ArticlePDF Available

To what extent does temperature affect sex ratio in red cherry shrimp, neocaridina davidi? The scenario global warming to offspring sex ratio

Authors:

Abstract and Figures

An invasive freshwater shrimp, Red Cherry Shrimp (Decapoda: Caridea: Atyidae), is naturally distributed in fresh water habitats of Asia. This forage species has an important role in aquatic ecosystems by transferring planktonic production into higher trophic levels mainly including fish and aquatic animals. However, temperature strongly affects sex ratio and in turn offspring quantity. In order to determine the effect of temperature on incubation period, egg yield, offspring sex ratio as well as survival, a comprehensive experiment was conducted at three temperatures (20, 23 and 26ºC). Significant differences among temperatures for hatching period were an expected result. Higher survival and more eggs were achieved at 26ºC comparing the lower experimental temperatures. The female/male ratio, which was 80% at 20°C and approximately 50% at 23ºC, drastically dropped to 18% at 26°C. This ratio may drop to 0% at higher temperatures, which are tolerance limits for Red Cherry Shrimp. Therefore, in sex-dependent selective breeding, the temperature should be taken into consideration. Consequently , as temperature increases the sex ratio of the offspring increases in favour of the male. The continuation of global warming and rising above 26°C may be an important source of stress on the natural sustainability of Red Cherry Shrimp stocks.
Content may be subject to copyright.
© by PSP Volume 26 No. 12/2017 pages 7575-7579 Fresenius Environmental Bulletin
7575
TO WHAT EXTENT DOES TEMPERATURE AFFECT SEX
RATIO IN RED CHERRY SHRIMP, NEOCARIDINA
DAVIDI? THE SCENARIO GLOBAL WARMING TO
OFFSPRING SEX RATIO
Ramazan Serezli1,*, Mehmet Sina Atalar1, Sevim Hamzacebi1, Ilker Zeki Kurtoglu2, Ilhan Yandi3
1Izmir Katip Celebi University, Faculty of Fisheries and Aquaculture, 35620, Izmir, Turkey
2Recep Tayyip Erdogan University, Faculty of Fisheries and Aquaculture, 53100, Rize, Turkey
3Recep Tayyip Erdogan University, Maritime Faculty 53100, Rize, Turkey
ABSTRACT
An invasive freshwater shrimp, Red Cherry
Shrimp (Decapoda: Caridea: Atyidae), is naturally
distributed in fresh water habitats of Asia. This for-
age species has an important role in aquatic ecosys-
tems by transferring planktonic production into
higher trophic levels mainly including fish and
aquatic animals. However, temperature strongly
affects sex ratio and in turn offspring quantity. In or-
der to determine the effect of temperature on incuba-
tion period, egg yield, offspring sex ratio as well as
survival, a comprehensive experiment was con-
ducted at three temperatures (20, 23 and 26ºC). Sig-
nificant differences among temperatures for hatch-
ing period were an expected result. Higher survival
and more eggs were achieved at 26ºC comparing the
lower experimental temperatures. The female/male
ratio, which was 80% at 20°C and approximately
50% at 23ºC, drastically dropped to 18% at 26°C.
This ratio may drop to 0% at higher temperatures,
which are tolerance limits for Red Cherry Shrimp.
Therefore, in sex-dependent selective breeding, the
temperature should be taken into consideration. Con-
sequently, as temperature increases the sex ratio of
the offspring increases in favour of the male. The
continuation of global warming and rising above
26°C may be an important source of stress on the
natural sustainability of Red Cherry Shrimp stocks.
KEYWORDS:
Neocaridina, heterapoda, extinction, global warming, sex
ratio
INTRODUCTION
Meiofauna including shrimps has an important
ecological role in aquatic ecosystems by transferring
planktonic production into higher trophic levels [1,
2]. In addition, shrimps have a potential economic
importance both in aquaculture and in aquarium sec-
tor as an ornamental species [3].
The Atyid shrimp Neocaridina davidi (Bouvier
1904), popularly known as “Red Cherry Shrimp
(RCS)”, is a small size freshwater shrimp distributed
throughout Taiwan, Vietnam, Korea, Japan, Russia
and China [2, 4, 5, 6] and it is able to tolerate much
colder temperature regimes [7].
RCS is also a popular species for fresh water
aquariums in Turkey [8]. It is very adaptable and
easy to culture but the sex ratio is an important factor
to consider because of a certain ratio, as in other
aquatic animals, is necessary for the continuity of the
generation [9].
Sex-determining mechanisms are broadly di-
vided into two major categories: genetic and envi-
ronmental [10]. The most important environmental
sex determining factors are temperature and photo-
period. These environmental parameters stimulate
and maintain gametogenesis and other reproductive
processes in freshwater invertebrates [1].
Aquatic animals adapt to the conditions they
are living in. If they cannot achieve this, growth dis-
turbances, physiological disorders, and stopping of
the ureamia, as well as disorders of egg development
and embryo development, are antagonistic.
According to climate forecasting models, it is
estimated the global mean temperature will increase
3 degree by 2050 and 6 degree by 2100 [11], this
may lead to major changes in biodiversity. In this
process, the tolerance to upper temperature limits of
aquatic animals will be determinant for their sur-
vival. In this study, female/male ratios, survival rates
and embryonic development times of the N. davidi
species, which is an important species for aquatic en-
vironment, were determined at three different (20,
23, 26°C) temperatures.
