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A preliminary study of the reproductive biology of the biofouling organism Caprella acanthogaster (Crustacea, Amphipoda) in Sanggou Bay, China
Aquaculture 450 (2015) 1–5
Contents lists available at ScienceDirect
Aquaculture journal homepage: www.elsevier.com/locate/aqua-online
A preliminary study of the reproductive biology of the biofouling organism Caprella acanthogaster (Crustacea, Amphipoda) in Sanggou Bay, China Yanwei Wei a, Jihong Zhang a,⁎, Wenguang Wu a, Yongfeng Yao a, Jie Chen b, Jianguang Fang a a Key Laboratory for Sustainable Utilization of Marine Fishery Resources, Ministry of Agriculture, Shandong Provincial Key Laboratory of Fishery Resources and Ecological Environment, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Science, Qingdao 266071, China b College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
a r t i c l e
i n f o
Article history: Received 13 August 2014 Received in revised form 15 June 2015 Accepted 22 June 2015 Available online 24 June 2015 Keywords: Caprella acanthogaster Embryonic development Reproductive biology Temperature
a b s t r a c t The duration of embryonic development and the numbers of offspring and body lengths at sexual maturity of the biofouling amphipod Caprella acanthogaster at different temperatures were studied. Embryonic development was divided into nine stages: fertilized egg, cleavage stage, morula, blastula, gastrula, limb-bud stage, heart-beat stage, fully developed juveniles, and hatching juveniles. The duration of embryonic development was 196 h at 14 °C and 117 h at 20 °C. Temperature had a significant influence on maturation time and body length at sexual maturity (P b 0.05). However, it did not have a significant effect on the body length of juveniles (P N 0.05). Mean body lengths of juveniles, mean body lengths at sexual maturity, and maturation times at 14 °C were: 1.52 ± 0.17 mm, 10.14 ± 1.24 mm, and 33.20 ± 3.27 days, respectively; and at 20 °C, they were: 1.37 ± 0.07 mm, 6.66 ± 0.75 mm, and 18.17 ± 2.56 days. The number of offspring (EO) was positively correlated with the body length (BL). At 14 °C, the relationship was: EO = 7.74 BL − 39.66 (R2 = 0.75) and, at 20 °C, it was: EO = 13.69 BL − 78.15 (R2 = 0.77). Statement of relevance: We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Biofouling amphipods of the genus Caprella often attach to the outer branches of algae, bryozoans or maricultural net. In China, Caprella are very abundant, mainly attached to the cultured seaweed, such as Gracilaria lemaneiformis (Zheng et al., 2011). Caprella could influence the survival and growth rates of cultured G. lemaneiformis by grazing upon the seaweeds. Caprella have unisexual reproductive characteristics and under suitable conditions their populations increase rapidly (Imada and Kikuchi, 1984; Takeuchi et al., 1990; Aoki, 1999). Therefore, as the density and biomass of Caprella are currently increasing, their impact on maricultural G. lemaneiformis becomes a serious problem. Their population dynamics are strictly influenced by environment conditions, including temperature, food availability, salinity, and dissolved oxygen. Temperature is a key factor influencing the distribution, density and life histories of Caprella spp. (Hosono, 2011; Hosono and Sakurai, 2006). However, reports on the influence of temperature on the reproduction of Caprella are contradictory. For example, Bynum (1978) found that the body size at sexual maturity of Caprella penantis was ⁎ Corresponding author at: 106 Nanjing Road, Qingdao City, Shandong Province, China. E-mail address: [email protected] (J. Zhang).
http://dx.doi.org/10.1016/j.aquaculture.2015.06.037 0044-8486/© 2015 Elsevier B.V. All rights reserved.
lower in summer than in winter. Fedotov (1992) studied the body size of premature females of Caprella mutica in May, June and July, and found that this temperature–size relationship also applied to this species. However, Hosono (2011) observed no significant difference in the sizes of C. mutica individuals cultured at 10 °C or 20 °C in the laboratory. Information on the species Caprella acanthogaster is limited to reports on its growth, survivorship, and first-brood body length (Cook et al., 2007; Lim and Alexander, 1986). To date, its embryonic development has not been studied and it is unknown whether the temperature–size rule applies to the life stages of C. acanthogaster. Here we report on aspects of the reproductive biology of C. acanthogaster, and the influence of temperature on it, which will help to understand the population dynamics and get antifouling method in the future.
2. Materials and methods 2.1. Embryonic development and body length of juveniles C. acanthogaster were collected in Sanggou Bay, Shandong Province, China in March and June 2013 and temporarily cultured in chambers with sand-filtered sea water and constant aeration.
