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Ontogenetic development of sensory structures on the antennules and antennae of the giant river prawn Macrobrachium rosenbergii (De Man).

ABSTRACT In this study the occurrence of sensory structures on the antennules and antennae of the giant river prawn Macrobrachium rosenbergii (De Man) during postembryonic ontogenetic development were examined. Larvae and postlarvae were obtained from hatchery recirculating tanks, juveniles from indoor nursery tanks, and adults from earthen grow-out ponds. The animals were fixed with Karnovsky fixative and dissected. Antennules and antennae were removed, metal-coated, and photodocumented using a scanning electron microscope. The antennules have aesthetascs and simple plumose and pappose setae; the antennae have simple, plumose and pappose setae. These structures increase in density, covered surface, and distribution during ontogeny and should be related to chemoreception and mechanoreception. The antennular statocyst that appears during larval stage VII of the giant river prawn has an array of sensory structures that enable the perception of chemical and tactile stimuli beginning with its early life stages. The ontogenetic changes observed allow an inference that initial-stage larvae, advance-stage larvae, juveniles, and adults have different capacities to exploit the environment.

KEY WORDS: aesthetascs, sensory structures, chemoreception, mechanoreception, antennule, antenna, Macrobrachium rosenbergii, giant river prawn

INTRODUCTION

Chemoreception and mechanoreception are the main methods used by decapod crustaceans to identify food particles and locate mates (Anger 2001, Bauer 2004). In general, these functions are performed by specialized structures on the body and appendages. These structures are cuticular extensions, with shafts of different shapes and sizes, that can function as mechanoreceptors and/or chemoreceptors. Most are bimodal mechanoreceptors-chemoreceptors, combining the anatomic characteristics and functions of the 2 types. The largest concentrations of tegumentary sensors are found on the antennules, antennae, mouth appendages, and pereiopods, which most often encounter food and substrate (Anger 2001). In addition to sensory reception, these integumental structures may act in a variety of vital functions, including locomotion, feeding, cleaning of the body and gills (Felgenhauer 1992, Bauer 2004), and mate recognition (Zhu et al. 2012).

Some descriptions of the sensory structures of decapod crustaceans have been reported (e.g., Ghiradella et al. 1968a, Ghiradella et al. 1968b, Ghiradella et al. 1968c, Ghiradella et al. 1970, Hallberg et al. 1992, Lavalli & Factor 1992, Johnson & Atema 2005, Zhu et al. 2012), but peer-reviewed studies on these structures in Macrobrachium spp. are extremely scarce. Shenoy et al. (1993) reported that the aesthetascs (small hairlike end organs on the antennular flagella) in Macrobrachium spp. that are borne apically during the early larval stages start shifting downward gradually in late-stage larvae and finally become arranged segmentally during the postlarval and juvenile phases, when the flagellar segments increase in number. Structurally they are very similar to those of adults but without any annulations on the stalk. According to Shenoy et al. (1993), the transformation from larval aesthetascs to the characteristic adult shape varies with the type of larval development. In species with prolonged larval development, such as Macrobrachium rosenbergii (De Man), Macrobrachium malcolmsonii (Milne Edwards), Macrobrachium idella (Hilgendorf), Macrobrachium equidens (Dana), and so on, which essentially require some amount of salinity for their metamorphosis, Shenoy et al. (1993) noted that it is only during the late larval stages that the aesthetascs gradually tend to become shorter and stouter. More recently, Bauer and Caskey (2006) described the antennal setae of Macrobrachium ohione (Smith) with a focus on mate recognition and sexual dimorphism.

Giant river prawns have the greatest importance among all the freshwater prawn species in global fisheries and aquaculture (New & Nair 2012), although other Macrobrachium species, such as Macrobrachium nipponense (De Haan), have significant national or regional importance. In common with many other species of the genus (Jalihal et al. 1993), Macrobrachium rosenbergii has a planktonic stage in brackishwater and a benthic stage in freshwater (Ling & Merican 1961). In addition, it performs extensive migration with or against the current, according to the stage of the life cycle or its physiological state, and changes its feeding habit from carnivorous to omnivorous (John 1957, George 1969, Ling 1969).

