Effects of sex change on number of olfactory chemoreceptors in Lysmata shrimp.
|Subject:||Shrimps (Physiological aspects)|
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: August, 2012 Source Volume: 31 Source Issue: 3|
|Product:||Product Code: 0913080 Shrimp NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish|
|Geographic:||Geographic Scope: United States Geographic Code: 1USA United States|
ABSTRACT Sexual dimorphism of the olfactory system is common in
crustaceans; however, it has never been confirmed empirically to be sex
dependent. In the current study, the growth pattern of aesthetasc (i.e.,
olfactory chemosensors of crustaceans) number in 4 protandric
simultaneous hermaphroditic shrimp species in the genus Lysmata with 2
social systems pair living (Lysmata amboinensis and Lysmata pederseni)
and group living (Lysmata boggessi and Lysmata wurdemanni)--from male
phase to euhermaphrodite phase were examined. The results show that the
aesthetasc numbers of both male-phase and euhermaphrodite-phase shrimp
are related in general to timing of sex change; in other words, those
shrimp that change sex later have greater aesthetasc numbers than those
that change sex earlier. This factor is the major reason contributing to
the high variation in aesthetasc numbers in euhermaphrodite-phase
shrimp. The aesthetasc number increased with shrimp growth during the
male phase, but thereafter male-phase shrimp change into
euhermaphrodite-phase shrimp and the aesthetasc number increased slowly
at first and then stabilized, and even decreased in some. Our results
suggest explicitly that the aesthetasc number in Lysmata shrimp is sex
dependent and most likely related to their social environment as well.
KEY WORDS: aesthetasc, social environment, decapod crustaceans, Lysmata
The olfactory system plays an important role in chemical communication in intraspecific and interspecific interactions, and interactions between organisms and environment, including mate searches (e.g., Gleeson 1982, Cowan 1991, Zhang & Lin 2006), kin recognition (e.g., Johnson & Atema 2005), food detection (e.g., Derby & Atema 1982, Derby et al. 2001), sexual selection (reviewed by Andersson (1994)), and habitat selection (e.g., Horner et al. 2008). Variation in the olfactory sensor morph and number may result in behavioral difference, and it affects reproductive success in insects (e.g., Markow 1987), shrimp (Zhang et al. 2009), mice (e.g., Wall et al. 2003), and salamanders (Maico et al. 2003).
Variation in olfactory sensor morph and number may occur between the sexes and among individuals. Sexual dimorphism of the olfactory sensor morph and number is common across animal taxa, such as in insects (e.g., Markow 1987), crustaceans (e.g., Hallberg et al. 1997), salamanders (Maico et al. 2003), and mice (e.g., Wall et al. 2003). At individual level, olfactory chemoreceptor number, even nerve number, varies among individuals--for example, in Lysmata shrimp (Zhang et al. 2008, Zhu et al. 2012). Aesthetasc (olfactory chemoreceptor of crustaceans) number is sex related and varies among individuals in Lysmata shrimp (Zhang et al. 2008, Zhu et al. 2012).
Shrimp in the genus Lysmata have attracted much attention because they have an unusual reproductive system, protandric simultaneous hermaphroditism (Bauer 2000). Gonads in the shrimp are ovotestis, which have testis and ovarian portions (Bauer & Holt 1998, Fiedler 1998). Individuals mature first as males (male phase, or MP); that is, the testis portion matures first. As the shrimp grow, the ovarian portion may also develop (i.e., sex change) so that the gonad is able to produce both eggs and sperm, a condition called simultaneous hermaphroditism (euhermaphrodite phase-EP). This condition has been termed the female phase by Bauer and Holt (1998). Intermolt EP shrimp that function as a male are able to mate with the newly molted EP shrimp that function as a female. Sex change in, for example Lysmata wurdemanni, is controlled mainly socially (Lin & Zhang 2001, Baeza & Bauer 2004, Zhang & Lin 2007), and some MP shrimp may not change sex (Baldwin & Bauer 2003, Zhang & Lin 2007). There is a distinct dichotomy in the sociobiology of Lysmata species (Bauer 2000). Pair-living species (e.g., Lysmata amboinensis, Lysmata grabhami, and Lysmata debelius) live in tropical waters and are specialized fish cleaners, whereas group-living species (e.g., Lysmata boggessi and L. wurdemanni) live mostly in subtropical and temperate areas, and are unspecialized, facultative fish cleaners (Wirtz 1997, Fiedler 1998). Precopulatory behavior of Lysmata shrimp is mediated by distance pheromones secreted by the female-role shrimp, which are detected by the male-role shrimp using aesthetascs (Zhang & Lin, 2006, Zhang & Lin, 2007). The behaviors have been demonstrated to be different between species in the 2 social systems (Zhang & Lin 2007). The group-living species displays more intense precopulatory behavior (Zhang & Lin 2006) than the pair-living species (Zhang & Lin 2007). The difference in the precopulatory behaviors is probably because the group-living species have more aesthetascs than the pair-living shrimp (Zhang et al. 2008, Zhang et al. 2009).