2
Y. Wei et al. / Aquaculture 450 (2015) 1–5
Totally 60 mature individuals, 30 males and 30 females of C. acanthogaster were selected and cultured together in 3-l glass containers in an incubator under a 14-h light:10-h dark cycle. Ovigerous females were removed immediately (time zero) and dissected to obtain fertilized eggs. 100 eggs were placed in a petri dish under the same conditions. Embryonic development was observed through a Nikon E200 microscope. To avoid damaging the eggs, observations on each egg were restricted to less than 1 min. Based on the reports about caprellid amphipod (Han et al., 2012; Ito et al., 2011), embryonic development is classified into 9 stages, named as: 1) fertilized eggs; 2) cleavage stage; 3) morula; 4) blastula; 5) gastrula; 6) limb-bud stage; 7) heart-beat stage; 8) unhatched juveniles; and 9) hatched juveniles. The experiment ended when juveniles hatched from the egg membranes. The embryonic development time was determined at 14 °C in March and 20 °C in June, which was according to the natural sea water temperature. And on the other hand, in March, the C. acanthogaster just began to proliferate, whereas in June it was in the inflection point of biomass rapid increase.
2.2. Sexual maturity 40 juveniles were cultured in 3-l glass containers and fed the seaweed G. lemaneiformis until they reached maturity. Females were identified as ‘mature’ when the oostegites (pereonites III and IV) were fully developed to form the brood pouch (Cook et al., 2007). At this time, the total body length at sexual maturity was measured.
2.3. Number of offspring C. acanthogaster were collected in March 2013 at a sea water temperature of 14 °C and in June 2013 at 20 °C. Twelve female individuals were respectively and randomly selected and, after measurement of their total body lengths, they were isolated for counting of the number of offspring released per female.
2.4. Data analysis Linear regressions between offspring number and body length were performed using SPSS 17.0 software. Tukey's multiplecomparison test was used for pairwise comparisons of embryonic development time at different temperatures with P b 0.05 considered statistically significant.
3. Results 3.1. Process and duration of embryonic development The embryonic development schedule of C. acanthogaster passed through nine stages showed in Table 1. The characteristics of each stage were as follows (Fig. 1): 1) Fertilized eggs: The fertilized eggs were black and slightly ovoid in shape. They were not released into the water but were retained within the brood pouch of females. The cytoplasm had a uniform appearance (Fig. 1-1). The specific gravity of fertilized eggs was greater than sea water; submerged eggs did not adhere to each other. 2) Cleavage stage: The fertilized eggs began to divide under laboratory conditions, forming two isometric cells (Fig. 1-2). The cells then entered the second division with the cleavage furrow perpendicular to the first division, forming four isometric cells (Fig. 1-3). Development then progressed through the 8-cell (Fig. 1-4), 16-cell (Fig. 1-5), and 32-cell stages (Fig. 1-6) to the morula stage. 3) Morula stage: Following numerous cell divisions, the embryo was composed of tens to hundreds of small identical cells (Fig. 1-7). 4) Blastula stage: (Fig. 1-8). At the blastula stage, there were no clear boundaries between the cells, which were separated into internal and external cells. The external cells surrounded the larger intimal cells. No blastocoele was present. 5) Gastrula stage: The gastrula was formed by invagination of the blastocyst at a specific location (Fig. 1-9) to form a spherical structure, which eventually developed into the cephalothorax, and a halfmoon-shaped structure, which developed into the pygidium (protostomic development). 6) Limb-bud stage: The limb buds first emerged as a transparent bulge on the summit of the spherical structure (Fig. 1-10). As development progressed, the bulge progressively increased to form the primordia of the head, maxillae and uropods. 7) Heart-beating stage: At this stage, heart begins to beat and irregular intervals were 39–42 s initially. Red eyespots appeared and embryonic development entered the early heart-beat stage (Fig. 1-11). 8) Unhatched juveniles: Embryonic development was considered complete when the antennae, pereopods and uropods were fully developed. At the moment, color of juvenile's trunk turned from black to gray or pale yellow. The body pulsations became more regular with a periodicity of 18–24 s with contractions sustained for 4–5 s. At this stage, juveniles appeared similar to adults (Fig. 1-12). 9) Hatched juveniles: Juveniles of C. acanthogaster hatched from the egg membranes (Fig. 1-13) and developed directly into adults without undergoing metamorphosis.
Table 1 Embryonic development schedule of Caprella acanthogaster at 20 °C. The time of Stage of embryonic development development
Developmental characteristic
Fig.