MATERIALS AND METHODS
Red cherry shrimp (N. davidi), about 1.5-2.0
cm, were supplied from local producers. The
shrimps were selected from 1.5-2.0 cm adult individ-
uals. They were evenly distributed to nine glass
aquaria. Java moss (Vesicularia dubiana) was added
in equal amounts to aquariums which have 5 cm of
basalt sand on the bottom. The study was conducted
© by PSP Volume 26 No. 12/2017 pages 7575-7579 Fresenius Environmental Bulletin
7576
as three replicates for each experimental tempera-
ture. Water temperatures were provided by aquarium
heaters (Atman-100 W) with ±0.5°C precision. Fe-
males with eggs in the dorsal were taken into 0.8 liter
containers individually after mating and observed
twice a day. After hatching, females are not paired
again. The dead larvae were immediately removed
and noted.
In the study, filtered and UV-treated tap water
was used and half of the rearing water was ex-
changed per week. Brood shrimp and their larvae
were fed ad libitum with commercial shrimp feed
(containing 40% crude protein) twice a day (09:00
and 18:00). Females were removed after the larvae
hatched separately, and number of larvae produced
by each female was recorded. Sex differentiation
was determined approximately after 3 months, males
identified as they are smaller and there are no
longitudinal stripe on dorsal females identified as
they have the formation of curves in the bellies, they
are bigger and have longitudinal stripe on dorsal.
The pH was 7.5-8.0, the conductivity was 200-400
μS, the TDS (total dissolved matter) values were in
the range of 100-200 ppm and oxygen >4 ppm.
Lighting was provided for 12 hours by using auto-
matic timer.
Sex determination of the Red Cherry Shrimp is
quite obvious. Females are larger than the males,
have a much darker red coloration and also have a
curved underbelly. Male shrimp have very little red
coloration and has a straight lateral line with no
curved shape.
Statistical Analysis. All statistical analysis
was performed using SigmaPlot (SigmaPlot 14.0,
Systat Software Inc., San Jose, CA, USA). Differ-
ences were deemed to be significant at P<0.05 and
P<0.01. To assess normality of distributions a Kol-
mogorov-Smirnov test was used and homogeneity of
variances was tested using F test. The data without
equal variance and/or normal distribution was tested
using Kruskal-Wallis whereas data with normal dis-
tribution and equal variance was subjected to a one-
way ANOVA. The significance of the difference be-
tween means was tested using Holm-Sidak and
Tukey All Pairwise Multiple Comparison Proce-
dures. Values are expressed as mean ± mean’s stand-
ard error. The chi-square test (w2) was used to deter-
mine whether the observed sex ratio differed from
the expected 1:1.
RESULTS
Red cherry shrimps were kept for 180 days at
three different temperatures. Egg development and
larval output were monitored at 20, 23 and 26°C dur-
ing the experiment. After egg formation at the dorsal
(also called as saddle), once shell changes and then
mating was observed. It was decided that the eggs
were fertilized by the fact that the eggs on the back
of the mating females passed through the abdomen,
was visually inspected. After three months, the sex
of the offspring can be clearly determined. Thirty
different offspring from each experimental group
were taken at the same temperature. Duration of egg
incubation, the number of offspring, the percentage
of female and male of offspring and survival rates
were determined.
The experiment conducted at three different
temperatures, it was observed that as the temperature
dropped, the number of eggs decreased. At 20, 23,
and 26°C, the fecundity are; 24.21±0.67,
32.31±0.70, and 34.44±0.60, respectively. It has
been seen that female produced a maximum of 45
eggs (Fig. 1).
FIGURE 1
The number of eggs produced by adult N. davidi
at 20, 23 and 26ºC. Vertical bars indicate stand-
ard error of the mean. Significant difference at
20 ºC (**P <0.01).
FIGURE 2
The hatching duration of N. davidi reared at 20,
23 and 26ºC. Kruskal-Wallis One Way Analysis
of Variance and Tukey All Pairwise Multiple
Comparison procedure. Vertical bars indicate
standard error of the mean. Different letters in-
dicate significant difference (P < 0.01).
Egg development is accelerated with increasing
temperature, increasing temperature decreases the
output time of the eggs. Eggs were hatched at
32.47±0.23 days at 20°C, 29.39±0.20 days at 23°C,
© by PSP Volume 26 No. 12/2017 pages 7575-7579 Fresenius Environmental Bulletin
7577
28.22±0.16 days at 26°C. The incubation period was
determined to be between 25 and 37 days, depending
on the water temperature (Fig. 2).
In three experimental groups (20, 23, 26°C), the
ratios of the females were; 82.76±0.37, 52.15±0.41,
and 20.73±0.33, respectively (Fig. 3).
FIGURE 3
The sex ratio (female/male) of N. davidi reared at
20, 23 and 26ºC. One Way Analysis of Variance
and Holm-Sidak All Pairwise Multiple Compari-
son Procedure. Error bars indicate ±SD. Differ-
ent letters indicate significant difference (P <
0.05).
Survival rates were not related to temperature.
The survival rates in the three groups (20, 23, 26°C)
were; 86.15±0.81, 89.78±0.46, 90.13±0.30 respec-
tively (Fig. 4).
FIGURE 4
The mean survival of N. davidi reared at 20, 23
and 26ºC. Kruskal-Wallis One Way Analysis of
Variance and Tukey All Pairwise Multiple Com-
parison procedure. Vertical bars indicate stand-
ard error of the mean. Significant difference at
20ºC (**P <0.01).
