Behavioral adaptations in larvae of brachyuran crabs: A review

Journal of Experimental Marine Biology and Ecology 482 (2016) 85–105

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Behavioral adaptations in larvae of brachyuran crabs: A review Charles E. Epifanio ⁎, Jonathan H. Cohen School of Marine Science and Policy, University of Delaware, 700 Pilottown Road, Lewes, DE 19958, USA

a r t i c l e

i n f o

Article history: Received 5 May 2016 Received in revised form 17 May 2016 Accepted 18 May 2016 Available online xxxx Keywords: Brachyuran Crab Larvae Swimming Behavior

a b s t r a c t Larval development in brachyuran crabs includes a number of zoeal stages followed by a single megalopal stage. Zoeae and megalopae are relatively strong swimmers, and movement up or down in the water column takes advantage of vertical shear in ambient currents with consequent transport in the horizontal dimension. For some species, this process is important in controlling the dispersal of early-stage larvae away from spawning sites and in maintaining the supply of late-stage larvae to juvenile nursery habitat. For other species it enables retention near spawning sites throughout the larval period. Vertical position in the water column also modulates predator-prey interactions, which impact growth and survival of larvae. Swimming behavior in larval crabs is regulated by both external cues detected in the water column and endogenous rhythms entrained by external oscillators. Gravity, hydrostatic pressure, and light are the primary external cues because of their predictability in the environment. Light is also the most common external oscillator entraining swimming rhythms. Secondary cues include salinity, temperature, turbulent kinetic energy, and feeding state. Crab larvae also respond to chemical and tactile cues that facilitate settlement in juvenile habitat. This paper presents a review of the physical and chemical characteristics of these cues, the behavioral responses of crab larvae to the cues, and the patterns of larval transport that emanate from these responses. © 2016 Elsevier B.V. All rights reserved.

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Larval responses to external cues . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. General aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Nature and detection of gravity, hydrostatic pressure, and light . . . . . . . . 2.2.1. Gravity and hydrostatic pressure . . . . . . . . . . . . . . . . . 2.2.2. Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Generalized effects of gravity, hydrostatic pressure, and light on larval behavior 2.4. Specific effects of gravity, hydrostatic pressure and light on larval behavior . . 2.4.1. Xanthid and panopeid crabs . . . . . . . . . . . . . . . . . . . 2.4.2. Other focal species . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Effects of salinity and temperature on larval behavior . . . . . . . . . . . . 2.5.1. General aspects . . . . . . . . . . . . . . . . . . . . . . . . . 2.5.2. Discontinuities in salinity and temperature . . . . . . . . . . . . . 2.5.3. Small changes in magnitude . . . . . . . . . . . . . . . . . . . Role of larval behavior in transport . . . . . . . . . . . . . . . . . . . . . . . . 3.1. General aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Horizontal currents. . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Effects of behavior on larval transport . . . . . . . . . . . . . . . . . . . 3.3.1. Mud crabs in the family Panopeidae . . . . . . . . . . . . . . . . 3.3.2. Blue crabs. . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3. Fiddler crabs . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.4. Dungeness crabs . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.5. Shore crabs . . . . . . . . . . . . . . . . . . . . . . . . . . .

⁎ Corresponding author. E-mail address: [email protected] (C.E. Epifanio).

http://dx.doi.org/10.1016/j.jembe.2016.05.006 0022-0981/© 2016 Elsevier B.V. All rights reserved.

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3.4. Transport models . . . . . . . . . . . . . . . . . . . . . Responses to chemical and tactile cues for settlement. . . . . . . . 4.1. General aspects. . . . . . . . . . . . . . . . . . . . . . 4.2. Concept of competency . . . . . . . . . . . . . . . . . . 4.3. Examples of responses to chemical cues in brachyuran larvae . 4.3.1. Blue crabs . . . . . . . . . . . . . . . . . . . . 4.3.2. Mud crabs . . . . . . . . . . . . . . . . . . . . 4.3.3. Fiddler crabs . . . . . . . . . . . . . . . . . . . 4.3.4. Asian shore crab . . . . . . . . . . . . . . . . . 4.3.5. Miscellaneous taxa . . . . . . . . . . . . . . . . 5. Summary and conclusions . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.