0h 1.5 h 3h 5h 7h 9h 12 h 18 h 32 h 48 h 80 h
Fertilized eggs 2 cell stage 4 cell stage 8 cell stage 16 cell stage 32 cell stage Morula stage Blastula stage Gastrula stage Limb-bud stage Heart-beating stage
1-1 1-2 1-3 1-4 1-5 1-6 1-7 1-8 1-9 1-10 1-11
104 h 117 h
Juveniles were fully developed Juveniles released from egg membrane
Slightly oval, submerged eggs, no sticky First division, forming 2 isometric cells Second division, cleavage furrow perpendicular to the first time, forming 4 isometric cells Third division, forming 8 isometric cells Fourth division, forming 16 isometric cells Fifth division, forming 32 isometric cells Composed of many small cells, the cells can differentiate. Boundaries between cells were not clear, the cells divided into inside cells and outside cells. Cell invaginated forms a kind of circular structure and a kind of half-moon structure. Transparent bulge increases gradually, which was primordium of head, maxilla and uropod. The heart began to beat, every time was 39–42 s, later the heartbeat frequency stability gradually, every time was 18–24 s and sustained 4–5 s. Juveniles were same as adult, 2 antennas, 1 maxill, 1 eye, 2 gnathopods, 3 pereopods and 3 uropods. Juveniles released from egg membrane, the body lengths were (1.37 ± 0.07) mm.
1-12 1-13
Y. Wei et al. / Aquaculture 450 (2015) 1–5
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Fig. 1. Stages in the embryonic development of Caprella acanthogaster. 1) fertilized egg; 2) 2-cell stage; 3) 4-cell stage; 4) 8-cell stage; 5) 16-cell stage; 6) 32-cell stage; 7) morula; 8) blastula; 9) gastrula; 10) limb-bud stage; 11) heart-beating stage; 12) fully developed juvenile; 13) juveniles released from egg membranes. Abbreviations, cf: cleavage furrow; me: membrane; icm: inner cell mass; tro: trophectoderm; fe: furrow of the entoblast; pr: primordium; ey: eye; hp: head primordium; mp: maxilla primordium; up: uropod primordium; ant: antenna; hea: head; pe: pereopod; gu: gut; ur: uropod.
3.2. Body length of juveniles and sexual maturity Temperature had a significant influence on the maturation time and the body length at sexual maturity of C. acanthogaster (P b 0.05). The duration of embryonic development from fertilized eggs to juveniles hatching from the egg membrane was 196 h at 14 °C and 117 h at 20 °C. However, temperature had no significant effect (P N 0.05) on the body length of juveniles (Table 2). At 14 °C, the mean values of the
Table 2 Body lengths at sexual maturity and maturation times of Caprella acanthogaster at 14 °C and 20 °C (mean ± SE, N ≥ 6). Temperature (°C)
Maturation time (d)
The body length of juveniles (mm)
The body length at sexual maturity (mm)
14 20
33.20 ± 3.27 18.17 ± 2.56a
1.52 ± 0.17 1.37 ± 0.07
10.12 ± 0.99 6.66 ± 0.75a
a
Represents significant difference between the result of 14 °C and 20 °C (P b 0.05).
body length of juveniles, body length at sexual maturity, and maturation time were 1.52 ± 0.17 mm, 10.14 ± 1.24 mm, and 33.20 ± 3.27 days, respectively; at 20 °C, they were 1.37 ± 0.07 mm, 6.66 ± 0.75 mm, and 18.17 ± 2.56 days, respectively. 3.3. Number of offspring There was a positive linear correlation between the number of offspring (EO) and body length (BL) at each temperature (Fig. 2). At 14 °C, the relationship was: EO = 7.74 BL − 39.66 (R2 = 0.75) and, at 20 °C, it was: EO = 13.69 BL − 78.15 (R2 = 0.77). That is, for C. acanthogaster of similar body length, more offspring were produced at higher temperatures. 4. Discussion Early cleavage of C. acanthogaster was holoblastic, which is a general characteristic of the embryonic development of Amphipoda (Magniette
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Acknowledgments This work was supported by the National Science & Technology Pillar Program (Grant No. 2011BAD13B06) and the National Basic Research Program of China (Grant No. 2011CB409805). We would like to thank the managers of Weihai Changqing Ocean Science and Technology Co., Ltd. and Chudao Fisheries Co., Ltd. for their help during the experiment. References
Fig. 2. Relationship between the body lengths of female Caprella acanthogaster and the number of offspring at 14 °C and 20 °C.
