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Larval biology of the crab Rhithropanopeus harrisii (Gould): a synthesis.

Introduction

The older literature on the distribution and life history of Rhithropanopeus harrisii (Gould) is reviewed by Williams (1984). Adults live subtidally in low-salinity areas of estuaries along the east coast of North and Central America, have been introduced to the west coast of the United States and Europe, and have recently been found in Japan (Masatsugu et al., 2007) and the Panama Canal (Roche and Torchin, 2007). The reproductive season varies with latitude (reviewed by Goncalves et al., 1995a). It occurs from July to August in northern areas, May to September in temperate areas, and April to November in southern areas such as the Gulf of Mexico (e.g., Hasek and Rabalais, 2001). The larvae of this species pass through four zoeal stages and a postlarval or megalopa stage that are planktonic before metamorphosing to the benthic juvenile (Connolly, 1925). The best descriptive drawings of the larvae and megalopal stages are shown in Costlow and Bookhout (1971). Since this species has been extensively studied, this synthesis is designed to review the physiological ecology and behavior of larvae throughout development to provide general concepts about larval crustaceans and zooplankton in general.

Larval Release

Although adults occur in salinities from about 0-18 ppt (Ryan, 1956) in estuaries, reproductive areas for R harrisii are limited by the presence of the rhizocephalan parasite Loxothylaxus panopaei. Female cyprids of the parasite settle on R. harrisii megalopae (Walker et al, 1992), causing sterilization of both adult males and females (Ritchie and Hoeg, 1981; Hoeg, 1995). However, infection by the parasite does not cause mortality in adult crabs when they are acclimated to salinities from 0 to 30 ppt. Larvae of L. panopaei survive poorly at salinities below 10 ppt but well in salinities from 10 to 15 ppt (Reisser and Forward, 1991). Thus, R. harrisii has a reproductive refuge below 10 ppt. During any summer, a gradient of reproducing females is observed in estuaries, with ovigerous R. harrisu common in low-salinity areas. Their numbers decrease and parasitized crabs increase upon moving seaward into higher salinity areas or as salinities increase in any one area.

At normal summer temperatures above 20 [degrees]C, embryo development takes about 10 days (unpubl. data). R. harrisii females, like those of most crabs, release larvae as a burst lasting less than 15 min. During larval release, the female elevates on her walking legs and vigorously pumps her abdomen, releasing larvae with each pump. For all crab species the timing of larval release is not random but occurs at times related to local tides and the light:dark cycle. When placed under constant conditions of temperature, salinity. and lighting in the laboratory, females continue to release larvae at specific times, which suggests the presence of an endogenous rhythm in larval release. An endogenous rhythm is normally defined as a biological activity that oscillates under constant conditions for a number of cycles and which has a free-running period length close to 24 h for a circadian rhythm and 12.4 or 24.8 h for a circatidal rhythm (Dunlap et al., 2004). A rhythm is free-running under constant conditions because it is not exposed to external timing cues, such as the light:dark cycle. Since larval release by crabs is usually a single event or at best two events, the criterion of the persistence of the rhythm for a number of cycles under constant conditions cannot be fulfilled. Thus, among crabs maintained under constant conditions, the presence of an endogenous rhythm in larval release is indicated by rhythmic releases of larvae by a population of crabs within a specific time interval on successive days at times related to the ambient light:dark or tidal cycles.

For R. harrisii, females from an estuary lacking tides have a circadian rhythm in larval release in that under constant conditions larvae are released by individual females in about the 2-3-h interval after sunset in the field (Forward et al., 1982; Fig. la). The rhythm can be entrained by the light:dark cycle, and release at night reduces visual predation on larvae and exposure to high water temperatures. Under constant conditions, females from an estuary with semidiurnal tides begin releasing larvae around the time of high tide and continue for about the next 2 h (Forward et at., 1982; Fig. lb). The rhythm can be entrained by tidal cycles in salinity (Forward et al., 1986) and hydrostatic pressure (Forward and Bourla, 2008). This timing pattern is typical for subtidal crustaceans in tidal areas (Forward, 1987a; Morgan, 1995). Larval release at the time of high tide favors seaward transport and dispersal of larvae during the subsequent ebb tide, effects that are useful for species that undergo development in coastal and offshore areas (Morgan, 1995). However, since R. harrisii zoeae are retained in estuaries near the adult habitats (Sandifer, 1973, 1975; Cronin, 1982; Goncalves et al., 1995a), release at high tide probably functions to avoid stressful low-salinity water.

[FIGURE 1 OMITTED]

Evidence for phenotypic flexibility in rhythms in larval release is indicated by transplantation experiments. Ovigerous R. harrisii with immature embryos can be transplanted from nontidal to tidal conditions and vice versa, and the rhythm (circadian or circatidal) in larval release changes to that of crabs in the new estuary (Forward et al., 1982). This change occurs quickly because the site of rhythmicity is in the developing embryos not the female (Forward and Lohmann, 1983). The experimental evidence is (hat under constant conditions detached eggs hatch at the same time as the female releases larvae. This situation is characteristic of subtidal crustaceans and has been observed in other species (Neopanope sayi, De Vries and Forward, 1991; Emerita talpoida, Ziegler and Forward, 2005).

At the time of egg hatching, embryos release a peptide pheromone cue (Rittschof et at., 1985) that induces stereotypic larval release behavior by the female, in which she vigorously pumps her abdomen to break open remaining eggs. Thus the embryos dictate the time of hatching, but the female is responsible for the synchronous release of larvae. In contrast, the control of the timing of larval release shifts to the female in intertidal and supratidal species (e.g., De Vries and Forward, 1991; Morgan, 1995), probably because the embryos cannot determine when a suitable release site will be located by a female (Christopher et al., 2008).