1. Introduction Studies of swimming behavior in brachyuran crab larvae date back to the second half of the 20th century, and the total repertoire of papers is extensive. Larval development in crabs usually occurs within the plankton and includes a number of zoeal stages followed by a single megalopal stage (Fig. 1). Zoeae and megalopae are relatively strong swimmers, and movement up or down in the water column takes advantage of vertical shear in ambient currents with consequent transport in the horizontal dimension (Forward et al., 2003a). This process is important in controlling dispersal of early-stage larvae away from spawning sites and in maintaining the supply of late-stage larvae to juvenile nursery habitat (Queiroga and Blanton, 2005). Vertical position in the water column also modulates predator-prey interactions, which impact growth and survival of larvae (Cohen and Forward, 2009). Swimming behavior in larval crabs is regulated by external cues detected in the water column. Gravity, hydrostatic pressure, and light, are the primary cues and interact with a suite of secondary cues with consequent effect on behavior (Naylor, 2006). Crab larvae also respond to chemical and tactile cues that facilitate settlement and metamorphosis in juvenile

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habitat (Forward et al., 2001). Continuing interest in the behavior of crab larvae stems from a growing appreciation of the role of larval recruitment in practical issues such as: inter-annual variation in fishery yields (Ogburn et al., 2012); invasion of alien habitat by non-indigenous species (Tilburg et al., 2011); and response of ecosystems to climate change (Steneck and Wahle, 2013). In the following sections of this review, orientation and swimming responses of decapod larvae to physical cues in the water column are discussed in detail. In some cases, a brief tutorial is provided concerning the characteristics and distribution of cues and the ways in which larvae perceive them. In an additional section, the role of swimming behavior in modulating dispersal is reviewed, along with the effects of behavioral parameters on the outcomes of model simulations of larval transport. This is followed by a section that concerns the chemical and tactile cues associated with appropriate juvenile habitat. A final section provides an integrative summary and conclusions. 2. Larval responses to external cues 2.1. General aspects Locomotory behavior in brachyuran crab larvae mediates vertical distribution and predator-prey interactions, among other processes, and is commonly regulated by external (exogenous) cues detected in the water column. Such cues are most valuable when they are predictable and constant within the environment. Accordingly, gravity, hydrostatic pressure, and light are the three central external cues affecting larval behavior (see reviews by Thorson, 1964; Forward, 1976, 1988; Naylor, 2006; Cohen and Forward, 2009). These cues are reviewed here, both in terms of the physical nature of the cue in the water column and the morphology/physiology of the sensory structures detecting them. This discussion provides a conceptual framework for understanding the studies that have been done on behavioral responses to gravity, hydrostatic pressure, and light in larvae of brachyuran crabs. The section concludes with an analogous discussion of the responses of brachyuran larvae to variation in salinity and temperature in both the horizontal and vertical dimensions. 2.2. Nature and detection of gravity, hydrostatic pressure, and light

Fig. 1. Examples of the external anatomy of the larval stages of a typical brachyuran crab. (A) Early zoeal stage. (B) Advanced zoeal stage. (C) Megalopal stage. Modified from Costlow and Bookhout, 1959.

2.2.1. Gravity and hydrostatic pressure For a larva in the water column, the gravitational field is uniform across depth with acceleration toward the center of the Earth. In contrast, hydrostatic pressure exists as a gradient that increases with depth as a function of water column mass. Both are highly predictable stimuli detected in brachyurans by a statocyst organ, which functions in providing feedback to motor systems in order to maintain equilibrium. The statocyst also stabilizes the body (appendages, eyes, etc.) and monitors angular acceleration (Fraser and Macdonald, 1994; Fraser, 2001; Fraser et al., 2004). In brachyurans, statocysts are tube-like