and Ginsburger-Vogel, 1982; Wolff and Scholtz, 2002; Browne et al., 2005a, 2005b). Embryonic development in Caprella scaura (Ito et al., 2011) and Ampithoe valida is similar (Han et al., 2012). Postembryonic development of C. acanthogaster proceeds by epimorphosis, in which hatching juveniles are similar to adults. But it possesses fewer segments in the antennae and appendages and in which surface protrusions, such as chaetae and acanthi, are underdeveloped. This process is also similar to the results observed by Zheng and Ding (1991) in Macrobrachium hainanense and Han et al. (2012) in A. valida. The duration of embryonic development in amphipods is known to depend on temperature (Takeuchi and Hirano, 1992; Maranhão and Marques, 2003) and this is consistent with the longer duration of embryonic development observed at 14 °C than at 20 °C in this paper. A similar relationship was observed for the duration of maturation. Accordingly, high temperatures have been reported to accelerate amphipod growth (Welton and Clarke, 1980; Muskó, 1992; Cunha et al., 2000; Maranhão and Marques, 2003), to shorten maturation time, to speed up the cleavage rate of fertilized eggs, and to shorten the brooding period (Highsmith and Coyle, 1991). Temperature is a key environmental factor that affects the life history pattern of amphipods (Sainte, 1991). Our data indicated that temperature had an important effect on the duration of embryonic development and of maturation of C. acanthogaster and also significantly influenced the body length at sexual maturity. C. acanthogaster followed the temperature–size rule that animals mature at larger sizes in lowertemperature environments and at smaller sizes in higher-temperature environments (Hosono and Sakurai, 2006; Hosono, 2011). This may have close relationship with energy allocation. Eriksson Wiklund and Sundelin (2001) studied temperature effects on reproduction in the amphipod Monoporeia affinis. The author found that high metabolic demands of the females at high temperatures led to smaller amounts of lipids available for gonad maturation. Unfortunately, the energy allocation in C. acanthogaster was not studied in this paper. There was a positive correlation between the body length of C. acanthogaster and the number of offspring, i.e., longer females produced more offspring. This is a common observation among amphipods (Hynes and Coleman, 1968; Maranhão and Marques, 2003). It was suggested that the size of the ovary is proportional to body length (Sheader, 1977), so that larger females produce more juveniles. Rajagopal et al. (1999) considered that female size, food availability and temperature determined the size of the brood pouch. Some studies have shown that under abundant food conditions, C. acanthogaster generates a larger brood pouch (Subida et al., 2005; Jeong et al., 2007). In this study of C. acanthogaster on the surface of the seaweed G. lemaneiformis, food would not have been limited and temperature was probably the main factor influencing the number of offspring.
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The amphipod Corophium multisetosum (Corophiidae) in Ria de Aveiro (NW Portugal). I. Life history and aspects of reproductive biology. Mar. Biol. 137, 637–650. Eriksson Wiklund, A.-K., Sundelin, B., 2001. Impaired reproduction in the amphipods Monoporeia affinis and Pontoporeia femorata as a result of moderate hypoxia and increased temperature. Mar. Ecol. Prog. Ser. 222, 131–141. Fedotov, P.A., 1992. Population and production biology of amphipod Caprella mutica in Posyet Bay, Sea of Japan. Russ. J. Mar. Biol. 17, 224–230. Han, Y.W., Li, J., Chen, P., Li, J.T., Dai, F.Y., Pan, L.Q., 2012. The reproduction of the Ampithoe valida and observing the development of Ampithoe valida embryonic development from morphology. Acta Hydrobiol. Sin. 6, 1193–1199. Highsmith, R.C., Coyle, K.O., 1991. Amphipod life histories: community structure, impact of temperature on decoupled growth and maturation rates, productivity, and P:B ratios. Am. Zool. 31, 861–873. Hosono, T., 2011. Effect of temperature on growth and maturation pattern of Caprella mutica (Crustacea, Amphipoda): does the temperature–size rule function in caprellids. Mar. Biol. 158, 363–370. Hosono, T., Sakurai, Y., 2006. Life history of Caprella acanthogaster (Amphipoda, Crustacea), a fouling organism on fishery facilities. Suisan Zoshoku 54, 107–114. Hynes, H.B.N., Coleman, M.J., 1968. A simple method of assessing the annual production of stream benthos. Limnol. Oceanogr. 13, 569–573. Imada, K., Kikuchi, T., 1984. Studies on some reproductive traits of three caprellids (Crustacea: Amphipoda) and their seasonal fluctuations in the Sargassum bed. Publications of Amakusa Marine Biology Laboratory, Jyushu University 7, pp. 151–172. Ito, A., Aoki, M.N., Yahata, K., Wada, H., 2011. Embryonic development and expression analysis of distal-less in Caprella scaura (Crustacea, Amphipoda, Caprellidea). Biol. Bull. 221, 206–214. Jeong, S.J., Yu, O.H., Suh, H.L., 2007. Life history and reproduction of Jassaslatteryi (Amphipoda, Ischyroceridae) on a seagrass bed (Zostera marina L.) in southern Korea. J. Crustac. Biol. 27, 65–70. Lim, S.T.A., Alexander, C.G., 1986. Reproductive behaviour of the caprellid amphipod, Caprella scaura typica, Mayer 1890. Mar. Freshw. Behav. Physiol. 