The peptides that are released from the embryos are dipeptides and tripeptides, which have a neutral amino acid at the amino terminus (e.g., glycine) and a basic amino acid (e.g., arginine) at the carboxyl terminus (Forward et al., 1987; Rittschof et al., 1989, 1990; Pettis et al., 1993). Interestingly, once these peptides were identified in larval release of R. harrisii, similar peptides were found to participate in larval release of other crabs (De Vries et al., 1991), and in other crustacean and mollusc behaviors (reviews by Browne et al., 1998; Rittschof and Cohen, 2004) such as settlement of barnacle (Tegtmeyer and Rittschof, 1989) and oyster larvae (Zimmer-Faust and Tamburri, 1994), and attraction of hermit crabs to gastropod predation sites (e.g., Pettis 1991; Rittschof, 1993).

Retention of Larvae in Estuaries and Vertical Migration

Once released into the water column in estuaries with semidiurnal tides, the larvae are unusual in that they are retained in low-salinity areas of estuaries (Sandifer, 1973, 1975; Cronin, 1982; Lampert and Epifanio, 1982) and are not exported out of the estuary for development offshore as observed for many other species of crabs (Epifanio and Garvine, 2001). The mechanism for retention is that zoeae vertically migrate around the depth of no net horizontal motion of water. Migration is timed relative to tides as larvae ascend during flood tide and descend during ebb tide (Cronin, 1982). This migration pattern is typical for retention in estuaries and is observed for copepods, mysids, and fish larvae (reviewed by Forward and Tankersley, 2001). Models indicate that horizontal transport is reduced because during ebb and flood tides animals migrate to the depth where horizontal currents are the weakest (e.g., Chen et al., 1997). The underlying behavior for R. harrisii zoeae is a circatidal rhythm in vertical migration that is observed in larvae collected in the field (Cronin and Forward, 1979) and larvae released in the laboratory (Cronin and Forward, 1983, 1986). Further studies demonstrated that the vertical migration rhythm was based upon a circatidal rhythm in swimming activity, in which zoeae are active during the time of rising tide and inactive during the time of ebb tides (Forward and Cronin, 1980). A similar rhythm in vertical migration is observed in fiddler crab postlarvae (Tankersley and Forward, 1994) during flood-tide transport up estuaries to adult habitats and in postlarval shrimp (Hughes, 1972).

Their retention in estuaries suggests that larvae should be very tolerant to salinity and temperature. Accordingly, studies show that they can develop to the first crab stage in salinities from 2.5 to 40 ppt and temperatures of 15-35 [degrees]C (Costlow et&L, 1966; Costlow and Bookhout, 1971; Christensen and Costlow, 1975; Rosenberg and Costlow, 1979; Morgan, 1987a; Laughlin, 1989; Laughlin and French, 1989a, b). However, the optimum conditions for development are a salinity of 15-20 ppt and a temperature of 20-25 [degrees]C (Christensen and Costlow, 1975; Goncalves et el., 1995b). Successful development in salinities from 2.5 to 40 ppt is unusual for crustacean larvae. For example, larvae of the crabs Sesarma cinereum (Costlow et al., 1960) and Panopeus herbstii (Costlow et al., 1962), both of which occur in higher salinity areas in estuaries, can only complete development at salinities above about 20 ppt. Development at low salinities by R. harrisii suggests that zoeae must be very good at osmoregulation. Accordingly, Kalber and Costlow (1966) found that zoeae regulate their hemolymph hyperosmotically to external salinities below 30 ppt and are isosmotic or slightly hypoosmotie at higher salinities. Interestingly, adults show a similar osmotic relationship to external salinity and are very good hyperosmotic regulators at low salinities (Diamond et al., 1989; Reisser and Forward, 1991). which is common among crustaceans that inhabit low-salinity areas (Pequeux, 1995).

In addition, superimposed upon the tidal vertical migration pattern is a nocturnal diel vertical migration (DVM), in which zoeae are higher in the water column during the night and lower during the day (Forward et al, 1984; Cronin and Forward, 1986). The migration pattern conforms to the isolume, or preferendum, hypothesis because larvae are ascending and descending with a particular light intensity that is close to the threshold light intensity for phototaxis (2.5 X [10.sub.11] photons [m.sub.-2] [s.sub.-1]). Although the isolume hypothesis for DVM of zooplankton was proposed almost a century ago (Ewald, 1910; Rose, 1925; Russell, 1927), field evidence is rare. Recent studies show that the day depth of zooplankton can be associated with an isolume (reviewed by Cohen and Forward, 2009) and zooplankton can change their day depth with changes in the depth of isolumes (e.g., Frank and Widder, 2002). However, observations that zooplankton actually vertically migrate with an isolume are confined to studies of migrations of sonic scattering layers (Boden and Kampa, 1967), of krill (Onsrun and Kaartvedt, 1988), and of R. harrisii zoea (Forward et al., 1984; Cronin and Forward, 1986).

Since changes of light intensity at sunrise and sunset are agreed to be the most important environmental factors involved in DVM (Forward, 1988), it is of interest to consider the photobiology and photobehavior of R. harrisii, which has a typical crustacean compound eye. Microspectrophotometric measurements indicate that adults have a visual pigment with an absorption maximum at 495 nm (Cronin and Forward, 1988). Studies of phototaxis (Forward and Costlow. 1974; Forward and Cronin, 1979) and polarotaxis (Via and Forward, 1975) indicate that all zoeal stages have a major response spectrum and action spectrum maximum at about 500 nm, with a minor peak at about 420 nm (Fig. 2). Short wavelength pigments are sometimes not seen in microspectrophotometry because they only occur in the eighth retinular cell. Thus, there is probably no ontogenetic change in visual pigments in R. harrisii, which is typical for crustaceans.