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Fig. 2. Structures for detecting gravity and light in brachyuran larvae. (A) Statocyst, drawn from adult portunid crab Scylla serrata showing fluid flow during anticlockwise rotation about the vertical axis. Modified from Sandeman and Okajima (1972). (B, C) Embryo of panopeid crab Rhithropanopeus harrisii approximately 3 days pre-hatch (B) and stage IV zoeal larva (C). Compound eye is denoted by white arrows. (D) Semi-thin section of R. harrisii apposition compound eye. Scale bar is 10 μm. Modified from Charpentier and Cohen (2015).

structures that develop from the dorsal inner wall of the antennule basilar joint (Sekiguchi and Terazawa, 1997). Structural details vary among species, with nearly all work having been done on adults. In general the brachyuran statocyst consists of a pair of orthogonal, semi-circular, fluid-filled canals with a row of long, thread hairs for detecting angular acceleration and hydrostatic pressure (Fig. 2A). These work in concert with a statolith, which is a particle accreted from sand grains, and has associated sensory hairs for detecting gravity and horizontal rotation (Sandeman and Okajima, 1972; Sekiguchi and Terazawa, 1997; Fraser, 2001; Fraser and Takahata, 2002). 2.2.2. Light While still predictable, the underwater light field is far more variable than either gravity or hydrostatic pressure. Light in aquatic habitats has been extensively reviewed elsewhere (Johnsen, 2012; Warrant and Johnsen, 2013; Cronin et al., 2014), but four important aspects of underwater light for understanding larval brachyuran behavior are introduced below. These are intensity, spectral composition, angular distribution, and polarization. Water molecules and dissolved/particulate constituents (e.g., dissolved organic matter, suspended sediment, and phytoplankton) affect these properties as part of the interaction between light and water. The intensity of the underwater light field decreases with depth as downwelling sunlight is attenuated through absorption and scattering. These processes are wavelength-dependent, resulting in a characteristic narrowing of spectral composition with depth and a peak transmittance of ~ 480 nm at mesopelagic depths in clear ocean water. Additionally, there is a “greening” of downwelling light with increasing proximity to land as the increased dissolved/

particulate constituents in the water column shift peak transmission of light to longer wavelengths. Superimposed on these wavelength distributions is a decrease in yellow wavelengths (540 to 640 nm) of downwelling light compared to those in blue and red regions of the spectrum. This is important for decapod larvae undergoing light-mediated diel vertical migration at twilight, when maximizing photon capture is adaptive (Forward and Cohen, 2010).1 The angular distribution of underwater light in shallow water is generally characterized by a skewed light field with higher intensity in the direction of the sun, which becomes more uniform and centered on the zenith as depth increases (Warrant and Johnsen, 2013). Recreating this light field is particularly critical for understanding larval behavior in the laboratory because highly directional light stimuli can result in artificial behavioral responses (see below; Forward et al., 1984; Forward, 1988). Finally, detection of linear polarization (i.e., scattering-produced alignment of electric vectors of light rays) is inherent to the visual system of brachyuran larvae (see below) and may have relevance to their behavior in two ways. First, in calm surface waters the atmospheric polarization pattern caused by sunlight interacting with water molecules in the air is visible to an animal looking at the sky and can be used as part of a sun-compass system to orient to shorelines (Goddard and Forward, 1 The term diel vertical migration is generally abbreviated as DVM and refers to diel variation in swimming activity that results in rhythmic changes in the vertical distribution of brachyuran larvae and other planktonic organisms. Light is the main exogenous cue for DVM (Forward, 1988) and may also function as an endogenous cue that entrains circadian rhythms in swimming behavior. The adaptive value of DVM is a matter of continuing debate, but there is consensus that the process functions, at least in part, as a predator-avoidance mechanism (Cohen and Forward, 2009).