It is also an important finding that cherry
shrimp eggs are fertilized after each pairing, not
paired females throw out the not fertilized eggs, and
that they do not carry eggs from the dorsal (saddle)
part to the abdomen.
DISCUSSION
Temperature and photoperiod are the two most
important factors affecting gametogenesis. The tem-
perature is also effective in the formation of gametes
sex. Studies of different species on the effect of tem-
perature on gender formation exist [12, 13, 14]. In
these studies, the sex ratio changes depending on the
temperature and the effects of different temperatures
on the female/male ratio were investigated. How-
ever, there is very little information available on red
cherry shrimp N. davidi. Tropea et al. [5] determined
growth, development and sex ratios at three different
temperatures (24, 28, 32°C) in their study of red
cherry shrimp. As the temperature increases, the
number of males increases similarly to our study.
However, 28 and 32ºC are risky for the growth and
development of this type. Weber and Traunspurger
[2] conducted experiments with N. davidi at 19-
20ºC. According to our observation, it is appropriate
to grow these shrimps in the range of 20-23ºC.
Many researchers have studied the effect of
temperature on fish sex ratio [12-15]. In these stud-
ies, it is reported that the decrease in the male ratio
is generally caused by the increase in temperature.
Luckenbach et al. [13], conducted a study on
southern flounder (Paralichthys lethostigma) and
found that the female ratio was low (18°C) and high
(28°C) temperatures, so temperature affects the sex
ratio.
When it comes to cultivation, sometimes fe-
male and sometimes male raising may be required.
For example, male guppies are demanding more be-
cause they have attractive colors. On the other hand,
females are preferred for fish breeding, while males
are preferred for tilapia breeding [14].
External differentiation between female and
male takes place during the second month after post
larval transformation as mentioned before [16].
Compos-Ramos et al. [16] studied the Li-
topenaeus vannamei and found that the female/male
ratio did not change and was it was 50% at 18 and
32°C.
It was determined the embryonic development
of N. denticulata sinensis that lasted for 15 days at
27°C water temperature, and each brood produced
21-51 larvae, large brood produced more larvae, and
larvae became an adult after 75 days [3]. We have
determined that the duration of the larvae output is
between 26 and 33 days, depending on the tempera-
ture. This difference may be due to species variation
or from the following phases. In our study, we cal-
culate time length between eggs transferred to fe-
males abdominal to grow as larvae. The female/male
ratio is important to keep the natural balance and
generation. Nowadays, when the global warming
problem is on the rise, it is necessary to continue to
study how this affects the generation of the living
things. As the female/male ratios of natural popula-
© by PSP Volume 26 No. 12/2017 pages 7575-7579 Fresenius Environmental Bulletin
7578
tions are affected by temperature changes [17], fu-
ture generations can be affected by extinction or ge-
netic disorders. In this study, it was determined that
the female ratio at temperatures of below 23°C and
the male ratio at temperatures between 23 and 26°C
increase. Increase or decrease of temperature affects
female/male ratio in N. davidi.
Sex determination mechanisms produce the sex
ratio, a key demographic parameter crucial for pop-
ulation viability [18]. As a conclusion, red cherry
shrimp (N. davidi) stock f/m ratio rate dramatically
changed in favour of female subjects, and survival
rate in favour of female subjects with increasing wa-
ter temperature from 23 to 26°C. These findings pro-
vide an important clue to the sustainability of natural
ecosystems as well as a result for aquarium hobby-
ists. The radical increase in global warming will also
affect the aquatic ecosystem mean, minimum and
maximum water temperature values. Similar studies
on ecosystem indicator species will allow valuable
information about the sustainability of these species.
By correlating these data with global warming, an
opportunity will be provided for future projections
on ecosystem sustainability.
ACKNOWLEDGEMENTS
This study was supported by the Scientific Re-
search Fundation of Izmir Katip Celebi University,
Project Number: 2014-TYL-SUUF-0023.
REFERENCES
[1] Soomro, A.N., Suzuki, H., Kitazaki, M., Yama-
moto, T. (2011) Reproductive aspects of two
atyid shrimp Caridina sakishimensis and
Caridina typus in head water streams of Kikai-
jima Island, Japan. Journal of Crustacean Biol-
ogy 31, 41-49.
[2] Weber, S., Traunspurger, W. (2016) Influence
of the ornamental red cherry shrimp Neocaridi-
na davidi (Bouvier, 1904) on freshwater meio-
faunal assemblages. Limnologica 59, 155161.
[3] Nur, F.A.H., Christianus, A. (2013) Breeding
and Life Cycle of Neocaridina denticulata
sinensis (Kemp, 1918). Asian Journal of Animal
and Veterinary Advances 8 (1), 108-115.
[4] Shih, H.-T., Cai, Y. (2007) Two new species of
the land-locked freshwater shrimp genus, Neo-
caridina Kubo, 1938 (Decapoda: Caridea: Atyi-
dae), from Taiwan, with notes on speciation on
the island. Zoological Studies 46, 680-694.
[5] Tropea, C., Stumpf, L., Greco, L.S.L. (2015) Ef-
fect of temperature on biochemical composi-
tion, growth and reproduction of the ornamental
red cherry shrimp Neocaridina heteropoda het-
eropoda (Decapoda, Caridae). Plos One 10 (3),
e0119468.