[FIGURE 2 OMITTED]

The spectral sensitivity of zooplankton undergoing DVM is predicted to agree with the sensitivity hypothesis (Forward, 1988), which states that the spectral position of visual sensitivity is matched to the spectral distribution of light in an animal's environment (Munz, 1958). Thus, zooplankton should be maximally sensitive to the most abundant light in their underwater environment. During the day in estuaries most of the light is in the yellow-red region at wavelengths above about 570 nm (Forward et al., 1988; Fig. 2). The extreme mismatch between the spectral sensitivity of R. harrisii zoeae (major peak at 500 nm) and their daytime underwater spectrum (>570 nm) led to the hypothesis that zooplankton are adapted to the spectrum underwater at the time of actual vertical migration (Forward et at., 1988). At twilight in air, the available spectrum changes dramatically due to the Chappuis effect, from a relatively constant level of photons from about 450 to 700 nm during the day to having peaks in the blue-green (450-530 nm) and red regions with a suppression from about 540 to 640 nm (see Forward et al., 1988). Since the underwater spectrum at twilight matches the spectrum in air regardless of water type, the spectral sensitivity of R. harrisii is, in fact, matched to the spectrum in its environment at the time of vertical migration. Interestingly, all other species of zoo-plankton have the same major spectral sensitivity maximum around 500 nm (Cronin and Forward, 1988; Forward, 1988; Cohen and Forward, 2009), and in fishes the visual pigments that are used for dim light vision (scotopic pigment) are also around 500 nm (e.g., Munz and McFarland, 1973; Hobson et al., 1981; Crescitelli et al., 1985).

When tested in a typical narrow trough, all zoeal stages of R. harrisii show a positive phototaxis to high light intensity and a negative phototaxis to low intensities (Forward. 1974; Forward and Costlow. 1974). The level of phototaxis varies with feeding: Stage I zoeae become more positive and less negative after starvation for 1 day (Cronin and Forward, 1980). and Stage II zoeae have increased positive phototaxis upon starvation but the negative phototaxis is not altered. Although Stages III and IV zoeae do not change phototaetic responses after 1 day of starvation, this is probably because they have greater energy reserves. An increased positive phototaxis is hypothesized to move larvae higher in the water column during the day, where more food is potentially available (Cronin and Forward. 1980).

Although the pattern of phototaxis to high- and low-intensity light is the reverse of that in most zooplankton (Forward, 1988), it is typical of all crab (Herrnkind, 1968; Forward, 1977, 1987b) and some fish larvae (Blaxter, 1968, 1969; Champalbert et al., 1991; Burke et al., 1996) when tested in a narrow light field. For R. harrisii, this pattern predicts that zoeae should show a reverse DVM pattern and be at the surface during the day due to positive phototaxis and at depth during the night due to negative phototaxis to low light at sunset. This prediction does not agree with field studies indicating that zoeae show a nocturnal DVM pattern and are deep in the water column during the day (Forward et al., 1984). The explanation for this inconsistency is that when stimulated by a highly directional light source, larvae are exposed to a very narrow beam of light that causes a trapping effect (Reviewed by Verheijen, 1958), in which the larvae become fixated on the light and swim either directly toward or away from it. In contrast, the natural downwelling light held underwater consists of a cone of light from the sun and sky, which subtends an angle of about 48.6[degrees] (critical angle) from the vertical. This cone is normally referred to as Snell's window. Outside the cone, light intensity is low and consists of scatter and reflected light (e.g., Forward et al., 1984; Buchanan et at, 1982).

When retested in a light held that simulates the natural underwater angular light distribution (ALD) of down-welling light, R. harrisii larvae show only the negative phototaxis to low light intensity, which indicates that positive phototaxis is a laboratory artifact (Forward et al, 1984: Forward, 1986). R. harrisii larvae are not unique because a study of Stage I zoea of other crab species also found great differences between photoresponses in a narrow light field and in a simulated underwater light field (Forward and Buswell, 1989). These results indicate that caution should be used in extending the phototactic responses observed in a narrow light field to actual photoresponses in the field. In some cases the phototactic responses observed in a narrow light field are valid (e.g., Forward and Hettler, 1992), but they should be verified by tests in a situation that mimics the underwater ALD to determine whether they will actually occur underwater.

The photoresponses underlying the ascent and descent phases of nocturnal DVM of R. harrisii larvae are different. During the descent phase at sunrise, zoeae descend near the isolume for the threshold intensity for negative phototaxis (Forward et al., 1984). The behavior underlying movement with the isolume can perhaps serve as a model for how any zooplankter could migrate with a preferred isolume and remain near an isolume during the day. Since the isolume is the lowest light intensity that evokes a phototactic response, at depths below the isolume, zoeae are essentially in darkness. Zoeae show a negative geotaxis in darkness, in which they ascend. Upon ascending to a depth where light is above the threshold intensity, a negative phototaxis is initiated and they descend (Forward et al., 1984; Forward. 1985). Thus, zoeae oscillate around the isolume. as they descend at sunrise and remain at the depth of the isolume during the day. These results lead to the hypothesis that the one isolume that could be perceived by all zooplankton species and would be easiest to use for depth maintenance and vertical migration is the light level corresponding to the lower visual threshold (Forward, 1988). This threshold would vary with species, depending upon their visual system. The only test of this hypothesis with other species was a study of two copepod species by Buskey et al. (1989). Unfortunately, they found that the day depth of the copepods did not correspond to the threshold light intensity for phototaxis. Thus, the hypothesis remains to be tested on other crustacean larval species.