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1991; Horvath and Varjú, 1995). Second, in water beneath the surface, horizontally polarized light created by downwelling sunlight interacting with water molecules also creates a visual cue for larvae (Via and Forward, 1975), and a mechanism that predators can use to improve contrast of larvae in the water column (Johnsen et al., 2011). In brachyuran larvae, light for vision is detected by a pair of apposition compound eyes (Fig. 2B, C), which in some cases can differ markedly in structure and function from the adult eye (reviewed in Cronin and Jinks, 2001). Apposition compound eyes contain repeated photoreceptor units, with each unit having a corneal lens and crystalline cone that focuses light onto a rhabdom with visual pigment (rhodopsin) contained in microvillar projections of retinular cells (Fig. 2D). Light absorbed by the visual pigment leads to the photochemical process of vision, and rhabdoms are optically isolated from one another by dense screening pigments that improve spatial resolution of the eye. This is accomplished by minimizing the mixing of photons between photoreceptor units (for discussion in comparison to other eye designs, see Land and Nilsson, 2012). Transparency is of paramount importance to brachyuran larvae and other planktonic organisms (Johnsen, 2014). This is evident in the condensed retina of apposition compound eyes in many larval crustaceans, where all light-absorbing pigment is located near the center of the compound eye, which makes the overall eye less conspicuous (Fig. 2C) (Cronin and Jinks, 2001). For an organism in an environmental light field, all wavelengths of light are not equal in their ability to evoke a visual response, and in turn, to influence light-mediated behavior. Rather, the spectral (wavelength) sensitivity of the eye describes the weight of each wavelength in light perception. Crustacean spectral sensitivity has been reviewed elsewhere (Forward, 1988; Marshall et al., 1999, 2003; Johnson et al., 2002; Cohen and Forward, 2009), and a recurring theme is that visual spectral sensitivity may be adaptive to facilitate light-mediated behaviors in a particular spectral habitat. Changes in spectral sensitivity between larval and adult stages occur in some brachyurans, such as the crab Bythograea thermydron which undergoes a major shift in habitat from pelagic to benthic at deep-sea hydrothermal vent sites in the deep ocean, and a concomitant eye reorganization including a shift in spectral sensitivity from a maximum absorbance (λmax) of 447 nm in zoeae, 479 nm in megalopae, and 489 nm in adults (Jinks et al., 2002). Such large ontogenetic changes in spectral sensitivity are uncommon in brachyurans (e.g., Cronin and Jinks, 2001; Marshall et al., 1999, 2003), despite changes in optical habitat. Spectral sensitivities of brachyuran larvae and adults are not necessarily matched to the daytime spectral quality of light in either the larval or adult habitat. Rather, values for λmax cluster in the blue/green region (460–530 nm), which has been interpreted as an adaptation of spectral sensitivity to maximize photon capture at twilight for both larvae and adults (Forward, 1988; Marshall et al., 1999, 2003; Cohen and Forward, 2009). 2.3. Generalized effects of gravity, hydrostatic pressure, and light on larval behavior Gravity, hydrostatic pressure, and light work in several ways to generate behaviors in brachyuran larvae, and these are reviewed here to provide a conceptual framework for understanding the behavioral studies that have been done on larval sensory adaptations. Specifically, light can serve a controlling, initiating, and/or orienting factor in larval behavior (Bainbridge, 1961). Control of a behavior refers to the light/ dark acclimation state of the organism's visual system, which influences the physiological ability to detect light stimuli. For example, exposure to daytime light levels induces morphological and physiological changes in the cells of the eye, thereby shifting the eye's sensitivity range to higher light levels (Douglass and Forward, 1989; Meyer-Rochow, 2001). This change in sensitivity then limits the light level at which a behavior will be evoked. Initiation of a behavior by light involves photo-stimuli directly triggering a behavior, and may involve the absolute light level or more commonly the relative magnitude or rate of change of