In a previous study, we demonstrated that aesthetasc number in MP shrimp is significantly higher than that in EP shrimp, and variation of the aesthetasc number in EP shrimp is apparently greater than that in MP shrimp (Zhang et al. 2008), and the aesthetasc number is related positively to shrimp size in MP, but may not be related to shrimp size in EP (Zhu et al. 2012). Because aesthetasc number is associated with the male mating success of Lysmata shrimp (Zhang et al. 2009), the lower aesthetasc number in EP shrimp may be a result of an adaptation of EP shrimp that save and channel more energy to female activities and functions to maximize female fitness (Zhang & Lin 2005). Hence, investigating how the aesthetasc number in MP and EP Lysmata shrimp varies would improve our understanding of the relationship between reproductive strategy of MP and EP shrimp and the olfactory system.
Within a species, sexual dimorphism of chemosensors has been found in many dioecious crustaceans (reviewed by Hallberg et al. (1997)). For example, male copepods generally have more and larger aesthetascs (Ohtsuka & Huys 2001). However, sexual dimorphism of chemosensors has never been tested empirically. Shrimp of the genus Lysmata are good model organisms for this type of test because they have a protandric simultaneous hermaphroditism reproductive system. We can determine whether aesthetasc number is sex dependent by comparing the change in aesthetasc number within individual Lysmata shrimp before and after sex change. The major aim of the current study is to examine the relationship between sex change and lower aesthetasc number, and the greater variation in aesthetasc number in EP shrimp than in MP shrimp. We found previously that variation of aesthetasc number in the pair species is lower than that in the group species (Zhang et al. 2008), suggesting that aesthetasc number change also might be related to the social environment (Zhang et al. 2008). Hence, we tested the hypothesis that change of aesthetasc number is also related to the social environment for 4 species: L. boggessi and L. wurdemanni (group living), and L. amboinensis and Lysmata pederseni (pair living) from MP to EP. The shrimp L. pederseni is classified morphologically and genetically as peppermint shrimp, such as L. boggessi and L. wurdemanni (Rhyne & Lin 2006, Baeza et al. 2009), but it is a pair-living species because it exhibits a symbiotic lifestyle (is the only such peppermint shrimp found thus far (Rhyne & Lin 2006)). Therefore, change in aesthetasc number in the 4 species should provide an insight into the effect of both genetic and social factors on the olfactory system of Lysmata shrimp.
MATERIALS AND METHODS
This study was conducted at the Florida Institute of Technology's Vero Beach Marine Laboratory. Juveniles of L. pederseni and adult shrimp of L. boggessi and L. wurdemanni were collected from Marathon and Sebastian inlets in Florida, respectively. The larvae of L. boggessi and L. wurdemanni were reared to postlarvae following the protocols described by Zhang et al. (1998) and Calado et al. (2003). Juvenile L. amboinensis, originally collected in Indonesia, were bought from a pet store. The physical conditions for this experiment were as follows: water temperature, 27-28[degrees]C, salinity, 35; and a 14-h light/10-h dark cycle with a light intensity of 600-1,000 lux by a full-spectrum fluorescent light source.
Growth Pattern of Aesthetasc Number
The growth pattern of aesthetasc number was compared between the group-living (L. boggessi and L. wurdemanni) and the pair-living (L. amboinensis and L. pederseni) species. The experiment was conducted in a flow-through system consisting of 20-L tanks (32 x 25 x 25 cm), each containing 2 postlarvae (L. boggessi and L. wurdemanni) or juveniles (L. amboinensis and L. pederseni). Seven replicates for each species were conducted.