The alternative hypothesis for the way in which light is used during DVM is the rate of change hypothesis, which states that the cues for initiating vertical movements are the relative rate and direction of change in light intensity from the ambient level (adaptation intensity), which can vary over the day. This hypothesis applies to most zooplankton and is best studied in Daphnia species (reviewed by Ringelberg, 1999; Ringelberg and van Gool, 2003). R. harrisii larvae conform to this hypothesis during the ascent phase of nocturnal DVM (Forward, 1985). However, applying this hypothesis is complex because light can act as an orienting, controlling, and initiating cue during DVM (Bainbridge. 1961). Aspects of light that can be used for orientation include the angle of polarization, the light-dark contrast at the edge of the critical angle (Snell's window), and the direction of the highest light intensity. The latter is the most obvious because positive and negative phototaxis to directional light leads to ascents and descents, respectively. Unfortunately, for R. harrisii larvae, the orientation cue is not light but gravity, as they use a negative geotaxis for orientation upward at sunset (Forward, 1985). Nevertheless, light does control the ''readiness" of the larvae to ascend through the level of light adaptation. Readiness can be defined as an increase or decrease in responsiveness to light cues that induce vertical migration (Bainbridge, 1961). Upon adaptation to levels of light intensity at twilight, zoeae are maximally responsive to light cues that induce vertical movements. Adaptation to light intensities above and below twilight levels reduces responsiveness (Forward. 1985). This relationship is also seen in other marine zooplankton (e.g., Stearns and Forward, 1984; Forward and Hettler, 1992; Cohen and Forward, 2005b). Finally, the rate of decrease in light intensity initiates upward swimming. As has been shown in a number of studies (e.g., Forward, 1985; Ringelberg. 1964, 1991; Forward and Hettler, 1992; Cohen and Forward, 2005a, b), the relative rates of decrease in light intensity that evoke an ascent response correspond to rates observed at sunset (reviewed by Cohen and Forward, 2009).

An important recent advance in the study of DVM is the recognition that the behavior is a phenotypic response activated by chemical cues (kairomones) from predatory fishes (reviewed by Cohen and Forward, 2009). A laboratory approach for documenting predator-induced phenotypic plasticity in DVM is to observe the behavior of zoo-plankton to light cues that are involved in DVM in the presence of odor cues from fish (e.g., Ringelberg, 1991). This approach indicates that zooplankton are not responding directly to kairomones from predators but rather that their behavioral responses to light are modified by the chemical cues.

Among R. harrisii larvae, the descent at sunset would be used to avoid visual predatory fishes during the day. As described above, during the descent larvae move down with an isolume due to negative phototaxis (Forward, 1985). When exposed to fish kairomones, the lower threshold light intensity for negative phototaxis decreases (Forward and Rittschof, 2000: Fig. 3). Thus, larvae would descend earlier at sunrise when visual predators, such as fish, are present, thereby lowering their predation risk. The actual chemical cues are probably sulfated and acetylated amines in disac-charide degradation products from the external mucus of fish (Forward and Rittschof, 2000). Since fish produce mucus continuously, changes in the level of mucus degradation products serve as an indicator of fish abundance. Furthermore, the unique and unstable nature of modified amines of disaccharides are ideal signal molecules because they have a high signal-to-noise ratio in seawater and a short half life, and are associated with fishes (Rittschof and Cohen, 2004).

[FIGURE 3 OMITTED]

Although nocturnal DVM functions in avoidance of visual predators (Lampert 1989, 1993: Hays, 2003), retention in estuaries requires R. harrisii larvae to ascend on flood tides during the day and night. Ctenophores and coelentcr-ate medusae are voracious zooplankton predators in estuaries. They occur near the surface and do not pursue their prey, but rather catch zooplankton through their feeding currents. Even though these predators appear relatively transparent, they do attenuate light and cast downward shadows (Forward, 1976). Before the negative phototaxis to low light intensities of R. harrisii zoeae was identified as important for DVM, it was hypothesized to function during a predator-avoidance shadow response to escape from ctenophores and medusae during the day (Forward, 1974; Forward and Costlow, 1974). The shadow response occurs in both narrow light fields (Forward, 1976) and a light field that mimics the underwater ALD (Forward, 1986; Cohen and Forward. 2003). If a zoea is close to the surface and passes under a ctenophore, it will detect different levels of decrease in light intensity that induce different behavioral responses. Small decreases evoke a sinking response. Decreases to a light level that evokes a negative phototaxis induce a biphasic response, in which larvae first sink and then show a negative phototaxis. Finally, large decreases to darkness induce a sinking response (Forward, 1976).