irradiance (Cohen and Forward, 2009). Orientation of a behavior, or guidance of behavioral movement, may or may not involve light, even if light has played a controlling or an initiating role. For example, movement of a larva may be initiated by light or another factor, after which the larva may display directed swimming towards (positive phototaxis) or away from (negative phototaxis) a light source, using the light gradient for directional information. Alternatively, the orientation component of light-induced swimming may result passively from nondirectional changes in speed (orthokinesis) or turning rate (klinokinesis), the magnitude of which will vary in a light gradient. For a negatively buoyant larva, increased speed or turning rate leads to ascent, while decreases in these swimming activities lead to descent. Another possibility is that orientation may not involve light at all, but instead be a directional response to another exogenous cue, such as gravity. Thus, a larva could be orienting upwards in the water column using gravity (negative geotaxis) or likewise be descending using gravity (positive geotaxis). In yet another scenario, initiation and orientation could solely involve hydrostatic pressure cues if larvae regulate depth by kinetic responses (barokinesis) that vary along a hydrostatic-pressure (i.e., depth) gradient. For example, in negatively buoyant larvae, ascent could be caused by increased swimming activity associated with rising hydrostatic pressure (high barokinesis), with descent initiated by decreased activity accompanying a fall in hydrostatic pressure (low barokinesis). Complete reviews of terminology associated with orientation to external cues are provided elsewhere (Fraenkel and Gunn, 1961; Campan, 1997). Importantly, and as will be discussed in detail below, the “primary” responses to light, gravity, and hydrostatic pressure (control, initiation, orientation) are all subject to the influence of “secondary” factors such as temperature, salinity, predator odor, etc. (Ringelberg, 1995). Finally, care must be taken in comparing laboratory studies of larval swimming behavior in response to light, gravity, and hydrostatic pressure because experimental methods have varied over time, which has influenced the results obtained. Light in particular presents difficulties in terms of the light stimulus itself, as well as the apparatus used for experiments. Regarding the light stimulus, both the intensity and wavelength components must be quantified and controlled, and many larval brachyuran phototaxis studies have employed white light stimuli quantified in photometric units (e.g., lux) rather than in preferred radiometric units (e.g., photons cm−2 s−1, W m−2). This poses two problems. First, photometric units are difficult to relate to underwater light fields that are dynamic in both intensity and spectrum over space and time (Cohen and Forward, 2005). Second, the spectral emission of “white” light is highly dependent on the chosen lamp (quartz-halogen, incandescent, LED, etc.), which is problematic as the spectral sensitivity of brachyuran eyes is not equal across these wavelengths (see Section 2.2.2 above), nor is it necessarily identical among species or ontogenetic stages (Forward, 1988). Fortunately, many commercial light meters reading in radiometric units are now available, making it increasingly straightforward to quantify spectral irradiance, or the 400–700 nm integrated quantity of photosynthetically active radiation (PAR) (Johnsen, 2012, 2016). Regarding the apparatus used for behavioral experiments, many larval phototaxis studies have used narrow horizontal troughs with the light at one end to test for phototactic behavior (i.e., positive phototaxis is quantified as swimming toward the light source). While these experiments are straightforward to set-up, and are useful to isolate phototaxis from geotaxis, they pose a problem in that for brachyuran larvae (and for zooplankton in general) they introduce an artefactual positive phototaxis to high light intensities through a light trapping effect (reviewed in Forward, 1988). A solution to this problem is to test larval photoresponses in a relatively simple apparatus that simulates the underwater angular light distribution. In this configuration, larvae are in a test chamber surrounded by water, and light is presented from above, resulting in downwelling light forming an unobstructed Snell's window, with relative intensity being greatest for downwelling light,

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then for side-welling light, then for upwelling light (e.g., Forward et al., 1984; Ringelberg, 2010). Larval responses to hydrostatic pressure can be conducted in this light field to test for interactions between light and pressure stimuli (e.g., Forward and Buswell, 1989). Furthermore, such a configuration can be used to isolate light apart from gravity as an orienting cue during swimming if light is presented from below rather than from above (e.g., Forward, 1985). While a range of experimental approaches can be used to assess light, gravity, and hydrostatic pressure as cues for brachyuran larval behavior, the limitations of each must be appreciated, particularly when generalizing across studies.