[6] Pantaleao, J.A.F., Gregati, R.A., da Costa, R.C.,
Lopez-Greco, L.S., Negreiros-Fransozo, M.L.
(2017) Post-hatching development of the orna-
mental “red cherry shrimp” Neocaridina davidi
(Bouvier, 1904) (Crustacea Caridae, Atyidae)
under labboratorial conditions. Aquaculture Re-
search 48, 553-569.
[7] Klotz, W., Wilhelm Miesen, F.W., Hullen, S.,
Herder, F. (2013) Two Asian fresh water shrimp
species found in a thermally polluted stream
system in North Rhine-Westphalia, Germany.
Aquatic Invasions 8, 333-339.
[8] Turkmen, G., Karadal, O. (2012) The Survey of
the Imported Freshwater Decapod Species via
the Ornamental Aquarium Trade in Turkey.
Journal of Animal and Veterinary Advances 11
(15), 2824-2827.
[9] Korpelainen, H. (1990) Sex-Ratios and condi-
tions required for environmental sex determina-
tion in animals. Biol Rev Camb Philos Soc. 65,
147-184.
[10] Goto-Kazeto, R., Abe, Y., Masai, K., Yamaha,
E., Adachi, S., Yamauchi, K. (2006) Tempera-
ture-dependent sex differentiation in goldfish:
Establishing the temperature-sensitive period
and effect of constant and fluctuating water tem-
peratures. Aquaculture 254, 617-624.
[11] Hayhoe, K., Wake, C., Anderson, B., Liang,
X.Z., Maurer, E., Zhu, J., Bradbury, J., De
Gaetano, A., Stoner, A.M., Wuebbles, D. (2008)
Regional climate change projections for the
Northeast USA. Mitigation and Adaptation
Strategies for Global Change 13, 425-436.
[12] Wang, H.P., Gao, Z.X., Rapp, D., O’Bryant, P.,
Yao, H., Cao, X.J. (2014) Effects of temperature
and genotype on sex determination and sexual
size dimorphism of bluegill sunfish Lepomis
macrochirus. Aquaculture International Sympo-
sium on Genetics in Aquaculture XI, 420421,
Supplement 1, S64-S71.
[13] Luckenbach, J.A., Godwin, J., Daniels, H.V.,
Borski, R.J. (2003) Gonadal differentiation and
effects of temperature on sex determination in
southern flounder (Paralichthys lethostigma).
Aquaculture 216, 315-327.
[14] Azaza, M.S., Dhraief, M.N., Kraiem, M.M.
(2008). Effect of water temperature on growth
and sex ratio of juvenile Nile Tilapia Oreo-
chromis niloticus (Linnaeus) reared in geother-
mal water in the south of Tunisia. J. Thermal Bi-
ology 33, 98-105.
[15] Cheung, W.W.L., Sarmiento, J.L., Dunne, J.,
Frölicher, T.L., Lam, V.W.Y., Palomares,
M.L.D., Watson, R., Pauly, D. (2012) Shrinking
of fishes exacerbates impacts of global ocean
changes on marine ecosystems. Nature Climate
Change 3, 254-258.
© by PSP Volume 26 No. 12/2017 pages 7575-7579 Fresenius Environmental Bulletin
7579
[16] Campos-Ramos, R., Garza-Torres, R., Guer-
rero-Tortolero, D.A., Maeda-Martínez, A.M.
and Obregón-Barboza, H. (2006) Environmen-
tal sex determination, external sex differentia-
tion, and structure of the androgenic gland in the
Pacific white shrimp Litopenaeus vannamei
(Boone). Aquaculture Research 37, 1583-1593.
[17] Baroiller, J.F., D’Cotta, H. (2001) Environment
and sex determination in farmed fish. Compara-
tive Biochemistry and Physiology Part C 130,
399-409.
[18] Ospina-Alvarez, N., Piferrer, F. (2008) Tempe-
rature-dependent sex determination in fish re-
visited: prevalence, a single sex ratio response
pattern, and possible effects of climate change.
Plos One 3 (7), 28-37.
Received: 17.08.2017
Accepted: 18.09.2017
CORRESPONDING AUTHOR
Ramazan Serezli
Izmir Katip Celebi University, Faculty of Fisheries,
Department of Aquaculture, 35620, Cigli, Izmir,
Turkey.
e-mail: rserezli@gmail.com
... Temperature is also known as the most important environmental, sex determining factor for aquatic species [18]. Some studies show that water temperature can affect the sex ratio of some fish species, as in tilapia [19][20][21], guppy [22], medaka [23], and european sea bass [24], and of some crustaceans namely Porcellionides pruinosus (Isopod) [25], Tigriopus californicus (Copepod) [26], and Neocaridina davidi (Caridea) [18]. ...
... Temperature is also known as the most important environmental, sex determining factor for aquatic species [18]. Some studies show that water temperature can affect the sex ratio of some fish species, as in tilapia [19][20][21], guppy [22], medaka [23], and european sea bass [24], and of some crustaceans namely Porcellionides pruinosus (Isopod) [25], Tigriopus californicus (Copepod) [26], and Neocaridina davidi (Caridea) [18]. Knowledge of the extent to which temperature affects sex ratios is relevant to gauge potential threats of rising temperature on fish populations [27]. ...
