattern
recognition, we previously photographed the dorsal surfaces of the newts using
a digital camera (Sony, DSCHX9V, 3.6V) on a tripod at a fixed height
(30cm). After capturing, each newt was
identified, measured, weighed, and the health status was checked.
Estimation of the survival rate
of the released N. kaiseri involved the
application of detection probability that was used for measuring N. derjugini (Sharifi & Vaissi 2014). This
detection probability was obtained when a known number of newts were kept in
several stone enclosures. The estimated
average detection probability for N. derjugini was
0.61 ± 0.19 SD. We used the average
detection probability as follows (Bailey et al. 2004): N = C/β where
C, β, and N are the number of individuals counted, the
probability of detection, and we adjusted the visual count respectively.
RESULTS
All of the individuals survived 100% during
transportation from the CBF to the release site. Overall, we detected 86 individuals during 12
surveys. At the end of the acclimatization
phase, we identified 13 individuals from 15 released newts within mesh bags
making the survival rate (mean ± SD) in this period 98 ± 0.04 %. We observed two dead newts on 17 June. At the end of the acclimatization period, the
body mass and SVL (mean ± SD) of the surviving newts were 1.69 ± 0.55 g and
38.33 ± 2.56 mm respectively.
In five visits from 22 July 2016 until 16 September
2016, only two released newts were found exactly at the point of release
between the mosses and herbs around the stream on 19 August and 16 September
2016. The body mass and SVL of the newts on 19 August and 16 September were
1.56g, 33.36mm and 1.33g, 35.51mm, respectively. The survival rate (mean ± SD) in this period
of 12 ± 0.04 % was considerably lower than the acclimatization phase. Based on the detection probability estimated
for N. derjugini, the observed newts after
final release were 13% of reintroduced newts.
Table 1 describes the number, SVL, body mass, percent of surviving newts
during acclimatization and free release periods and based on detection
probability.
DISCUSSION
Release in controlled conditions has revealed the
success of the acclimatized animals after release and the higher rates of
individual survival (Mitchell et al. 2011).
The soft-release of captive-born individuals has shown that this kind of
release could provide an opportunity to adapt to the new environment, minimize
mortality, and reduces the anxiety (Moseby et al.
2014). In the present study, we tested
the survival rate in the acclimatization phase and during free release. The present trial translocation showed that
that two-year-old captive-born newts would be able to survive in a natural
habitat during acclimatization phase and the average survival rate of two year
old newts in this period without humans was 98%. The high rate of survival during the
acclimatization period is partly attributable to the protective mesh bags that
avoid the impact of native predators and provides more time to adapt to natural
conditions. Also, a similar
translocation by Sharifi & Vaissi
(2014) on N. derjugini that is a closely
related species to N. kaiseri had demonstrated
that young captive-born newts (in the relatively protected enclosure) can
survive to the second growing season in the wild.
The survival rate in the free release phase was 12% of
the released individuals. The present
trial translocation showed that the survival of two-year-old captive born newts
in the mesh bags remained high in the natural habitat during the
acclimatization phase. We did not
observe any newts on 22 July and 5 August, while in the next surveys two newts
were found. Therefore, it is possible
that more newts survived and we were not able to find them. Failure to find these newts is likely due to
the small size of the released newts and the complexity of the environment.
McFadden et al. (2016) encountered major difficulties in finding the Northern
Corroboree Frog Pseudophryne pengilleyi
after reintroduction, due to their small size and cryptic behavior. The study by Randall et al. (2016) on the
Northern Leopard Frog Lithobates pipiens revealed another major difficulty in the
reintroduction program: the low number of individuals released and complexity
of the habitat. Also, Bell et al. (2010)
carried out the release with low numbers (<30) of the Maud Island Frog Leiopelma pakeka
and demonstrated that the risk of predators had probably reduced the success of
translocation.
We observed that the newts were moving to the wet
areas around the water and hiding under vegetation cover at the time of the
release. In the next surveys after the free
release, some individuals were found close to the release site. Studies show soft-releases can increase site
fidelity that is a common aspect of reintroductions with many amphibians (Wanless et al. 2002; Attum et al.