Thus, larvae move down, away from dark objects above them, in the water column. At first these responses appear anomalous because upward movement at sunset also occurs in response to a decrease in light intensity. DVM and the shadow response are separated by the rate of decrease in light intensity. Rapid decreases evoke the shadow response, while the relatively slow rates of decrease at sunset induce the ascent response (Forward, 1985). In clean seawater the threshold amount of change necessary to induce a shadow response is equivalent to a 50% decrease in light intensity (Cohen and Forward, 2003), while the response saturates at a 90% decrease (Forward, 1976). Since an estuarine cteno-phore (Mnemiopsis leidyi) attenuates about 90% of the light, its shadow can be detected by crab larvae and induce downward movement due to sinking and negative photo-taxis away from an overhead predator. The negative photo-taxis to low light intensities is observed in other species of crab larvae (Herrnkind, 1968; Forward, 1977, 1987b), larvae of the shrimp Pa/aemonetes pugio (Wilson et al, 1985), and fish larvae (Blaxter, 1968, 1969; Champalbert et al., 1991; Burke et al., 1996), and some fish larvae descend upon exposure to a decrease in light intensity (Forward et al., 1996). which indicates that the shadow response is prevalent among different species of larvae. Alternatively, the negative phototaxis is not seen in estuarine copepods, which are readily consumed by ctenophores. Field studies indicate that copepod abundance is reduced in areas where estuarine ctenophores are abundant, whereas crab zoeae do not seem to be affected (e.g., Phillips et al., 1969; Burell and van Engel, 1976). For example, Deason and Smayda (1982) found that abundance of the copepod Acartia tonsa was rapidly reduced each summer in Narragansett Bay (RI) as the population of the ctenophore Mnemiopsis leidyi increased, and Deason (1982) estimated that during August, ctenophore predation removed a bay-wide mean of about 20% of the zooplankton standing stock each day.

Since the shadow response is used to avoid ctenophores, which release large amounts of mucus that is similar to the mucus of fishes, it was hypothesized that the external mucus from the ctenophore Mnemiopsis leidyi serves as a kairomone that increases the sensitivity of R. harrisii zoeae during the shadow response (Cohen and Forward, 2003). When exposed to clean seawater, the minimum decrease in light intensity to evoke the shadow response was 50%; however, in the presence of ctenophore odor water the threshold decrease was only 9% (Fig. 4). Curiously, fish mucus has the same effect. Further tests showed that components of the mucus, such as aminosugar disaccharide having acetylamine functionality, also reduce the threshold (Cohen and Forward, 2003). These results indicated that when ctenophores and fishes are abundant, R. harrisii larvae are more sensitive to rapid reductions in light intensity, and the shadow response will be more effective at predator avoidance. Thus, external mucus is used as a kairomone in both DVM and the shadow response.

[FIGURE 4 OMITTED]

In addition to the shadow response and DVM, the large spines on R. harrisii zoeae also function to deter predation by small fishes (Morgan. 1989). These spines have not evolved to stabilize larvae or retard sinking, but rather they increase the apparent size of zoeae and are noxious to small fish (Morgan, 1989). Field studies indicate that the feeding preferences of estuarine fishes in order of descending preference are copepods, crab larval species that have small spines and are exported from estuaries, and decapod larvae such as R. harrisii that have large spines and develop in estuaries (Morgan, 1990). Similarly, laboratory studies found that estuarine fishes preferentially feed on crab zoeae that are exported from estuaries rather than on R. harrisii zoeae (Morgan, 1987b).

Behavioral Responses to Temperature, Salinity, and Hydrostatic Pressure

If environmental gradients exist in the water column, then the changes that occur with increasing depth are a decrease in temperature and an increase in salinity and pressure. What is clear from the many studies of the behavioral responses of zooplankton is that they do not respond directly to these environmental factors, but rather that changes in these factors act as "releasers" for behavioral responses to light (phototaxis) and gravity (geotaxis) and for changes in activity. Ascents occur upon a positive phototaxis; negative geotaxis and activity increase with the opposite responses, resulting in a descent. As proposed by Sulkin (1984) for crab larvae, zooplankton have a negative feedback system associated with these environmental factors and behavioral responses. The general model is that exposures to environmental conditions that occur upon ascending (temperature increase, salinity decrease, and pressure decrease) induce downward movement due to negative phototaxis, positive geotaxis, and activity decrease. Zooplankton encountering the opposite changes in environmental factors upon descending will ascend due to a positive phototaxis, a negative geotaxis, and an activity increase. This negative feedback system functions for depth regulation and avoidance of adverse environmental conditions.

The negative feedback model for depth regulation was developed from studies using step changes in temperature, salinity, and hydrostatic pressure and from tests in vertical columns with sharp discontinuities in temperature and salinity. Studies with R. harrisii larvae agree with the model because step changes in environmental factors encountered upon descending--such as an increase in pressure (Wheeler and Epifanio, 1978; Forward and Wellins, 1989), a decrease in temperature (Ott and Forward, 1976), and an increase in salinity (Latz and Forward, 1977)--induce an ascent. In addition, R. harrisii zoeae show a dramatic increase in swimming speed, termed high barokinesis (Sutkin, 1984), upon a step pressure increase (Bentley and Sulkin, 1977; Forward and Wellins, 1989; Forward, 1990a), which is a common response among crustacean larvae (Sulkin, 1973, 1984). Alternatively, changes that occur upon ascending--such as a decrease in pressure (Wheeler and Epifanio, 1978; Forward and Wellins, 1989), an increase in temperature (Ott and Forward, 1976), and a decrease in salinity (Latz and Forward, 1977)--induce a descent. Regardless of whether vertical movement results from photolaxis, geotaxis, or an activity change, R. harrisii larvae ascend and descend as predicted by the negative feedback model.