12, 217–230. Magniette, F., Ginsburger-Vogel, T., 1982. Etablissement d'une table chronologique du developpement embryonnaire, a differentes temperatures, chez Orchestia gammarellus (Pallas) (Crustacea, Amphipode). Bull. Soc. Zool. Fr. 107, 101–110. Maranhão, P., Marques, J.C., 2003. The influence of temperature and salinity on the duration of embryonic development, fecundity and growth of the amphipod Echinogammarus marinus Leach (Gammaridae). Acta Oecol. 24, 5–13. Muskó, I.B., 1992. Life history of Corophium curvispinum G.O. Sars (Crustacea, Amphipoda) living on macrophytes in Lake Balaton. Hydrobiologia 243/244, 197–202. Rajagopal, S., Van der Velde, G., Paffen, B.G.P., van den Brink, F.W.B., de Vaate, A.B., 1999. Life history and reproductive biology of the invasive amphipod Corophium curvispinum (Crustacea: Amphipoda) in the Lower Rhine. Arch. Hydrobiol. 144, 305–325. Sainte, M.B., 1991. A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223, 189–227. Sheader, M., 1977. Production and population dynamics of Ampelisca tenuicornis (Amphipoda) with notes on the biology of its parasite Sphaeronella longipes (Copepoda). J. Mar. Biol. Assoc. U. K. 57, 955–968. Subida, M.D., Cunha, M.R., Moreira, M.H., 2005. Life history, reproduction, and production of Gammarus chevreuxi (Amphipoda: Gammaridae) in the Ria de Aveiro, northwestern Portugal. J. N. Am. Benthol. Soc. 24, 82–100. Takeuchi, I., Hirano, R., 1992. Growth and reproduction of the epifaunal amphipod Caprella okadai Arimoto (Crustacea: Amphipoda: Caprellidea). J. Exp. Mar. Biol. Ecol. 161, 201–212. Takeuchi, I., Yamakawa, H., Fujiwara, M., 1990. Density fluctuation of caprellid amphipods (Crustacea) inhabiting the red alga Gelidium amansii (Lamouroux) Lamouroux, with
Y. Wei et al. / Aquaculture 450 (2015) 1–5 emphasis on Caprella okadai Arimoto. La mer, la Socie'te´ franco-japonaised'oce´ anographie, Tokyo 28, p. 36. Welton, J.S., Clarke, R.T., 1980. Laboratory studies on the reproduction and growth of the amphipod, Gammarus pulex (L.). J. Anim. Ecol. 581–592. Wolff, C., Scholtz, G., 2002. Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev. Biol. 250, 44–58.
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Contents lists available at ScienceDirect
Aquaculture journal homepage: www.elsevier.com/locate/aqua-online
A preliminary study of the reproductive biology of the biofouling organism Caprella acanthogaster (Crustacea, Amphipoda) in Sanggou Bay, China Yanwei Wei a, Jihong Zhang a,⁎, Wenguang Wu a, Yongfeng Yao a, Jie Chen b, Jianguang Fang a a Key Laboratory for Sustainable Utilization of Marine Fishery Resources, Ministry of Agriculture, Shandong Provincial Key Laboratory of Fishery Resources and Ecological Environment, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Science, Qingdao 266071, China b College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
a r t i c l e
i n f o
Article history: Received 13 August 2014 Received in revised form 15 June 2015 Accepted 22 June 2015 Available online 24 June 2015 Keywords: Caprella acanthogaster Embryonic development Reproductive biology Temperature
a b s t r a c t The duration of embryonic development and the numbers of offspring and body lengths at sexual maturity of the biofouling amphipod Caprella acanthogaster at different temperatures were studied. Embryonic development was divided into nine stages: fertilized egg, cleavage stage, morula, blastula, gastrula, limb-bud stage, heart-beat stage, fully developed juveniles, and hatching juveniles. The duration of embryonic development was 196 h at 14 °C and 117 h at 20 °C. Temperature had a significant influence on maturation time and body length at sexual maturity (P b 0.05). However, it did not have a significant effect on the body length of juveniles (P N 0.05). Mean body lengths of juveniles, mean body lengths at sexual maturity, and maturation times at 14 °C were: 1.52 ± 0.17 mm, 10.14 ± 1.24 mm, and 33.20 ± 3.27 days, respectively; and at 20 °C, they were: 1.37 ± 0.07 mm, 6.66 ± 0.75 mm, and 18.17 ± 2.56 days. The number of offspring (EO) was positively correlated with the body length (BL). At 14 °C, the relationship was: EO = 7.74 BL − 39.66 (R2 = 0.75) and, at 20 °C, it was: EO = 13.69 BL − 78.15 (R2 = 0.77). Statement of relevance: We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Biofouling amphipods of the genus Caprella often attach to the outer branches of algae, bryozoans or maricultural net. In China, Caprella are very abundant, mainly attached to the cultured seaweed, such as Gracilaria lemaneiformis (Zheng et al., 2011). Caprella could influence the survival and growth rates of cultured G. lemaneiformis by grazing upon the seaweeds. Caprella have unisexual reproductive characteristics and under suitable conditions their populations increase rapidly (Imada and Kikuchi, 1984; Takeuchi et al., 1990; Aoki, 1999). Therefore, as the density and biomass of Caprella are currently increasing, their impact on maricultural G. lemaneiformis becomes a serious problem. Their population dynamics are strictly influenced by environment conditions, including temperature, food availability, salinity, and dissolved oxygen. Temperature is a key factor influencing the distribution, density and life histories of Caprella spp. (Hosono, 2011; Hosono and Sakurai, 2006). However, reports on the influence of temperature on the reproduction of Caprella are contradictory. For example, Bynum (1978) found that the body size at sexual maturity of Caprella penantis was ⁎ Corresponding author at: 106 Nanjing Road, Qingdao City, Shandong Province, China. E-mail address: [email protected] (J. Zhang).