For L. boggessi and L. wurdemanni, sibling postlarvae (total length, 0.8 [+ or -] 0.1 cm) were held individually in 1-L beakers containing 800 mL seawater with gentle aeration to determine the initial aesthetasc number before being stocked in the tanks. Shrimp molts were collected, and the aesthetasc number was counted with an Olympus compound microscope. The aesthetasc number of a lateral flagellum on each row and the number of the rows were counted. Either the right or left lateral flagellum was used, because there is no difference in the number of aesthetascs between the 2 rows (Zhang et al. 2008). After determining the initial aesthetasc number, 2 postlarvae with the same or similar (the aesthetasc number difference between the 2 postlarvae is [less than or equal to]2) aesthetasc numbers were housed together. The shrimp were fed with frozen adult Artemia once daily, and the holding water was changed completely daily.
For L. amboinensis and L. pederseni, each tank contained 2 juveniles of similar size (carapace length, 5.1 [+ or -] 0.2 mm for L. amboinensis and 3.6 [+ or -] 0.2 mm for L. pederseni). The shrimp were fed with frozen adult Artemia once daily. The shrimp were checked daily for molts, and aesthetascs were counted.
Student's t-test was used for the comparison of aesthetasc number of the fast growers at sex change and the slow growers that had not yet changed sex, and between the aesthetasc numbers of the slow growers and the fast growers at sex change (see Results for the meaning of fast and slow grower). To compare the growth pattern of the aesthetasc number in MP and EP shrimp, aesthetasc increments within the 2 molts before and after sex change were compared using Student's t-test.
The shrimp Lysmata boggessi was monitored over 22 molts (about 155 days). Aesthetasc number increased over the molts in MP shrimp and the early several molts in EP shrimp. Of the 2 shrimp in a tank, one grew faster than the other. The fast growers changed sex 15-24 days (2-3 molt durations) earlier than the slow growers. Aesthetasc number of the fast growers (mean [+ or -] SD, 118.8 [+ or -] 2.9) at sex change was significantly greater (Student's t-test, t = 11.763, df = 12, P < 0.001) than that of slow growers (99.6 [+ or -] 3.2) that had not yet changed sex. After the fast growers became EP, the aesthetasc number of the slow growers before sex change increased faster than the fast growers. Aesthetasc number of the slow growers exceeded that of the fast growers in about 15 days (2 molt durations) when the slow growers were still MP after the fast growers became EP (Fig. 1A). The aesthetasc number of the slow growers (147.9 [+ or -] 3.1) at sex change was significantly greater (Student's t-test, t = 6.713, df = 12, P < 0.001) than that of the fast growers (138.4 [+ or -] 2.1) at sex change. After changing sex, the aesthetasc numbers of both the EP shrimp grew slowly to a stable level, then decreased slightly and even declined. However, the aesthetasc number of the earlier sex changers was never higher than that of the late sex changers (Figs. 1A and 2). Aesthetasc increments within the 2 molts before sex change (38.2 [+ or -] 3.7) were significantly greater (Student's t-test, t = 10.168, df = 12, P < 0.001) than after sex change (19.4 [+ or -] 3.2; Fig. 2).
The shrimp L. wurdemanni was monitored over 20 molts (about 155 days). The fast growers changed sex 14-22 days (2-3 molt durations) earlier than the slow growers. The growth pattern of aesthetasc number is the same as that in L. boggessi (Figs. 1B and 2). Aesthetasc number of the fast growers (120.4 [+ or -] 2.8) at sex change was significantly greater (Student's t-test, t = 8.213, df= 12, P < 0.001) than that of slow growers (107.2 [+ or -] 3.2) that had not yet changed sex. After the fast growers became EP, the aesthetasc number of the slow growers before sex change increased faster than the fast growers. The aesthetasc number of the slow growers (145.3 [+ or -] 2.4) at sex change was significantly greater (Student's t-test, t = 6.969, df= 12, P < 0.001) than that of the fast growers (136.9 [+ or -] 2.1) at sex change. Aesthetasc increments within the 2 molts before sex change (41.3 [+ or -] 4.2) were significantly greater (Student's t-test, t = 12.908, df = 12, P < 0.001) than after sex change (16.4 [+ or -] 2.9; Fig. 2).
[FIGURE 1 OMITTED]
[FIGURE 2 OMITTED]
The shrimp L. amboinensis was monitored for about 170 days. The fast grower changed sex 12-24 days (1-2 molt durations) earlier than the slow grower. As in L. boggessi and L. wurdemanni, the aesthetasc number of the first sex changer (93.9 [+ or -] 4,8) was significantly lower (Student's t-test, t = 6.800, df = 12, P < 0.001) than that of the second sex changer (118.1 [+ or -] 8.1) when they changed sex. After changing sex, the aesthetasc number increased slightly, then started declining during several molts (Figs. 1C and 2). Aesthetasc increments within the 2 molts before sex change (16.3 [+ or -] 2.4) were significantly greater (Student's t-test, t = 13.006, df = 12, P < 0.001) than after sex change (3.7 [+ or -] 0.9; Fig. 2).