... Male ratio was higher at low temperature treatment (24 • C) than for the other temperature treatments (p < 0.05), which indicated a possibility of water temperature having an affect on sex ratio in mud crab, such as has been commonly reported in teleostei fish [19][20][21][22][23][24], and also in some crustaceans [18,25,26]. Interestingly, male ratio produced in this study was higher at low temperature (24 • C), whereas in teleostei fish, high temperature of ≥28 • C and aboveusually produces higher male ratio [19][20][21]. ...
Article
Full-text available
This study was carried out to determine the physiological changes (survival, growth, molting cycle, sex differentiation, and gill condition) of mud crab, Scylla paramamosain crablet at different water temperatures of 24, 28 and 32 °C, and ambient temperature of 27 to 30 °C. Thermoregulatory behavior, represented by preferred temperature (29.83 ± SD 2.47 °C), critical thermal minimum (17.33 ± SD 0.58 °C), critical thermal maximum (40 ± SD 0.00 °C), and thermal tolerance interval (22.67 ± SD 0.58 °C), were checked for Crablet 1 stage only (with ambient temperature as acclimation temperature).Both low (24 °C) and high (32 °C) temperatures were associated with lower growth performance, and survival rate (p < 0.05), in comparison with both 28 °C and ambient temperature treatments.Male ratio at low temperaturetreatment (24 °C) was higher (80.09 ± SD 18.86%) than for other treatments (p < 0.05), observed as 44.81 ± D 10.50%, 41.94 ± SD 19.44%, and 76.30 ± SD 5.13% for 28 °C, 32 °C and ambient temperature treatments, respectively. However, there was no significant difference observed between 24 °C, 28 °C, and ambient temperature treatments. Anatomical alterations of gill lamellae of S. paramamosain crablet for both 32 °C, and 24 °C treatments, appeared thinner and paler than at both 28 °C, and ambient temperature treatments. Based on this study, temperature of 28 to 30 °C was recommended as the optimal temperature for the long-term nursery phase of S. paramamosain.
... For the vast majority of aquatic species (including crustaceans), sex determination is a secondary process (sex is determined after a considerable time period post hatching) (Abucay et al., 1999;Kato et al., 2011;Darnell et al., 2013). For aquatic crustaceans, sex is usually determined 45-90 days after hatching with the duration species-specific but also depends on some environmental variables including temperature, salinity and nutrition (Huang and Chou, 2015;Serezli et al., 2017;Levy et al., 2019). But the internal biological processes (including changes in expression of candidate gene/s, physiological and biochemical alterations) for sex determination can be initiated several days to weeks beforehand, depending on species (Rigaud et al., 1997;Kato et al., 2011;Tropea et al., 2015;Loughland and Seebacher, 2020). ...
... However, there is also sex specific sensitivity to temperature fluctuation; males are sensitive (cause higher rates of mortality) to high temperatures in some species while females show this tendency for other species (Rigaud et al., 1997;Kato et al., 2011;Darnell et al., 2013;Mat et al., 2017;Serezli et al., 2017). Testing the effect of temperature only on sex ratios can be counter-productive in this regard; instead, an integrative approach (physiological traits including growth, metabolism and developmental duration, coupled with changes in expression of thermal stress response and sex determining genes) would be reliable. ...
... Relatively higher growth performance, the highest survivability rate (64 %) and almost equivalent proportion of sex ratios were obtained (51 % male and 49 % female) at the control temperature (28℃) indicating an optimum condition for the P. monodon larvae. At optimum temperature organisms show better growth performance, higher survivability and equal proportions of sex ratios (Serezli et al., 2017;Acquafredda et al., 2019). In tropical environments, aquatic species inhabit at temperature ranges very close to their maximum thermal tolerance limit (Val et al., 2006). ...
Article
Full-text available
Temperature is an important abiotic factor influencing growth, development, metabolic performance and sex determination of aquatic organisms. The present study was conducted to test the effect of six different temperature levels (24℃, 26℃, 28℃ as control, 30℃, 32℃ and 34℃) on the physiological (growth, developmental durations, survivability, sex ratios and O 2 consumption) and genetic (changes in expression pattern of seven candidate genes: three male sex determining genes, three female sex determining genes and a single thermal stress response gene) aspects of black tiger shrimp (Penaeus monodon) larvae. Temperature treatments significantly altered the growth performance of shrimp individuals (P < 0.05) with the highest growth performance obtained at 32℃, moderate levels were obtained at 28− 30℃ and the lowest levels were obtained at the remaining temperatures. Temperature treatments significantly shortened the larval developmental durations at 28℃, 30℃ and 32℃ (required 44-46 days for sex differentiation) while 52-63 days were required at 24℃, 26℃ and 34℃. Temperature treatments also altered sex ratios of experimental P. monodon individuals; significantly higher (P < 0.05) proportions of males (coupled with higher expression levels of male sex determining genes) were obtained at lower temperatures (24℃ and 26℃) while larger proportions of females (with higher expression levels of female sex determining genes) were obtained at higher temperature levels (30℃, 32℃ and 34℃). The thermal stress response gene, heat shock protein (HSP70) showed constant expression levels at 28℃ but higher expression levels were obtained at other temperatures. Results imply that higher temperature can significantly increase the expression of female sex determining genes to produce larger proportions of females in P. monodon that in turn can help to improve aquaculture production.