Observations of the aesthetascs of Macrobrachium spp. that depend on a change in salinity for metamorphosis indicate that structural changes during the larval phase may be related to the level of salinity requirement or salinity dependence during their development (Shenoy et al. 1993). This phenomenon may also reflect the marine ancestry of these species. Other than the work of Shenoy et al. (1993) and Bauer and Caskey (2006), no other relevant literature has been found, indicating that a more detailed examination of the aesthetascs of Macrobrachium rosenbergii would be valuable. Based on this premise, the occurrence of sensory structures on the antennules and antennae during the postembryonic ontogenetic development of M. rosenbergii was investigated through the use of electron microscopy.

[FIGURE 1 OMITTED]

MATERIALS AND METHODS

Culture and Maintenance of Prawns

All the animals used were obtained from the stock of the Crustacean Sector of the Aquaculture Center, Sao Paulo State University, Brazil. Larviculture was conducted in a recirculating system according to the methods of Valenti et al. (2009). The larvae were fed Artemia nauplii during their entire cycle, and artificial feed (see formulation in Mallasen and Valenti [1998]) was added at stage VII onward (Barros & Valenti 2003). Postlarvae were maintained in indoor nursery tanks (1,000 L. with recirculation) to the juvenile stage, at a density of 6 postlarvae/L. The animals were fed a commercial feed containing 38% crude protein. Temperature was maintained at 30 [+ or -] 1[degrees]C by thermostats and heaters. The juveniles analyzed were 5 wk old. Adult prawns were taken from earthen grow-out ponds, stocked at a density of 8 individuals/[m.sup.2], and had been reared on a commercial pelleted feed (35% crude protein). Males and females with a mean length of 16 cm, which showed all secondary sex characteristics, were analyzed.

Collection, Fixation, and Dissection of the Animals

Ten animals for each larval stage--10 postlarvae, 10 juveniles, and 6 adults--were sampled at random. The animals were placed in plastic flasks with Karnovsky fixative and stored in a refrigerator for 24 h. They were then washed and stored in 0.1 M sodium cacodylate buffer. The antennules and antennae were removed from each animal under stereomicroscopy for observation of the sensory structures.

Scanning Electron Microscopy

The antennules and antennae were postfixed in an osmium tetroxide solution for 2 h, dehydrated in an ascending ethanol series from 30%-100%, dried in a TOUSIMIS 780-A critical-point dryer, metal-coated, and photographed using JEOL JSM-5410 and JEOL 5.200 electron microscopes.

Sensory structures were classified according to external morphology based on the pattern used previously for crustaceans (Felgenhauer 1992, Lavalli & Factor 1992, Bauer 1999, Zenon et al. 2001). Although all the development stages were analyzed, herein only photographs of stages in which important differences were found are illustrated.

RESULTS

Antennules

Setae for both chemical and mechanical reception were identified on the antennules. Plumose setae and aesthetascs are present on the peduncle, and simple setae on the antennular flagellum were noted, from stage I larvae to adults. Serrate setae were found only on the statocysts, which appear during larval stage VII. All setae increase in density and area of distribution during ontogenesis. The antennule is an appendix with large concentrations of chemical receptors, such as plumose setae.

During zoea I, the antennular peduncle is unisegmented. One plumose seta occurs on the basal region. Aesthetascs were identified from this stage onward. During zoea II (2-day-old larvae), the peduncle has 2 segments, with some plumose setae on the articulations and distal region of the segments (Fig. 1A). During zoea III, the terminal segment has 2 long plumose setae. During larval development, the setae enlarge in the distal region of the segments. During all larval stages (Figs. 1A-F and 3 A), the plumose setae are smaller, with sparse setules in relation to juveniles (Fig. 1G, H) and adults (Fig. 2A-C). During the juvenile stage, the peduncle widens and the plumose setae are larger and are arranged on the margins of the articles in high density (Fig. 1G, H). During all stages, the plumose setae have a thin cuticle. The aesthetascs were found to increase in number and length during development (Fig. 3B). They are long, smooth, and segmented, and apparently have no apical orifice. Simple setae are inserted on the surface of the antennular peduncle in juveniles (Fig. 3C).