The problem with step-change experiments is that zoea in the field encounter vertical gradients in environmental factors and less commonly experience sharp discontinuities. Thus, in the water column, zoeae perceive rates of changes in environmental factors that depend upon the magnitude of vertical gradients, speed of vertical movement, vertical currents, and density structures of the water column. Furthermore, for zoea to perceive a change in temperature, salinity, or pressure, the cue must change by a detectable rate and amount (Forward, 1989a). For R. harrisii, the threshold rate of salinity increase to evoke an ascent response is 1.1 X [10.sup.-3] ppt [s.sup.-1] for the first and last zoeal stages. Since these thresholds changed little with acclimation salinity, zoeae are responding to the change in salinity, not the acclimation salinity level. Nevertheless, salinity must also change by an absolute amount from the acclimation level for detection. The absolute amounts of change necessary for the response is 0.05-0.11 ppt for Stage I zoea and 0.21-0.29 ppt for Stage IV zoea (Forward, 1989a). The sinking speed of Stage I zoeae is 3.1 mm [s.sup.-1], while Stage IV zoeae sink faster, at 7.8 mm [s.sup.-1] at 25 [degrees]C and 20 ppt (Latz and Forward, 1977). Alternatively, the ascent speeds of Stages I and IV zoeae are 6.3 and 6.2 mm [s.sup.-1]. Considering larval sinking rates and the threshold for detection of a rate of salinity increase, Stage I zoeae would be able to detect salinity gradients of 0.35 ppt [m.sup.-1], and Stage IV zoeae could detect 0.14 ppt [m.sup.-1]. Both these gradients are common in estuaries (Forward, 1989a). A change in sodium chloride concentration is the primary cue signaling a salinity change (Harges and Forward, 1982).

When exposed to very slow rates of change in tempera-lure, as would occur in vertical gradients in estuaries, R. harrisii larvae were remarkably sensitive (Forward, 1990b). A temperature decrease evokes an ascent response in darkness, probably due to a negative geotaxis. The threshold rates for Stage I and IV zoeae were 1.0 X [10.sup.3] and 1.7 X [10.sup.-3] [degrees]C [s.sup.-1], respectively. The absolute amounts of temperature decrease before a response were 0.38 and 0.49 [degrees]C for Stage I and IV zoeae, respectively. Larvae descended in darkness upon a temperature increase, probably due to a positive geotaxis or an activity decrease. The threshold rates were 1.2 X [10.sup.-3] and 3.9 X [10.sup.-3] [degrees] C [s.sup.-1] for Stage 1 and IV zoea, respectively. Absolute amounts of increase at detection were 0.28 and 0.29 [degrees] C for Stage 1 and IV zoea. The minimum detectable gradients upon descending, based upon sinking speeds for Stage I and IV zoeae, ranged from 0.22 to 0.32 [degrees] C [m.sup.-1]; upon ascending, the minimum detectable gradients, based on swimming speeds, were 0.19 to 0.63 [degrees] C [m.sup.-1] (Forward, 1990b). These gradients are very small and are common in estuaries.

When exposed to different rates of increase in hydrostatic pressure, R. harrisii zoeae ascend. In darkness, rates of pressure increase at and above 0.175 mbar [s.sup.-1] induced an ascent response and high barokinesis in Stages I-III zoeae, while the same responses had a threshold of 1.19 mbar [s.sup.-1] for Stage IV zoea (Forward and Wellins. 1989). The absolute amount of change necessary for behavioral responses at the threshold rates of change varies with light intensity (see below). Because one millibar is equivalent to about 10 mm of water depth, rates of pressure change for a zoea depend upon ascent and descent speeds. Since Stage I zoeae have sinking and descent swimming speeds ranging from 2.96 to 3.65 mm [s.sup.-1] (Latz and Forward. 1977), they can perceive a pressure increase upon descending. For Stage IV zoeae, the sinking speed at 7.8 mm [s.sup.-1] is too slow for detection of a pressure increase; but downward swimming can reach 19.3 mm [s.sup.-1] (Latz and Forward, 1977), indicating that larvae can swim down fast enough for a response.

Upon ascending, the decrease in pressure induces a descent response due to positive geotaxis (Forward and Wellins, 1989). Since ascent swimming speeds of Stage I zoeae range from 1.85 to 10.9 mm [s.sup.-1], they can swim up fasl enough to exceed the threshold rale for detection of a decrease in pressure at 0.53 mbars [s.sup.-1]. A threshold rate of decrease in pressure was not found for Stage IV zoeae. However, Stage HI zoeae swim up at a rate ranging from 3.14 to 9.2 mm [s.sup.-1] and their threshold rate of decrease was 0.4 mbars [s.sup.-1], which shows that they can ascend fast enough for a response.

Collectively, these studies indicate that R. harrisii zoeae can ascend and descend fast enough to detect natural gradients in temperature, salinity, and pressure. The rates of change in these environmental factors induce behavioral responses that are consistent with the negative feedback model (Sulkin, 1984). Thus, studies using step changes in environmental factors will not indicate the sensory thresholds for detection or the minimum gradients that can be perceived, but they will indicate the behavioral responses involved in the negative feedback system for depth regulation.