... Mizue and Iwamoto (1961) briefly reported on a successful overwintering of this shrimp in Japanese freshwaters; however, neither water temperature nor other environmental conditions were specified in the publication; Oh et al. (2003) found this shrimp successfully reproducing and overwintering in one Korean temperate stream, and our data support this finding. Moreover, Serezli et al. (2017) suggested that lower water temperature (below 23°C) causes a female-biased sex ratio in the population, which is crucial for population viability. ...
... On the other hand, we found the red cherry shrimp also occurs in non-thermal streams. Hence, even if the red cherry shrimp is generally perceived as an invasive species (Serezli et al., 2017), our findings potentially raise the predicted invasiveness of this species, which was assessed as a medium-risk in previously analyzed markets trading in ornamental decapods (Uderbayev et al., 2017;Weiperth et al., 2018). Although we have no data about any symbionts attached on the carapace surface of captured shrimps, the potential introduction of bdelloid rotifers, stalked protozoans, and scutariellid temnocephalidans previously found on shrimps imported from Indonesia (Patoka et al., 2016a) cannot be excluded, and the probability of these symbionts establishing new populations via shrimp introductions is unknown. ...
Article
Full-text available
The international pet trade has caused numerous introductions of non-native species globally. This is true also for freshwater decapod crustaceans including the red cherry shrimp. This tiny creature has been previously found in thermally-polluted waters in Europe (Germany and Poland). Here we present its first occurrence in Hungary and in the entire Carpathian Basin. The species was sampled once per month over one year, from November 2017 to November 2018 in a natural thermal pond (spa) and also in an adjoining non-thermal brook in Miskolctapolca, Hungary. Shrimps were preyed upon by adult fishes in the locality but many individuals, including ovigerous females and juveniles, were recorded within the survey continuously. The density of shrimps was positively correlated with the water temperature, despite some individuals being found in the non-thermal stream and also in winter. We consider that the population of this species in Hungary is now well-established and self-sustaining.
... Thirdly, non-native decapods exhibited variable responses to climate change, with most species (29 out of 32 studied species, some species repeated across multiple publications) significantly affected by climate change. Nearly half of the studied non-native species were also projected to experience decreased habitat suitability, population abundance survival and fecundity in their introduced ranges (see Olsson et al., 2010;Capinha et al., 2012Capinha et al., , 2013Gallardo & Aldridge, 2013;Hansen et al., 2013;Serezli et al., 2017;Préau et al., 2019), cautioning against the generalisation of non-native decapods benefitting from climate change. ...
Article
Freshwater decapod crustaceans, with representatives from four main taxonomic groups (Anomura, Astacidea, Brachyura, Caridea), form a large and prominent functional group distributed globally across all types of freshwater habitats. Freshwater decapods play critical ecological roles in aquatic communities and ecosystems, and at the same time have widespread cultural and economic significance. A large proportion of freshwater decapods are imperilled by threats including pollution, habitat loss, invasive species, and importantly, climate change. Direct impacts of climate change, as well as its synergistic effects with other threats, pose a substantial but potentially understudied and possibly even underestimated risk to the conservation of freshwater decapod crustaceans. We assessed patterns of climate change impacts on freshwater decapods, as well as the extent of related research, at a global scale. Based on a comprehensive literature survey of all years up to November 2019, we found that only 49 publications, starting from the first relevant article in 2003, contained empirical evidence of climate change effects on freshwater decapods, with a total of 145 native and 11 non-native freshwater decapod species studied in relation to climate change. Climate-change research has also been increasing for all four groups, but more than half of the literature included the freshwater crayfishes Astacidea. We also found a strong bias towards the Australasian region in climate-change research in freshwater decapods, while no published studies were recorded in the Oceania biogeographic region. Importantly, almost three-quarters of native freshwater decapod species studied were projected/reported to be significantly affected by climate change, while more than 90% of the non-native freshwater decapod species studied were projected/reported to be significantly affected by climate change. Considering the severe impacts demonstrated for several species, and coupled with the notable taxonomic and geographic gaps in research into the rest of the freshwater decapods, there is an urgent need for greater representation in climate-change research across species and in regions of high diversity (such as the Neotropical, Afrotropical, and Indomalayan regions), in order for conservation interventions and measures to be beneficial to the most threatened groups.
... However, the sex ratio in both shrimps species was similarly skewed toward females. Temperature severely affects the sex ratio in N. davidi, with females being more prevalent at lower temperatures (80% at 20°C) and males at higher temperatures (Serezli et al. 2017). The water temperature of Békás Pond fluctuates over time, with the lowest temperature being 21.9°C near its outlet (Weiperth et al. 2019). ...
Article
Full-text available
The present contribution is the first record of ornamental freshwater shrimp Caridina babaulti from European open waters and the first evidence of introduction outside its native range. Among 120 non-native freshwater shrimps collected in Miskolctapolca, Hungary, seven individuals (5.8%) were identified as C. babaulti and included one ovigerous female, while the others (94.2%) were Neocaridina davidi. Morphological analysis and the Standard DNA Barcoding Procedure confirmed the taxonomic identification of the two species. The presence of C. babaulti in Miskolctapolca is most likely due to intentional or unintentional releases by aquarium owners. The low number of captured individuals and this species' absence in a previous survey suggest that the shrimp is of recent introduction. C. babaulti and the well-established N. davidi have similar environmental tolerance; hence, this species might potentially form a viable population if not removed.