http://dx.doi.org/10.1016/j.aquaculture.2015.06.037 0044-8486/© 2015 Elsevier B.V. All rights reserved.
lower in summer than in winter. Fedotov (1992) studied the body size of premature females of Caprella mutica in May, June and July, and found that this temperature–size relationship also applied to this species. However, Hosono (2011) observed no significant difference in the sizes of C. mutica individuals cultured at 10 °C or 20 °C in the laboratory. Information on the species Caprella acanthogaster is limited to reports on its growth, survivorship, and first-brood body length (Cook et al., 2007; Lim and Alexander, 1986). To date, its embryonic development has not been studied and it is unknown whether the temperature–size rule applies to the life stages of C. acanthogaster. Here we report on aspects of the reproductive biology of C. acanthogaster, and the influence of temperature on it, which will help to understand the population dynamics and get antifouling method in the future.
2. Materials and methods 2.1. Embryonic development and body length of juveniles C. acanthogaster were collected in Sanggou Bay, Shandong Province, China in March and June 2013 and temporarily cultured in chambers with sand-filtered sea water and constant aeration.
2
Y. Wei et al. / Aquaculture 450 (2015) 1–5
Totally 60 mature individuals, 30 males and 30 females of C. acanthogaster were selected and cultured together in 3-l glass containers in an incubator under a 14-h light:10-h dark cycle. Ovigerous females were removed immediately (time zero) and dissected to obtain fertilized eggs. 100 eggs were placed in a petri dish under the same conditions. Embryonic development was observed through a Nikon E200 microscope. To avoid damaging the eggs, observations on each egg were restricted to less than 1 min. Based on the reports about caprellid amphipod (Han et al., 2012; Ito et al., 2011), embryonic development is classified into 9 stages, named as: 1) fertilized eggs; 2) cleavage stage; 3) morula; 4) blastula; 5) gastrula; 6) limb-bud stage; 7) heart-beat stage; 8) unhatched juveniles; and 9) hatched juveniles. The experiment ended when juveniles hatched from the egg membranes. The embryonic development time was determined at 14 °C in March and 20 °C in June, which was according to the natural sea water temperature. And on the other hand, in March, the C. acanthogaster just began to proliferate, whereas in June it was in the inflection point of biomass rapid increase.
2.2. Sexual maturity 40 juveniles were cultured in 3-l glass containers and fed the seaweed G. lemaneiformis until they reached maturity. Females were identified as ‘mature’ when the oostegites (pereonites III and IV) were fully developed to form the brood pouch (Cook et al., 2007). At this time, the total body length at sexual maturity was measured.
2.3. Number of offspring C. acanthogaster were collected in March 2013 at a sea water temperature of 14 °C and in June 2013 at 20 °C. Twelve female individuals were respectively and randomly selected and, after measurement of their total body lengths, they were isolated for counting of the number of offspring released per female.
2.4. Data analysis Linear regressions between offspring number and body length were performed using SPSS 17.0 software. Tukey's multiplecomparison test was used for pairwise comparisons of embryonic development time at different temperatures with P b 0.05 considered statistically significant.