The shrimp L. pederseni was monitored for about 140 days. The fast grower changed sex 1-8 days (0-1 molt duration) earlier than the slow grower. Like the other 3 species, the aesthetasc number of the first sex changer (122.6 [+ or -] 2.4) was significantly lower (Student's t-test, t = 2.246, df = 12, P = 0.044) than that of the second sex changer (132.1 [+ or -] 11.0) when they changed sex. After changing sex, aesthetasc number increased slowly to a stable level, then started decreasing slightly from the 5th molt after sex change (Figs. 1D and 2). Aesthetasc increments during the 2 molts before sex change (29.6 [+ or -] 4.1) were significantly greater (Student's t-test, t = 11.801, df = 12, P < 0.001) than after sex change (7.2 [+ or -] 2.9; Fig. 2).
Sexual dimorphism in aesthetasc number has been found in many dioecious crustaceans (reviewed by Hallberg et al. 1997). However, the dimorphism has never been confirmed empirically to be sex dependent. In the current study, we found that aesthetasc number of the 4 shrimp species in the genus Lysmata during the MP increased significantly faster than during the EP (Figs. 1 and 2), confirming empirically that aesthetasc number is sex dependent. As in many dioecious crustacean species (e.g., Johansson & Hallberg 1992, Shenoy et al. 1993, Ohtsuka & Huys 2001), MP Lysmata shrimp normally bear greater numbers of aesthetascs than EP shrimp (Zhang et al. 2008, Zhu et al. 2012), and the results obtained from the previous study clearly indicate that this is a proximate cause of the difference in mating success between MP and EP shrimp serving the male role (Zhang et al. 2009). Different from dioecious species, Lysmata shrimp change sex. MP or male-role EP shrimp use the aesthetasc to detect the soluble sex pheromone secreted by female-role shrimp. Aesthetasc number increased slightly then declined after MP shrimp changed sex to EP shrimp (Fig. 1), suggesting that the decrease in aesthetasc number in EP shrimp (especially in group-living species) is probably an adaption to the reduced male-role mating activity (Zhang & Lin 2004, Zhang et al. 2009), which allows the shrimp to channel more energy to female activities and function (Zhang & Lin 2005). Aesthetasc number related to mating success might be a cause of sexual selection and speciation in the group-living Lysmata species because "rates of speciation may depend on sensory abilities, and on the scope for distinct variation of traits used in mate recognition" (Andersson 1994, p. 223).
Our previous studies indicate that variation in aesthetasc number of EP shrimp of similar size is greater than that of MP shrimp of similar size (Zhang et al. 2008), and there is no significant relationship between shrimp size and aesthetasc number in EP shrimp (Zhu et al. 2012). Aesthetasc number increased significantly faster before sex change than after sex change (Figs. 1 and 2), indicating explicitly that aesthetasc number change is sex dependent. Our current study shows that the aesthetasc number of both MP and EP shrimp is related to the timing of the sex change, and the late sex changer has a greater aesthetasc number than the earlier sex changer. This is the major reason contributing to the high variation of aesthetasc number in EP shrimp, and probably why there is no significant relationship between shrimp size and aesthetasc number in EP shrimp (Zhu et al. 2012). In L. pederseni, there is a marginally significant difference in aesthetasc number between the early and late sex changers at sex change because the timing of sex change was similar ([less than or equal to] 1 molting cycle) between the 2 shrimp.
Although the general growth patterns of aesthetasc number in the 4 species are similar (i.e., the number increased consistently in MP shrimp and increased slowly, and even decreased, after MP became EP), there is slight difference among the 4 species. Aesthetasc number in L. boggessi and L. wurdemanni (groupliving species) increased considerably (38.2 [+ or -] 3.7 for L. boggessi and 41.3 [+ or -] 4.2 for L. wurdemanni) within the 2 molts before sex change, moderately (16.3 [+ or -] 2.4) in L. amboinensis, and intermediately (29.6 [+ or -] 4.1) in L. pederseni (Fig. 2). This difference is probably associated with both social environment and genetics. The shrimp L. pederseni is similar morphologically and genetically to group-living species, such as L. wurdemanni and L. boggessi (Rhyne and Lin 2006, Baeza et al. 2009), but is a pair-living species like L. amboinensis.