... The last temperature value was established as the control treatment, being an adequate temperature for its culture based on . The lowest temperature levels were determined according to previous researches, which demonstrated the high tolerance of N.davidi to a wide range of water temperatures (Klotz, Miesen, Hüllen, & Herder, 2013;Serezli, Atalar, Hamzacebi, Kurtoglu, & Yandi, 2017). ...
Article
This study analysed the effects of three temperatures (20, 24 and 28ºC) on survival, body coloration, carotenoid content, body weight, biochemical composition and spermatophore quality in the shrimp Neocaridina davidi. In all treatments, survival was >90%. Female body coloration and total carotenoid content, for both males and females, did not statistically differ among treatments. Female weight was similar for the three temperatures, while male weight was higher at 20ºC and 24ºC. Total lipid content was higher in female and male shrimps raised at 20ºC. Total protein content was higher in females exposed at 28ºC, but in contrast, males showed the lowest value at the same temperature. The histological and histochemical analyses of the male reproductive system did not reveal differences among treatments. At 20ºC, a delay in ovaries maturation was observed, as well as a smaller amount of ovigerous females at the end of the experimental period. Hence, these results suggest that a temperature range from 20ºC to 28ºC is adequate for satisfactory growth, with no change being exerted on spermatophore quality, body female coloration or carotenoid content, but biochemical composition was affected. Nevertheless, the lowest temperature had a clear impact on the metabolism and reproduction of N. davidi.
Article
Full-text available
Temperature increases can often speed up embryonic development and shorten gestation times in viviparous and ectothermic vertebrates. Viviparity is rare among invertebrates, however, and it is unclear what effects modest rises in temperature have on viviparous animals with exoskeletons. The intertidal marine isopod Cirolana harfordi in Australia is a species whose female members incubate their young inside their thorax and give birth to live young. This mode of reproduction contrasts the typical oviparous reproductive mode of most isopods. We investigated the impacts of increased temperature on the length of pregnancy and the number of offspring produced by C. harfordi individuals. Populations of C. harfordi were maintained at control (18 °C, to represent average environment temperature at the start of the breeding season) and two increased temperature treatments (20 °C and 22 °C). Increased temperature reduced development time to the juvenile stage and increased the number of young produced. It appears that the reproductive physiology of this viviparous invertebrate is affected by modest changes in temperature.
Article
Full-text available
Meiofauna serve as a link between microbial production and higher trophic levels, such as macroinvertebrates and juvenile fish. However, the role of meiofauna in the freshwater food web has not been accurately evaluated, and the influence of shrimp predation on freshwater meiofaunal assemblages is unknown. In this study, the predation effects of Neocaridina davidi, an ornamental freshwater shrimp native to inland water bodies in Asia, on meiofaunal density, biomass, structure, and secondary production were examined using model ecosystems (microcosms) that were sampled repeatedly over 42 days. Shrimp predation altered the structure of the meiofaunal community over the course of the experiment, in particular the density, biomass, and secondary production of nematodes, microcrustaceans, and oligochaetes. An analysis of the stomach contents of N. davidi indicated a high degree of omnivory and the frequent consumption of meiofaunal organisms. The results indicated that predation by the freshwater shrimp N. davidi depresses the overall abundance, biomass, and secondary production of meiofaunal assemblages. Moreover, they also provide insights into food-web ecology and the first evidence of freshwater shrimp predation on meiofaunal assemblages.
Article
Full-text available
The effect of water temperature on biochemical composition, growth and reproduction of the ornamental shrimp, Neocaridina heteropoda heteropoda, was investigated to determine the optimum temperature for its culture. The effect of embryo incubation temperature on the subsequent performance of juveniles was also evaluated. Ovigerous females and recently hatched juveniles (JI) were maintained during egg incubation and for a 90-day period, respectively, at three temperatures (24, 28 and 32°C). Incubation period increased with decreasing water temperature, but the number and size of JI were similar among treatments. At day 30 of the 90-day period, body weight and growth increment (GI) at 24°C were lower than those at 28 and 32°C. On subsequent days, GI at 24°C exceeded that at 28 and 32°C, leading to a similar body weight among treatments. These results suggest growth was delayed at 24°C, but only for 30 days after hatching. The lipid concentration tended to be lowest, intermediate and highest at 28, 32 and 24°C, respectively, possibly as a consequence of the metabolic processes involved in growth and ovarian maturation. Protein and glycogen concentrations were similar among treatments. Both the growth trajectory and biochemical composition of shrimps were affected by the temperature experienced during the 90-day growth period independently of the embryo incubation temperature. During the growth period, shrimps reached sexual maturity and mated, with the highest proportion of ovigerous females occurring at 28°C. All the females that matured and mated at 32°C lost their eggs, indicating a potentially stressful effect of high temperature on ovarian maturation. Based on high survival and good growth performance of shrimps at the three temperatures tested over the 90-day period it is concluded that N. heteropoda heteropoda is tolerant to a wide range of water temperatures, with 28°C being the optimum temperature for its culture.
Article
Full-text available
In this study, the situation with imported freshwater decapod species via the live aquarium ornamental trade in Turkey was investigated year round during 2011. The scientific and common names, native geographic regions, import sizes and prices were recorded. Among the 28 imported freshwater decapod species recorded in this survey, 15 are shrimps, 9 are crayfish and 4 are crabs. Those imported species might have escaped or have been released into the wild due to misguided cultural habits or incorrect conservation concepts. The objective of this study is to raise awareness of imported freshwater decapods and to present a list of the species currently traded in the aquarium industry in Turkey.