Since Latz and Forward (1977) found that changes in phototactic responses upon step changes in salinity lasted less than 5 min, environmental factors must change for a zoea to respond behaviorally. This implies that for larvae to stay near a particular depth and detect pressure increases and decreases, they must descend and ascend, respectively. This observation leads to the concept of the depth regulatory window based upon responses to pressure change as zoeae move vertically. For R. harrisii, the dimensions of the window are defined by how far a larva (1) ascends before the response to a pressure decrease induces a descent response and (2) descends before the pressure increase induces an ascent response. These distances identify the absolute amount of pressure change that must occur before an ascent or descent response occurs. Remarkably, the dimensions of the window depend upon the level of light adaptation when tested in a light system that simulates the natural ALD (Forward, 1989b). When Stage I and TV zoeae were in darkness or at the threshold light intensity (2.5 X [10.sup.-3] photons [m.sub.-2] [s.sup.-1]) for negative phototaxis, the distance larvae descended before responding to a pressure increase was much shorter than the distance they would ascend before responding to a pressure decrease. When adapted to a middle light intensity level (2.8 X [10.sup.-3] photons [m.sup.-1] [s.sup.-1]), both zoeal stages descended and ascended approximately equal distances before responding. Finally, at the highest light level tested (2.8 X [10.sup.15] photons [m.sup.-2] [s.sup.-1]), the ascent distance was much shorter than the descent distance (Forward, 1989b). These results predict an ascent in the water column when adapted to low light intensities and descent when adapted to high light intensities due to responses to hydrostatic pressure. Interestingly, light adaptation intensity serves as a controlling cue for both depth regulation and the photoresponses involved in DVM. Thus, Sulkin's (1984) negative feedback model provides the general mechanism of depth regulation. The effects of light adaptation on the limits of the depth regulatory window provide an additional component that allows depth regulation throughout the water column and not just at an absolute depth.

Metamorphosis

Cues that accelerate or delay the time that megalopae take to metamorphosis to the first crab stage have been studied in many coastal and estuarine crab species (reviewed by Forward et al., 2001). The generalities are that chemical cues from adult habitat substrates, aquatic vegetation, biofilms, conspecific odor, estuarine water, humic acids, and prey odor accelerate metamorphosis by reducing the time to metamorphosis. Alternatively, cues that delay metamorphosis are adverse environmental conditions such as hypoxia and ammonia/ammonium and chemical cues from predators, while neutral cues are clean structural material and chemical cues from some other species.

With the exception of R. harrisii, all brachyuran crab species that have been studied have larvae that develop in coastal and offshore areas away from the adult population and return to the estuary or coastal areas for metamorphosis to a benthic first crab. Nevertheless, R. harrisii shows similar responses to cues for metamorphosis (Fitzgerald et al., 1998). The time to metamorphosis is reduced by exposure to estuarine water, adult odor, and high salinity. It is lengthened by exposure to offshore water and low salinity. Since larvae are retained in estuaries but occur in many estuaries, this flexibility allows R. harrisii to delay metamorphosis until megalopae encounter a suitable area in the parent estuary and to populate new estuaries.

Toxicology Studies

R. harrisii larvae have been used for a variety of toxicology studies to identify lethal and sublethal concentrations. The attributes of R. harrisii for these studies are that (1) the larvae are easy to rear in the laboratory with low mortality; (2) they are robust and can complete development in a wide range of temperatures and salinities; and (3) since they are retained in estuaries, they would be exposed to land runoff that could contain pesticides, herbicides, and other potential toxicants. Effects on mortality and time for development have determined [LC.sub.50] levels under different temperature and salinity combinations, while sublethal effects have considered changes in swimming speed, phototaxis, and respiration. The intent of these studies was to identify concentration levels above which aquatic organisms would be adversely affected. The specific test chemicals are shown in Table 1 and include insect growth regulators (Forward and Costlow, 1976, 1978; Payen and Costlow, 1977; Chris-tensen et al, 1977a, b, 1978, 1984; Clare et al., 1992; Celestial and McKenney, 1994; Nates-Sergio and McKen-ney, 2000; Cripe et al, 2003; Tuberty and McKenney, 2005; McKenney, 2005); the herbicide Alachlor (Takacs et al, 1988); the pesticides Methoxychlor (Bookhout et al., 1976), Kepone (Bookhout et al, 1980), and Mirex (Bookhout et al, 1972); components of drilling fluids (Bookhout et al, 1984a, b); polycylic aromatic hydrocarbons (Laughlin and Neff, 1979a, b, 1980, 1981; Laughlin et al., 1981); fuel oil (Laughlin et al., 1978); tributyltin/dibutylin compounds (Laughlin, 1983; Laughlin et al., 1983, 1984; Laughlin and French, 1989c); copper (Sanders and Jenkins, 1984); cadmium (Rosenberg and Costlow, 1976); and mercury (McKenney and Costlow, 1982).
Table 1
Toxicology studies

Test Compounds                        References

Insect Growth Regulators

  MON-0585 Altosid[R] ZR-515  Forward and Costlow, 1976

  MON-0585 Altosid[R] ZR-515  Payen and Costlow, 1977; Forward and
                              Costlow, 1978; Christiensen et al.,
                              1977a; Celestral and McKenney, 1994;
                              McKenney. 2005

  Altozar[R]ZR-512            Forward and Costlow, 1978; Christiensen
                              et al., 1977b

  Dimilin[R] TH-6040          Forward and Costlow, 1978; Christiensen et
                              al., 1978; Christiensen et al., 1984

  Fenoxycarb[R]               Nates-Sergio and McKenney, 2000; Cripe et
                              al., 2003;

  Pyriproxyfen[R]             Tuberty and McKenney, 2005; McKenney, 2005

  RH-5849                     Tuberty and McKenney, 2005; cKenney, 2005;
                              Clare et al., 1992

Herbicide

  Alachlor[R]                 Takac et ai, 1988

Pesticides

  Mirex                       Bookhout et al., 972

  Methoxychlor                Bookhout et al, 1976

  Kepone                      Bookhout et al., 1980

Drilling Fluids

  Soluble factors             Bookhout et al., 1984a

  Hexavalent Chromium         Bookhout et al., 1984b

Polyaromatic Hydrocarbons

  Phenanthrene                Laughlin and Neff, 1979a; Laughlin and
                              Neff, 1980