3. Results 3.1. Process and duration of embryonic development The embryonic development schedule of C. acanthogaster passed through nine stages showed in Table 1. The characteristics of each stage were as follows (Fig. 1): 1) Fertilized eggs: The fertilized eggs were black and slightly ovoid in shape. They were not released into the water but were retained within the brood pouch of females. The cytoplasm had a uniform appearance (Fig. 1-1). The specific gravity of fertilized eggs was greater than sea water; submerged eggs did not adhere to each other. 2) Cleavage stage: The fertilized eggs began to divide under laboratory conditions, forming two isometric cells (Fig. 1-2). The cells then entered the second division with the cleavage furrow perpendicular to the first division, forming four isometric cells (Fig. 1-3). Development then progressed through the 8-cell (Fig. 1-4), 16-cell (Fig. 1-5), and 32-cell stages (Fig. 1-6) to the morula stage. 3) Morula stage: Following numerous cell divisions, the embryo was composed of tens to hundreds of small identical cells (Fig. 1-7). 4) Blastula stage: (Fig. 1-8). At the blastula stage, there were no clear boundaries between the cells, which were separated into internal and external cells. The external cells surrounded the larger intimal cells. No blastocoele was present. 5) Gastrula stage: The gastrula was formed by invagination of the blastocyst at a specific location (Fig. 1-9) to form a spherical structure, which eventually developed into the cephalothorax, and a halfmoon-shaped structure, which developed into the pygidium (protostomic development). 6) Limb-bud stage: The limb buds first emerged as a transparent bulge on the summit of the spherical structure (Fig. 1-10). As development progressed, the bulge progressively increased to form the primordia of the head, maxillae and uropods. 7) Heart-beating stage: At this stage, heart begins to beat and irregular intervals were 39–42 s initially. Red eyespots appeared and embryonic development entered the early heart-beat stage (Fig. 1-11). 8) Unhatched juveniles: Embryonic development was considered complete when the antennae, pereopods and uropods were fully developed. At the moment, color of juvenile's trunk turned from black to gray or pale yellow. The body pulsations became more regular with a periodicity of 18–24 s with contractions sustained for 4–5 s. At this stage, juveniles appeared similar to adults (Fig. 1-12). 9) Hatched juveniles: Juveniles of C. acanthogaster hatched from the egg membranes (Fig. 1-13) and developed directly into adults without undergoing metamorphosis.
Table 1 Embryonic development schedule of Caprella acanthogaster at 20 °C. The time of Stage of embryonic development development
Developmental characteristic
Fig.
0h 1.5 h 3h 5h 7h 9h 12 h 18 h 32 h 48 h 80 h
Fertilized eggs 2 cell stage 4 cell stage 8 cell stage 16 cell stage 32 cell stage Morula stage Blastula stage Gastrula stage Limb-bud stage Heart-beating stage
1-1 1-2 1-3 1-4 1-5 1-6 1-7 1-8 1-9 1-10 1-11
104 h 117 h
Juveniles were fully developed Juveniles released from egg membrane
Slightly oval, submerged eggs, no sticky First division, forming 2 isometric cells Second division, cleavage furrow perpendicular to the first time, forming 4 isometric cells Third division, forming 8 isometric cells Fourth division, forming 16 isometric cells Fifth division, forming 32 isometric cells Composed of many small cells, the cells can differentiate. Boundaries between cells were not clear, the cells divided into inside cells and outside cells. Cell invaginated forms a kind of circular structure and a kind of half-moon structure. Transparent bulge increases gradually, which was primordium of head, maxilla and uropod. The heart began to beat, every time was 39–42 s, later the heartbeat frequency stability gradually, every time was 18–24 s and sustained 4–5 s. Juveniles were same as adult, 2 antennas, 1 maxill, 1 eye, 2 gnathopods, 3 pereopods and 3 uropods. Juveniles released from egg membrane, the body lengths were (1.37 ± 0.07) mm.
1-12 1-13
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Fig. 1. Stages in the embryonic development of Caprella acanthogaster. 1) fertilized egg; 2) 2-cell stage; 3) 4-cell stage; 4) 8-cell stage; 5) 16-cell stage; 6) 32-cell stage; 7) morula; 8) blastula; 9) gastrula; 10) limb-bud stage; 11) heart-beating stage; 12) fully developed juvenile; 13) juveniles released from egg membranes. Abbreviations, cf: cleavage furrow; me: membrane; icm: inner cell mass; tro: trophectoderm; fe: furrow of the entoblast; pr: primordium; ey: eye; hp: head primordium; mp: maxilla primordium; up: uropod primordium; ant: antenna; hea: head; pe: pereopod; gu: gut; ur: uropod.