Article
Full-text available
Neocaridina denticulata sinensis (Kemp, 1918) or also known as red cherry shrimp (RCS) became popular in aquarium industry since its first introduction in 2003 until now. Little is known of this particular species since documented report is very scarce. Thus, this study was conducted to gather some information on its breeding behavior and life cycle until first maturity in laboratory condition. Fertilized eggs were found to be oval in shape with color varies from greenish to yellowish. The egg size was comparatively large, with an average diameter of 1.19 mm. Embryonic development of N. d. sinensis lasted for 15 days at 27°C. Newly hatched larvae look like a miniature version of the adult with an average total length of 2.3 mm. A female can produced about 21-51 larvae per hatching. Larger females produced more larvae. It takes 60 days for larvae to reach juvenile stage, where male and female were still undifferentiated. Juveniles become adults 15 days later. Females were obvious with the presence of orange colored ovary at the cephalothorax region. Within one to three days, these males and females are ready to spawn. During this study, N. d. sinensis cultured in freshwater were found to be susceptible to clitellate annelid (Holtodrilus sp.). Culture of this species in slightly saline condition between 5-10 ppt was an effective treatment for this annelid.
Article
Full-text available
The river Erft and its tributary Gillbach in western Germany are thermally polluted, and harbour exotic plant and animal species introduced by aquarium hobbyists. Here, we report for the first time the occurrence of two species of fresh water shrimp, Neocaridina davidi (Bouvier, 1904) and Macrobrachium dayanum (Henderson, 1893), from these heavily modified waters. We briefly discuss their taxonomy and provide characters for distinguishing the species. Due to its dependence on warm waters, it is unlikely that M. dayanum populations will persist permanently beyond the range of the thermal pollution. In contrast, N. davidi is able to tolerate much colder temperature regimes, and might disperse further into the Rhine drainage. Known parasites of N. davidi are however rather specific, and do most likely not pose a threat to native or other introduced crustacean species.
Article
Full-text available
Two new species of land-locked shrimp, Neocaridina saccam and N. ketagalan (Decapoda: Caridea: Atyidae), are described from Tainan, southwestern Taiwan, and Taipei, northern Taiwan, respectively. Based on morphological and molecular (mitochondrial 16S rRNA and cytochrome oxidase I genes) evidence, both can be distinguished from their congeners. A speciation model for this genus on the island of Taiwan is also proposed based on geological events and molecular clock estimates.
Article
Full-text available
Changes in temperature, oxygen content and other ocean biogeochemical properties directly affect the ecophysiology of marine water-breathing organisms. Previous studies suggest that the most prominent biological responses are changes in distribution, phenology and productivity. Both theory and empirical observations also support the hypothesis that warming and reduced oxygen will reduce body size of marine fishes. However, the extent to which such changes would exacerbate the impacts of climate and ocean changes on global marine ecosystems remains unexplored. Here, we employ a model to examine the integrated biological responses of over 600 species of marine fishes due to changes in distribution, abundance and body size. The model has an explicit representation of ecophysiology, dispersal, distribution, and population dynamics. We show that assemblage-averaged maximum body weight is expected to shrink by 14-24% globally from 2000 to 2050 under a high-emission scenario. About half of this shrinkage is due to change in distribution and abundance, the remainder to changes in physiology. The tropical and intermediate latitudinal areas will be heavily impacted, with an average reduction of more than 20%. Our results provide a new dimension to understanding the integrated impacts of climate change on marine ecosystems.
Article
The ‘Red Cherry shrimp’, Neocaridina davidi is a small freshwater caridean shrimp living, originally, in various kinds of inland water bodies around Asian countries. This shrimp has reached several countries for ornamental use; however, basic information on the biology of the species is still scarce in the literature. Its early post embryonic development morphology has not yet been described. This paper focused on the production and the development of early post-hatching stages of N. davidi, its male secondary sexual features, observation of the gonads and the presence of females with embryos. The larval development of N. davidi was almost suppressed as noted by the presence of relatively large-sized eggs, first stage hatching as a decapodid; and the tail fans were present only from the 2nd post-hatching stage. A biological important consequence of the presence of this Red Cherry shrimp species in the Neotropics is its potential release into nature, which could cause its rapid dispersion affecting populations of other indigenous caridean freshwater shrimps.
Article
Growth of juvenile Nile tilapia, Oreochromis niloticus (Maryut strain) was studied under laboratory conditions. Four thermal regimes (22, 26, 30, and 34 °C) were tested on 480 20-day-old fry. Significant (P<0.05) effects of temperature on growth were observed. Results showed that the final mean weight was significantly higher at 26 and 30 1C than at 22 and 34 1C. Feed conversion ratio (FCR) and daily weight gain (DWG) were better at 26 and 30 1C. At all temperatures, survival rates were not affected. These results suggest that the best growth and feed utilization of O. niloticus juveniles may be higher at 26 and 30 1C. A second experiment was performed to assess the effect of ambient water temperature during the period of sex differentiation on the sex ratio. Results showed that the high-temperature (almost 36.90 1C) treatments yielded a significantly higher proportion of males (64.20–80%) with lower survival rates (60–81%), whereas the sex ratio of progenies reared at temperature below 36 1C never deviated significantly from the balanced sex ratio. This study provided clear evidence that the exposure of progenies to ‘‘masculinizing’’ temperature may significantly decrease the survival rate of fish.