In previous studies, we have proposed the ultimate and proximate reasons to explain the difference in aesthetasc number between the pair-living and group-living species (Zhang & Lin 2005, Zhang et al. 2008, Zhang et al. 2009). Ultimately, the pair-living shrimp do not need to search actively for mates as those species living in aggregation do because the shrimp are confined in a small habitat (Wirtz 1997, Fiedler 1998, Rhyne & Lin 2006, Zhang et al. 2007). In the group-living species, because of the high competition in obtaining a mating partner, shrimp with a greater number of aesthetascs are more sensitive to capturing signals, so they have a greater chance of obtaining a mating partner (Zhang et al. 2009). Alternatively, higher stimulation frequency by soluble pheromone to the chemoreceptors in the group-living species than in the pair-living species may be one of the major factors to shape the difference in aesthetasc number of shrimp in the 2 social systems. In the group-living species, shrimp are provoked more frequently by soluble pheromone released from premolt EP shrimp than in pair-living species. The relationship between chemical stimulus and the number of olfactory sensilla has been demonstrated (Rosselli-Austin & Williams 1990, Chapman & Lee 1991). For example, enriched neonatal odor exposure leads to increased numbers of olfactory bulb mitral and granule cells (RosselliAustin & Williams 1990), and the number of olfactory sensilla on the antennae of the grasshopper Schistocerca americana increased when the insects were exposed to less complex odors (Chapman & Lee 1991). Whether the effect of the soluble pheromone on the olfactory system of Lysmata shrimp is similar to that of food odor on the olfactory system of insects is worth investigating in the future.
This study was supported in part by Proaquatix, Inc., and the National Science Foundation of China (project no. 30970445).
Andersson, M. 1994. Sexual selection. Princeton, N J: Princeton University Press. 599 pp.
Baeza, J. A. & R. T. Bauer. 2004. Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behav. Ecol. Sociobiol. 55:544-550.
Baeza, J. A., C. D. Schubart, P. Zillner, S. Fuentes & R. T. Bauer. 2009. Molecular phylogeny of shrimp from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and social monogamy. Biol. J. Linn. Soc. Lond. 96:415-424.
Baldwin, A. P. & R. T. Bauer. 2003. Growth, survivorship, life span, and sex change in the hermaphroditic shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Mar. Biol. 143:157-166.
Bauer, R. T. 2000. Simultaneous hermaphroditism in caridean shrimp: a unique and puzzling sexual system in the Decapoda. J. Crustac. Biol. 20): 116-128.
Bauer, R. T. & G. J. Holt. 1998. Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Mar. Biol. 132:223-235.
Calado, R., L. Narciso, S. Morais, A. L. Rhyne & J. Lin. 2003. A rearing system for the culture of ornamental decapod crustacean larvae. Aquaculture 218:329-339.
Chapman, R. F. & J. C. Lee. 1991. Environmental effects on numbers of peripheral chemoreceptors on the antennae of a grasshopper. Chem. Senses 16:607-616.
Cowan, D. F. 1991. The role of olfaction in courtship behavior of the American lobster Homarus americanus. Biol. Bull. 181:402-407.
Derby, C. D. & J. Atema. 1982. The function of chemo- and mechanoreceptors in lobster (Homarus americanus) feeding behaviour. J. Exp. Biol. 98:317-327.
Derby, C. D., P. Steullet, A. J. Horner & H. S. Cate. 2001. The sensory basis of feeding behaviour in the Caribbean spiny lobster, Panulirus argus. Mar. Freshw. Res. 52:1339-1350.
Fiedler, G. C. 1998. Functional, simultaneous hermaphroditism in female-phase Lysmata amboinensis (Decapod: Caridea: Hippolytidae). Pac. Sci. 52:61-69.
Gleeson, R. A. 1982. Morphological and behavioral identification of the sensory structures mediating pheromone reception in the blue crab, Callinectes sapidus. Biol. Bull. 163:162-171.
Hallberg, E., K. U. I. Johansson & R. Wallen. 1997. Olfactory sensilla in crustaceans: morphology, sexual dimorphism, and distribution patterns. Int. J. Insect Morphol. Embryol. 26:173-180.
Homer, A. J., M. J. Weissburg & C. D. Derby. 2008. The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, Panulirus argus, to conspecific urine signals. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 194:243-253.