3.2. Body length of juveniles and sexual maturity Temperature had a significant influence on the maturation time and the body length at sexual maturity of C. acanthogaster (P b 0.05). The duration of embryonic development from fertilized eggs to juveniles hatching from the egg membrane was 196 h at 14 °C and 117 h at 20 °C. However, temperature had no significant effect (P N 0.05) on the body length of juveniles (Table 2). At 14 °C, the mean values of the
Table 2 Body lengths at sexual maturity and maturation times of Caprella acanthogaster at 14 °C and 20 °C (mean ± SE, N ≥ 6). Temperature (°C)
Maturation time (d)
The body length of juveniles (mm)
The body length at sexual maturity (mm)
14 20
33.20 ± 3.27 18.17 ± 2.56a
1.52 ± 0.17 1.37 ± 0.07
10.12 ± 0.99 6.66 ± 0.75a
a
Represents significant difference between the result of 14 °C and 20 °C (P b 0.05).
body length of juveniles, body length at sexual maturity, and maturation time were 1.52 ± 0.17 mm, 10.14 ± 1.24 mm, and 33.20 ± 3.27 days, respectively; at 20 °C, they were 1.37 ± 0.07 mm, 6.66 ± 0.75 mm, and 18.17 ± 2.56 days, respectively. 3.3. Number of offspring There was a positive linear correlation between the number of offspring (EO) and body length (BL) at each temperature (Fig. 2). At 14 °C, the relationship was: EO = 7.74 BL − 39.66 (R2 = 0.75) and, at 20 °C, it was: EO = 13.69 BL − 78.15 (R2 = 0.77). That is, for C. acanthogaster of similar body length, more offspring were produced at higher temperatures. 4. Discussion Early cleavage of C. acanthogaster was holoblastic, which is a general characteristic of the embryonic development of Amphipoda (Magniette
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Acknowledgments This work was supported by the National Science & Technology Pillar Program (Grant No. 2011BAD13B06) and the National Basic Research Program of China (Grant No. 2011CB409805). We would like to thank the managers of Weihai Changqing Ocean Science and Technology Co., Ltd. and Chudao Fisheries Co., Ltd. for their help during the experiment. References
Fig. 2. Relationship between the body lengths of female Caprella acanthogaster and the number of offspring at 14 °C and 20 °C.
and Ginsburger-Vogel, 1982; Wolff and Scholtz, 2002; Browne et al., 2005a, 2005b). Embryonic development in Caprella scaura (Ito et al., 2011) and Ampithoe valida is similar (Han et al., 2012). Postembryonic development of C. acanthogaster proceeds by epimorphosis, in which hatching juveniles are similar to adults. But it possesses fewer segments in the antennae and appendages and in which surface protrusions, such as chaetae and acanthi, are underdeveloped. This process is also similar to the results observed by Zheng and Ding (1991) in Macrobrachium hainanense and Han et al. (2012) in A. valida. The duration of embryonic development in amphipods is known to depend on temperature (Takeuchi and Hirano, 1992; Maranhão and Marques, 2003) and this is consistent with the longer duration of embryonic development observed at 14 °C than at 20 °C in this paper. A similar relationship was observed for the duration of maturation. Accordingly, high temperatures have been reported to accelerate amphipod growth (Welton and Clarke, 1980; Muskó, 1992; Cunha et al., 2000; Maranhão and Marques, 2003), to shorten maturation time, to speed up the cleavage rate of fertilized eggs, and to shorten the brooding period (Highsmith and Coyle, 1991). Temperature is a key environmental factor that affects the life history pattern of amphipods (Sainte, 1991). Our data indicated that temperature had an important effect on the duration of embryonic development and of maturation of C. acanthogaster and also significantly influenced the body length at sexual maturity. C. acanthogaster followed the temperature–size rule that animals mature at larger sizes in lowertemperature environments and at smaller sizes in higher-temperature environments (Hosono and Sakurai, 2006; Hosono, 2011). This may have close relationship with energy allocation. Eriksson Wiklund and Sundelin (2001) studied temperature effects on reproduction in the amphipod Monoporeia affinis. The author found that high metabolic demands of the females at high temperatures led to smaller amounts of lipids available for gonad maturation. Unfortunately, the energy allocation in C. acanthogaster was not studied in this paper. There was a positive correlation between the body length of C. acanthogaster and the number of offspring, i.e., longer females produced more offspring. This is a common observation among amphipods (Hynes and Coleman, 1968; Maranhão and Marques, 2003). It was suggested that the size of the ovary is proportional to body length (Sheader, 1977), so that larger females produce more juveniles. Rajagopal et al. (1999) considered that female size, food availability and temperature determined the size of the brood pouch. Some studies have shown that under abundant food conditions, C. acanthogaster generates a larger brood pouch (Subida et al., 2005; Jeong et al., 2007). In this study of C. acanthogaster on the surface of the seaweed G. lemaneiformis, food would not have been limited and temperature was probably the main factor influencing the number of offspring.
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