2.4. Specific effects of gravity, hydrostatic pressure and light on larval behavior Looking broadly across brachyuran species, behavioral responses to light and gravity vary over ontogeny consistent with changing demands for horizontal transport and diel vertical migration. First-stage zoeal larvae of all species studied to date (Table 1) exhibit strong negative geotaxis, in line with uniformly shallow depth distributions (Forward et

Table 1 Ontogeny of larval brachyuran swimming responses to gravity and light stimuli tested in the laboratory. For gravity, arrows refer to negative (↑) and positive (↓) geotaxis. For light, arrows refer to negative (↓) and positive (↑) phototaxis when tested at low light intensities. Instances of no observed response (X) and no data collected (−) are also indicated. Phototaxis studies are grouped by whether they employed highly direction light in troughs (*) or simulated natural angular light distributions (†). References: a (Ott and Forward, 1976), b (Latz and Forward, 1977), c (Wheeler and Epifanio, 1978), d (Forward et al., 1984), e (Sulkin et al., 1980), f (Sulkin and Van Heukelem, 1982), g (Sulkin, 1975), h (Park et al., 2004), i (Cohen et al., 2015), j (Ichikawa et al., 2014), k (Bigford, 1977), l (Bigford, 1979), m (Jacoby, 1982), n (Kelly et al., 1982), o (Schembri, 1982), p (Sulkin et al., 1983), q (Arana and Sulkin, 1993), r (Forward and Costlow, 1974), s (Forward et al., 1984), t (Forward and Buswell, 1989), u (Tankersley et al., 1995), v (Forward, 1987b), w (Webley and Connolly, 2006). Cue

Species

Gravity Rhithropanopeus harrisii Callinectes sapidus Cataleptodius floridanus Hemigrapsus sanguineus Erimacrus isenbeckii Cancer irroratus Panopeus herbstii Metacarcinus magister Geryon quinquedens Ebalia tuberosa Eurypanopeus depressus Hemigrapsus oregonensis Light Rhithropanopeus harrisii Callinectes sapidus Cataleptodius floridanus Hemigrapsus sanguineus Metacarcinus magister Erimacrus isenbeckii Uca pugilator Uca pugnax Panopeus herbstii Armases cinereum Panopeus obesus Pilumnus sayi Sesarma reticulatum Neopanope sayi Cancer gracilis Lophopanopeus bellus bellus Hemigrapsus oregonensis Scyra acutifrons Scylla serrata Cancer irroratus