  Naphthalene                 Laughlin and Neff, 1979a; Laughlin and
                              Neff, 1979b; Laughlin and Neff, 1981

  Jet fuel (JP5)              Laughlin et al., 1981

  Fuel oil                    Laughlin et al., 1978

Metals

  Mercury                     McKenney and Costlow, 1982

  Cadmium                     Rosenberg and Costlow, 1976

  Copper                      Sanders and Jenkens, 1984

  Tributyltin                 Laughlin, 1983; Laughlin et al., 1983;
                              Laughlin et al., 1984; Laughlin and
                              French, 1989c

  Dibutyltin                  Laughlin and French, 1989c


Summary and Conclusions

Characteristics of Rhithropanopeus harrisii larvae are summarized in Table 2. Since adults occur in low-salinity areas of estuaries and zoeae are retained in these areas, it is informative to separate larval characteristics into those that are related to the larval habitat and those that are common. to other crab larval species. Since zoeae are retained in estuaries, they develop in a highly variable environment. Accordingly, they can complete development in a very wide range of temperatures and salinities, even though the optimum is 20-25 [degrees]C and 15-20 ppt. They are retained in low-salinity areas of estuaries by a tidal rhythm in vertical migration. As is characteristic of crabs that occur in low-salinity areas, they arc very good at hyperosmotic regulation of their blood osmolality. Their spines are much longer than those of crab species that develop in coastal and offshore areas and are used to deter predators such as small estuarine fishes.
Table 2
characteristics of Rhithronanopeus harrisii larvae

Larval aspects        Characteristics        References

Development of Stage  --Temperature range    e.g., Costlow et al.,
I zoea to first crab  15-35 [degrees]C       1966
stage

                      --Salinityrange
                      2.5-40 ppt

Optimum conditions    --Temperature 20-25    Christiensen and
for development       [degrees]C --Salinity  Costlow.1975:Goncalveset
                      20 ppt                 al.,1995b

                      --Salinity 20 ppt

                      --Duration Stage I
                      zoea to First crab
                      stage = 12-15 day
                      at optimum
                      temperature and
                      salinity

Osmoregulation        Hyperosmotic below 30  Kalber and Costlow. 1966:
                      ppt and isomotic or    Reisser and Forward.
                      slightly ypoosmotic    1991
                      above 30 ppt for all
                      zoeal stages,
                      megalopae. and
                      adults

Characteristics in    --Mean Depth Stage J   Cronin. 1982
the water column      zoea = 1.8 m Stage IV
                      zoea = 2.06 m

                      --Estuarine retention  Cronin and Forward, 1979
                      due to tidal vertical
                      migration in all
                      zoeal stages

Swimming speeds       --Stage I zoea = 2-9   Latz and Forward. 1977
                      mm [s.sup.-1]

                      --Stage IV zoea =
                      4-13 mm [s.sup.-1]

Environmental cues    --Light                Forward and Costlow, 1974
that can be detected                         Ott and Forward, 1976;

                      --Temperature          Forward, 1990b

                      --Salinity             Latz and Forward, 1977;
                                             Forward, 1989a

                      --Hydrostatic          Wheeler and Epifanio,
                      pressure               1978; Forward and Wellins,
                                             1989

Predator avoidance    --Shadow response      Forward, 1976 Morgan,
mechanisms                                   1987b, 1989. 1990

                      --Spines               Forward et al., 1984;
                                             Forward, 1985

                      --Nocturnal diurnal
                      vertical migration

Vision                --Spectral             Forward and Costlow,
                      sensitivity maxima =   1974; Cronin and Forward.
                      420 nm and 500 nm      1988


                      --Light intensity      Forward et al., 1984
                      threshold = 2.5 x
                      [10.sup.11] photons
                      [m.sup.-2] [s.sup.-1]


Considering crab larvae in general, the swimming and sinking speeds of R. harrisii are equivalent to those of other species. These speeds are adequate for them to detect natural vertical gradients in temperature, salinity, and hydrostatic pressure in estuarine areas, which they use for the negative feedback systems for depth regulation and avoidance of adverse environmental conditions. Nocturnal diel vertical migration (DVM) is the most common vertical migration pattern of zooplankton and functions to reduce exposure to visual predators during the day. The shadow response is also common among crab and fish larvae and functions to reduce exposure to zooplankton predators, such as ctenophores and coelen-terates, that float near the surface. Both DVM and the shadow response indicate that the compound eyes of larvae are important for predator avoidance. Accordingly, both photoresponses are enhanced by exposure to breakdown products of mucus from zooplankton predators such as fishes and ctenophores. The absorption maximum of their primary visual pigments (500 nm) is not adapted to light underwater in an estuary during the day but does match the spectrum at twilight, which is characteristic of vertically migrating zooplankton in all types of water. The threshold light intensity for phototaxis is similar to values for other crab larvae and zooplankton {Forward. 1988). Thus, R. harrisii larvae have some unique characteristics that allow them to successfully populate low-salinity areas of estuaries, but they also have characteristics that generalize to estuarine and coastal species.

Acknowledgments

I thank Dr. Jonathan Cohen for his critical comments on the manuscript.

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RICHARD B. FORWARD, JR.

Duke University Marine Laboratory, Nicholas School of the Environment, 135 Duke Marine Lab Road, Beaufort, North Carolina 28516

Received 6 October 2008; accepted 17 February 2009.

E-mail: rforward@duke.edu

Abbreviations: ALD, angular light distribution; DVM, diel vertical migration.
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