Simple setae occur on the antennular flagellum during all ontogenetic stages. They are short and smooth, and are arranged in tufts inserted in a basal orifice located in the distal region of the articles. Four or 5 simple setae were observed during larval stage X (Fig. 3B) and in juveniles (Fig. 3F).

Statocysts appear in the proximal region of the antennular peduncle from stage VII onward. During the earlier larval stages, only a tumescence was observed in the same position. Figures 3D and E illustrate the statocyst of a juvenile that has simple setae interspersed with serrate ones. The serrate setae are robust, with strong setules along the setal shaft. The setules are dentiform and are set along the shaft in opposite positions to each other. Simple setae are smooth and are similar in size to the serrate setae (Fig. 3E).

[FIGURE 2 OMITTED]

Antennae

Antennae occur from the first larval stage onward and may have plumose, pappose, or simple setae on their exopodites. Plumose setae are present during all life stages, and increase in size and density during ontogenesis; however, pappose setae appear during the postlarval stage and simple setae during the juvenile stage. The most characteristic antennal seta is the plumose type, which is located on the margin of the exopodite. Occurring during all larval stages, they are transformed into short setae with perforated tips in adults (Fig. 4H). The antennal flagellum bears simple setae during all life stages.

During zoea I, the antennal exopodite is long, with a small spine in the distal region. The margin has plumose setae with well-spaced setules. The antennal flagellum is unisegmented and has 1 plumose seta on its extremity. No setae were seen along the antennal flagellum; these occur only during the following stages. During larval stage II, the setae increase slightly in density. This characteristic continues until zoea V, when 18 plumose setae appear (Fig. 4A). From this stage onward, the plumose setae on the margin of the exopodite are set more closely, as seen during stage X (Fig. 4B). These differences are more marked in the juvenile (Fig. 4C), when the setules become more dense. The plumose setae have long setules, which are arranged in opposition to each other on the setal shaft and slant upward. The cuticle is slight and the setae probably have both chemical and mechanical functions. Although the general developmental pattern of the exopodite setae is similar throughout most stages, in the adult it is possible to perceive some morphological differences. Setules occur only on setae that have short setal shafts (Fig. 4D). The setules do not reach the neighboring setal shafts, and the tips are perforated (Fig. 4G, H).

[FIGURE 3 OMITTED]

A special type of simple setae was observed from the juvenile stage onward. These setae are organized in groups of 3, with an apical orifice, and are set between each plumose seta of the exopodite (Fig. 4E, F). They are short, smooth, and have an apical orifice. The groups of 3 are closely united in a rectilinear arrangement and do not surpass the basal septum. These setae have the typical structure of chemoreceptors.

From postlarvae onward, the antennal peduncle has 3 segments. Pappose setae are present on the middle article from this stage onward, as shown in the juvenile (Fig. 5F). These pappose setae have 2 distinct rows of long, light, delicate setules, which are inserted alternately on the setal shaft. On the articulation of the basal orifice is a protective covering that consists of a layer with grooves and an irregular upper edge. On one side of the setal sheath, the edge is lower; near the other edge it slopes upward, thus it is higher than on the opposite side (Fig. 5F).

The antennal flagellum has simple setae, clustered at the apex, during all life stages (Fig. 5A-D). Simple setae also appear along the antennal flagellum, except in zoea XI (Fig. 5E), arranged in the distal region of each antennal segment. These are short and are inserted in a basal orifice, characteristic of a sensory structure. No aesthetascs were observed in the antennae.