First zoea

Intermediate zoea

Megalopa Ref

↑ ↑ ↑ ↑ ↑ ↑ ↑ ↑ ↑ ↑ ↑ ↑

↑↓ ↑↓ ↑ ↑↓ ↓ ↑ ↑ ↑ ↓ − − −

X ↑ ↓ ↓ ↓ ↓ ↓ − − − − −

a,b,c,d e,f g h,i j k,l g m n o p q

↓ ↓ ↑ X X ↑↓ X X ↓ X X ↑ ↑ ↓ ↓ ↓

↓ ↑ ↑ ↓ ↑ ↑↓ − − − − − − − − − −

X ↓ ↑ X X ↑↓ ↓ ↓ ↑ − − − − − − −

r*,s† f*,t†,u† g* i† m* j* t†,u† t†,u† g*, t† t† t† t† t† t† v* v*

↓

−

−

v*

↓ − −

− − −

− ↑ ↑

v* w† l*

89

al., 1984; Kunze et al., 2013). In many species, this is accompanied by high barokinesis that reinforces upward swimming (e.g., Wheeler and Epifanio, 1978; Sulkin et al., 1983; Forward and Buswell, 1989; Forward and Wellins, 1989; Forward et al., 1989). Phototaxis in the first zoeal stage is variable, with some species not responsive to light at all (Table 1), which again is consistent with field observations of limited DVM in early stage zoeae (Epifanio et al., 2013). Subsequent zoeal stages show deeper and more variable depth distributions concomitant with changes in behavioral responses to light and gravity, namely strong negative phototaxis at low light intensities, coupled with more variable geotactic behavior. Megalopae again display uniform depth regulation, but transition to a benthic lifestyle with generally opposite behavioral responses to early zoeal stages, including positive geotaxis and variable responses to light (Table 1). Below, crabs in the families Xanthidae, Panopeidae, and several other taxa are discussed in more detail to illustrate how behavioral responses to gravity, hydrostatic pressure, and light are integrated into larval behavior. 2.4.1. Xanthid and panopeid crabs Early study of behavioral responses of brachyuran larvae to environmental stimuli dates to the 1930s and characterized swimming responses to isolated external factors (see Forward, 1976 for review). Beginning in the early 1970s, work on crabs in the families Xanthidae and Panopeidae demonstrated how collective swimming responses to gravity, hydrostatic pressure, and light provide a fundamental negative feedback mechanism for depth regulation (reviewed by Sulkin, 1984; Forward, 2009). Sulkin (1973) studied swimming responses of Cataleptodius floridanus (formerly Leptodius floridanus) and Panopeus herbstii in response to gravity in a small laboratory chamber in darkness. Rotating the chamber from horizontal to vertical allowed larvae to swim relative to gravity, and they displayed negative geotaxis (ascent) at all zoeal stages. Similar results were found for first-stage zoeae of Eurypanopeus depressus (Sulkin et al., 1983), as well as for all zoeal stages of Rhithropanopeus harrisii (Wheeler and Epifanio, 1978; Forward et al., 1984). Thus, the tendency for zoeae in darkness is to counteract the sinking that results from negative buoyancy with swimming and ascent in the water column. As larvae move vertically in the water column, they encounter a hydrostatic pressure gradient. To study larval swimming behavior in response to pressure, the same chamber configuration as for geotaxis was used, but with chamber seawater in closed loop with a device that adjusts static head or fluid compression to generate step increases or decreases in hydrostatic pressure within the chamber. With this approach, a range of studies complementary to the geotaxis work established that step changes in hydrostatic pressure result in barokinetic changes (high barokinesis for step increases, low barokinesis for step decreases), observed as changes in swimming speed and/or vertical position. This type of study was conducted for a number of taxa including: C. floridanus (Sulkin, 1973), E. depressus (Sulkin et al., 1983), R. harrisii (Bentley and Sulkin, 1977; Wheeler and Epifanio, 1978; Forward and Wellins, 1989; Forward, 1990), P. herbstii (Forward and Buswell, 1989), Panopeus obesus (Forward and Buswell, 1989), and Neopanope sayi (Forward et al., 1989). In xanthid and panopeid species where experiments were conducted over larval ontogeny, responses to hydrostatic pressure could be limited to the first zoeal stage (C. floridanus), or be observed at all zoeal stages (R. harrisii). As a larva sinks/swims in the water column, the perceived change in pressure per unit time will be a function of the pressure gradient itself, and the larva's movement through it. Accordingly, experiments with step changes can establish the overall response of larvae to hydrostatic pressure, but stimuli incorporating rates of pressure change are required to determine a response threshold. This was done with panopeids by Forward and colleagues using stage I (ZI) and stage IV (ZIV) zoeal larvae of N. sayi (Forward et al., 1989), and all zoeal stages of R. harrisii (Forward and Wellins, 1989). In both species, high barokinesis occurred upon rates of pressure increase in darkness. For