Johansson, K. U. I. & E. Hallberg. 1992. Male-specific structure in the olfactory system of mysids (Mysidacea: Crustacea). Cell Tissue Res. 268:359-368.
Johnson, M. E. & J. Atema. 2005. The olfactory pathway for individual recognition in the American lobster Homarus americanus. J. Exp. Biol. 208:2865-2872.
Lin, J. & D. Zhang. 2001. Reproduction in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni: any two will do? Mar. Biol. 139:919-922.
Maico, L. M., A. M. Burrows, M. P. Mooney, M. I. Siegel, K. P. Bhatnagar & T. D. Smith. 2003. Size of the vomeronasal organ in wild microtus with different mating strategies. Acta Biol. Hung. 54:263-274.
Markow, T. A. 1987. Behavioral and sensory basis of courtship success in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 84:6200-6204.
Ohtsuka, S. & R. Huys. 2001. Sexual dimorphism in calanoid copepods: morphology and function. Hydrobiologia 453/454:441-466.
Rhyne, A. & J. Lin. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on L. rathbunae (Crustacea: Decapoda: Hippolytidae). Bull. Mar. Sci. 79:165-204.
Rosselli-Austin, L. & J. Williams. 1990. Enriched neonatal odor exposure leads to increased numbers of olfactory bulb mitral and granule cells. Brain Res. Dev. Brain Res. 51:135-137.
Shenoy, S., D. R. Jalihal & K. N. Sankolli. 1993. Ecological diversity with reference to aesthetascs in freshwater prawns. Crustaceana 65:300-308.
Wall, W. B. V., M. J. Beck, J. S. Briggs, J. K. Roth, T. C. Thayer, J. L. Hollander & J. M. Armstrong. 2003. Interspecific variation in the olfactory ability of granivorous rodents. J. Mammal. 8:487-496.
Wirtz, P. 1997. Crustacean symbionts of the sea anemone Telmatactis cricoids at Madeirn and the Cannary Island. J. Zool. (Lond.) 242:799-811.
Zhang, D., S.- L. Cai, H. Liu & J. Lin. 2008. Antennal sensilla in the genus Lysmata (Caridea). J. Crustac. Biol. 28:433-438.
Zhang, D. & J. Lin. 2004. Fertilization success without anterior pleopods in shrimp Lysmata wurdemanni, a protandric simultaneous hermaphrodite (Crustacea: Decapoda: Caridea). J. Crustac. Biol. 24: 470-473.
Zhang, D. & J. Lin. 2005. Comparative mating success of smaller male-phase and larger male-role euhermaphrodite-phase shrimp, Lysmata wurdemanni (Caridea: Hippolytidae). Mar. Biol. 147:1387-1392.
Zhang, D. & J. Lin. 2006. Mate recognition in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Caridea: Hippolytidae). Anim. Behav. 71:1191-1196.
Zhang, D. & J. Lin. 2007. Effects of density and simulated recruitment and mortality on sex change in a protandric simultaneous hermaphroditic shrimp, Lysmata wurdemanni. Mar. Biol. 150:639-645.
Zhang, D., J. Lin & R. L. Creswell. 1998. Effects of the food and temperature on survival and development in the peppermint shrimp Lysmata wurdemanni. J. World Aquacult. 29:471-476.
Zhang, D., J. Lin & C. Huang. 2009. Relationship between olfactory sensor number and mating in a marine shrimp, Lysmata wurdemanni. Mar. Freshw. Behav. Physiol. 42:265-273.
Zhang, D., A. L. Rhyne & J. Lin. 2007. Density-dependent effect on reproductive behaviour of Lysmata amboinensis and L. boggessi (Decapoda: Caridea: Hippolytidae). J. Mar. Biol. Assoc UK87:517-522.
Zhu, J., D. Zhang, J. Lin & M. S. Grace. 2012. Aesthetascs in Lysmata spp. shrimp: sexual dimorphism and relationship with social environments. Mar. Biol. 159:507-517.
DONG ZHANG, (1,2) * ZONGLI YAO, (1) QIFANG LAI (1) AND JUNDA LIN (2)
(1) East China Sea Fisheries Research Institution, Chinese Academy of Fisheries Sciences, 300 Jungong Road, Shanghai 200090, P. R. China; (2) Vero Beach Marine Laboratory, Florida Institute of Technology 805 E. 46th Place, Vero Beach, FL 32963
* Corresponding author. E-mail: firstname.lastname@example.org
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