DISCUSSION

Aesthetascs have been shown to be olfactory in decapods (Ache 1982); they enable the sensory perception of highly soluble compounds in very low concentrations at a distance from their source. Thus, antennular chemoreceptors make possible the detection of low-molecular weight stimuli, such as olfactory sex pheromones or food attractants, at some distance from the source of the odor stimulus. These substances can stimulate sexual or appetite behavior and can orient the animal toward potential mates or food. The addition of a chemoattractant, such as betaine, taurine, glycine, or proline, to rearing water stimulates a vigorous search for food and leads to increased weight gain over time in Macrobrachium rosenbergii (Harpaz & Steiner 1990, Harpaz 1997). Meyers and Zein-Eldin (1972) discovered that carideans have a strong preference for more odoriferous foods, because diffusion of certain substances in the water stimulated individuals to approach. Barros and Valenti (1997) observed some larvae of M. rosenbergii swim actively toward food, mainly during the final zoeal stages (VII-XI). Therefore, there can be a presumption that the aesthetascs and plumose setae of the antennules have an olfactory chemoreception function in M. rosenbergii. These organs may confer a capacity to locate food in the water column and/or on the substrate, and also for mate recognition. Attractiveness experiments are necessary to confirm this hypothesis.

[FIGURE 4 OMITTED]

The neuroanatomy of crustaceans suggests that aesthetascs would be essential to all complex chemosensory tasks. Steullet et al. (2002) showed that aesthetascs are not required for seemingly complex olfactory tasks in Caribbean spiny lobsters (Panulurus argus Latreille); when aesthetascs were ablated, the animals could still discriminate between complex food odor mixtures. On the other hand, Johnson and Atema (2005) demonstrated that American lobsters (Homarus americanus Milne Edwards) with ablated aesthetascs could not recognize previous opponents. It is clear that the exact description and function of aesthetascs in crustaceans need further investigation.

Bauer (2004) stated that the antennal flagella of carideans have abundant tactile and chemoreceptors, especially for gustation. They respond to insoluble, surface-bound, or very low-solubility compounds at high concentration (contact chemoreception). In addition, they can be used in the perception of female contact pheromones by males. Adults of Macrobrachium rosenbergii showed simple setae similarly to Macrobrachium ohione (Bauer & Caskey 2006), but not denticulate ones. In addition, M. rosenbergii showed plumose setae, which were absent in M. ohione.

[FIGURE 5 OMITTED]

The feeding process is probably related to the morphological and physiological development of the sensory structures of Macrobrachium rosenbergii. Plumose setae occur on the antennules and antennae as soon as the larvae hatch. During development, they increase in number and in the size of the setal shaft, but the variation in types is minimal. In the juvenile, different setae arise on the antennae, such as simple setae with an apical orifice. They may be associated with the perception of food deposited on substrates by direct contact, because at this stage the animals assume a benthic habitat. These new setae may also be associated with the detection of salinity and/or current direction, facilitating migration to freshwater. No different setae arise in adults, suggesting the setae used for sex pheromone detection are present since the juveniles phase. Thus, they probably are not used exclusively for sexual functions. Similar increases in sensory structures during development have been observed in other decapods (Bauer 2004). An increase in setae on the antennae and antennules from zoea I to the juvenile stage of Macrobrachium amazonicum (Heller) was observed by Vega-Peres (unpubl. data). On the other hand, Lavalli and Factor (1992) reported that the setae on the mouthparts of Homarus americanus diversify during larval development.

In the current study, several sensory structures were observed on the antennules and antennae of Macrobrachium rosenbergii during all postembryonic stages. Aesthetascs were present in the antennules and absent on the antennae, as has been observed in general in decapod crustaceans (Bauer & Caskey 2006). The sensory structures observed indicate that M. rosenbergii larvae are born with an apparatus that allows them to exploit the environment. Thus, it is very improbable that they feed themselves merely by chance encounters during the larval phase, as assumed by Moller (1978). In addition, it is likely that this species enhances its capacity to interact with the environment during ontogenesis, because of the increase in sensory structures. This information should be considered when planning facilities and developing diets for farming M. rosenbergii. It can assist in the development of techniques for stress management and can facilitate the capture and ingestion of food, thus improving animal welfare and increasing productivity in commercial culture.