2011). The newts that were observed on
19 August and 16 September after direct release were precisely hidden in the
vegetation cover in the initial release site.
Moreover, we needed the transmitter for study dispersal and home range
of newts after reintroduction while the results show that the use of the
transmitter in released individuals can lead to vulnerability and an increase
in the likelihood of their death (Miloski & Titus
2008). In addition, studies on
salamanders have used few external transmitters because of the movement of salamanders
and the complexity of their habitat (Dervo et al.
2010); and internal transmitters have been used in larger species such as the
Spotted Salamander Ambystoma maculatum
(McDonough & Paton 2007) and Chinese Giant Salamander Andrias
davidianus (Zhang et al. 2018). In a study that was conducted to investigate
the survival of 22 Chinese Giant Salamanders after reintroduction the internal
transmitter was used. It, however, took
too much time for the salamanders to recover from surgery (they needed almost
four months to fully recover). Furthermore internal transmitters only last for
about one year, and it is difficult to replace expired transmitters with new
units, thus longer monitoring plans could not be applied (Zhang et al. 2018). The use of the internal transmitter in this
study was impossible due to the low number and small size of the individuals
that would increase mortalities at the beginning of release. Sharifi & Afroosheh (2014) have been able to effectively use
photographic identification method as a non-invasive method in
N. derjugini, the sister species of N. kaiseri to determine the home range of this newt during
a breeding season. The result of this
study showed very small home range and high site fidelity of N. derjugini.
CONCLUSION
The present trial on the soft-release of two-year-old
captive born Kaiser’s Mountain Newts in spring and summer involving an
acclimatization period and a free release phase showed a high survival rate in
the first stage, and a lower survival rate in the second stage. There were major difficulties including small
size, cryptic behavior and complexity of habitat, and
low number of released newts during direct release. Possible reasons for the failure of
translocation can be predation or lack of site fidelity after free
release. We hope the findings of this
experimental research help future reintroduction programs. We suggest a larger number of newts in a
predator-free release environment in future translocations. Also, we encourage comparison of trained and
untrained newts in soft-release strategies in future reintroductions. Information on all studies will open the door
for a successful reintroduction of N. kaiseri.
Table 1. Date and number of the
released individuals of Neurergus kaiseri into the wild, the age, SVL and body mass of
released individuals, number of observed individuals during acclimatization
phase, percent of individuals observed after and before free release phase,
percent of surviving individuals based on next surveys and an estimate of the
survival of newts outside mesh bags
based on detection probability (db).
Date |
No.
released |
No.
observed |
SVL
(mm) |
Body
mass (mg) |
%
observed |
%
survived |
%
survived based on dp |
29.iv.2016 |
5 |
- |
34.31 ±
2.23 |
1.24 ± 0.16 |
- |
|
|
6.v.2016 |
5 |
5 |
35.62 ±
2.57 |
1.48 ± 0.22 |
100% |
|
|
13.v.2016 |
5 |
10 |
37.21 ±
2.08 |
1.65 ± 2.11 |
100% |
|
|
20.v.2016 |
0 |
15 |
35.71 ±
2.46 |
1.61 ± 0.48 |
100% |
|
|
3.vi.2016 |
0 |
15 |
35.91 ±
2.35 |
1.57 ± 3.21 |
100% |
|
|
17.vi.2016 |
0 |
13 |
36.04 ±2.49 |
1.68 ± 3.10 |
87% |
|
|
1.vii.2016 |
0 |
13 |
36.55 ±
2.55 |
1.69 ± 3.50 |
100% |
|
|
15.vii.2016 |
13* |
13 |
38.33 ±
2.56 |
1.69 ± 3.55 |
100% |
|
|
22.vii.2016 |
0 |
0 |
|
|
0% |
15% |
0 % |
5.viii.2016 |
0 |
0 |
|
|
0% |
15% |
0 % |
19.viii.-2016 |
0 |
1 |
|
|
8% |
15% |
13 % |
2.ix.2016 |
0 |
0 |
|
|
0% |
8% |
0 % |
16.ix.2016 |
0 |
1 |
|
|
8% |
8% |
13 % |
Note: The
star mark is the date of free release into the wild outside the mesh bags. |
For
figures & image – click here
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