The larvae of Macrobrachium rosenbergii live in an estuarine meroplankton (John 1957, George 1969) and take part in the dynamics of this environment. Larvae of M. rosenbergii require brackishwater for development (Ling 1969). Thus, ovigerous females migrate downstream and, after the larvae hatch, they are swept along by the water flow (Ling & Merican 1961). Estuary dynamics are driven by 4 tidal changes, altering the current direction and forming thermal and saline stratifications. Thus, larvae should perceive the changes in the environment to position themselves in the most appropriate water layer. Certain parameters, such as light intensity, hydrostatic pressure, temperature, salinity, and chemical factors, provide information for larval orientation, if the larvae can detect spatial gradients. In the current study, it was demonstrated that M. rosenbergii has an apparatus of sensory structures that could perceive these variations. The sensory setae, such as aesthetascs and plumose setae, confer a capacity for chemical perception and may play an important role in early larval stages, when the larvae float in the water column and have no statocysts. This structure, which is covered by a variety of mechanoreceptors, first appears at the base of the antennules during larval stage VII. Thus, statocysts must coordinate the direction of larval movement. Actually, during this phase, the larvae swim in a more coordinated way (pers. obs.) and actively seek inert foods (Barros & Valenti 2003). On the other hand, it is known that juveniles and adults can perceive salinity (Derby & Harpaz 1988), and this may be important in the process of migration to freshwater. Therefore, the sensitive structures observed in the antennules and antennae of M. rosenbergii are likely to play an important role in the survival strategy of the species in the environment.

The morphological and functional diversification of setae may be associated with the life cycle stage and the habitat occupied. In Macrobrachium rosenbergii, some different types of setae appeared concomitantly with the change from a planktonic to benthic habitat, which coincides with larval migration from an estuarine habitat to freshwater. Nevertheless, most modifications occur gradually, with a continuous increase in the density and diversity of sensory structures. Therefore, the adaptations of the larvae seem to be more related to ontogenetic development than to the habitat occupied.

In conclusion, the larvae of Macrobrachium rosenbergii are born with an apparatus of sensory structures that allows them to perceive and exploit the environment. It is assumed these structures must have been developed during the course of evolution to make it possible to seek and capture food, as well as to position the animals in the water column. The ontogenetic changes observed allow an inference that larvae during the initial stages, larvae during advanced stages, juveniles, and adults all have different capacities to exploit the environment. This capacity must increase with development, because larger numbers of sensory structures arise during ontogenetic development. Further studies are necessary to prove the association between the sensory structures of giant river prawns and the detection of food and salinity.

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VIRGINIA MARIA CAVALARI HENRIQUES, (1) GUILHERME FULGENCIO DE MEDEIROS, (2) MICHAEL B. NEW, (3) LAURA SATIKO OKADA NAKAGHI (4) AND WAGNER C. VALENTI (5) *

(1) UFERSA--Federal University of Semi-Arid, Rua Otavio Lamartine, 657 Petropolis Natal, RN, Brazil 59020-050; (2) UFRN--Federal University of Rio Grande do Norte, Department of Oceanography and Limnology, Natal, RN, Brazil 59078-900; (3) Amazon River Prawn Research Network, Wroxton Lodge, Institute Road, Marlow, Bucks SL71BJ, UK; (4) UNESP--Sao Paulo State University, Aquaculture Center, FCAV, Department of Morphology and Physiology, Jaboticabal, SP, Brazil 19884-900; (5) UNESP--Sao Paulo State University, Aquaculture Center, Coastal Campus of Sao Vicente, Praga Infante Dom Henrique s/n, Sao Vicente, SP, Brazil 11330-900

* Corresponding author. E-mail: wcvalenti@gmail.com

DOI: 10.2983/035.033.0318
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Author:Henriques, Virginia Maria Cavalari; De Medeiros, Guilherme Fulgencio; New, Michael B.; Nakaghi, Laur
Publication:Journal of Shellfish Research
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Date:Dec 1, 2014
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