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R. harrisii, ZI–III larvae responded to rates of pressure increase greater than 0.175 mbar s− 1, while ZIV larvae required a 1.19 mbar s−1 rate of increase to evoke a response. For N. sayi, both ZI and ZIV larvae responded to rates of pressure increase greater than 0.4 mbar s − 1. In complementary experiments with rates of pressure decrease in darkness, larvae of all stages in both species responded to rates of decrease exceeding 0.4–0.71 mbar s − 1, except R. harrisii ZIV larvae which did not respond. Analysis of larval swimming speeds suggests that these rates of change are experienced by larvae in the water column. Forward and Wellins (1989) noted that during laboratory experiments in darkness, the distance R. harrisii zoeal larvae travelled before taking corrective behavioral action was longer when they were stimulated with a continuous rate of pressure decrease than during stimulation with a rate of pressure increase. This would reinforce the upward movement of larvae while in darkness. Accordingly, they hypothesized a depth regulatory window controlled by the light acclimation state of the larva. Forward (1989) confirmed this hypothesis by testing swimming behavior of R. harrisii ZI and ZIV larvae to rates of pressure change under a range of light acclimation levels. In accordance with the hypothesis, he found that (1) upon pressure decreases the ascent distance was shorter than descent distance when acclimated to high light levels, (2) under pressure increases the descent distance was shorter than ascent distance when acclimated to low light levels, and (3) the ascent/descent distances were equivalent when acclimated to intermediate light levels. Apart from light acclimation effects on reactions to pressure, brachyuran larvae respond behaviorally to the vertical gradient in light intensity. Here as well, experiments with xanthids and panopeids have been pivotal to understanding depth-regulation behavior. There is considerable variability in early reports of light-mediated swimming behavior in brachyuran larvae (reviewed in Sulkin, 1984; Forward, 1976, 1988; Table 1). A common result in much of the earlier work, generally conducted in narrow columns or troughs, was positive phototaxis in dark-acclimated zoeae, with some negative phototaxis at low light intensities following light-acclimation (e.g., C. floridanus and P. herbstii; Sulkin, 1975; R. harrisii, Forward, 1974; Forward and Costlow, 1974; E. depressus, Sulkin et al., 1983). Later experimental work by Forward and colleagues, however, determined that positive phototaxis was a laboratory artifact created by the trapping effect of light beams in narrow chambers (reviewed in Forward, 1988). Phototaxis studies conducted in simulated natural light fields showed only negative phototaxis (R. harrisii, Forward et al., 1984; Forward, 1986; P. herbstii and N. sayi, Forward and Buswell, 1989) or no photoresponse (P. obesus, Forward and Buswell, 1989). There are two functional implications of negative phototaxis for xanthid and panopeid larvae. First, downward movement upon rapid decreases in light intensity is part of a predator-avoidance shadow response (Forward, 1976, 1977, 1986). Light is attenuated by predators (e.g., gelatinous zooplankton), which casts a shadow on zoeae and triggers their downward escape. Further evidence for this has come from the finding that chemical cues emitted by predators increase the sensitivity of the shadow response in R. harrisii zoeae, making them more responsive to shadows when predators are abundant (Cohen and Forward, 2003; Rittschof and Cohen, 2004). The second functional implication of negative phototaxis concerns depth regulation. At light intensities above the visual threshold, larvae descend by negative phototaxis, while at light intensities below the visual threshold, larvae are in functional darkness and ascend by negative geotaxis. This has been most extensively studied in R. harrisii, where the behavior contributes to the descent phase of its diel vertical migration, and its maintenance of a daytime depth at an isolume approximating its visual threshold (Forward et al., 1984; Forward, 1985; reviewed in Forward, 2009; Cohen and Forward, 2009). Similar to the shadow response, chemical cues from predators decrease the light intensity required to evoke negative phototaxis in R. harrisii zoeae, with the mechanism involving both structural and physiological changes to photoreceptor cells in the retina (Charpentier and Cohen, 2015). Thus, zoeae are

predicted to occupy a deeper daytime depth when predators are more abundant than during periods when predators are less abundant. As with pressure, the behavioral response of xanthid larvae to the rate of change in light is important to understanding their swimming behavior in the water column. Among brachyuran larvae, this has only been rigorously studied in R. harrisii zoeae. Forward (1985) demonstrated that R. harrisii ZIV larvae ascend in response to relative rates of light intensity decrease. Light acclimation to twilight intensities and rates of decrease (e.g., −4 × 10−3 s−1) yielded the strongest response, which is consistent with similar studies in other zooplankton taxa (reviewed in Cohen and Forward, 2009). Collectively, the experimental work on swimming behavior of xanthid and panopeid larvae to gravity, pressure, and light stimuli can be synthesized by the light-dependent negative feedback model of depth regulation (Sulkin, 1984; Forward, 1989). In the absence of strong vertical mixing in the water column, the distribution of larvae results from negative buoyancy, which leads to a descent that is either reinforced or offset by behavioral responses. In this way, a passively sinking larva that experiences either darkness (i.e., ambient light levels below the threshold for detection by its visual system) and increasing hydrostatic pressure will respond behaviorally by exhibiting negative geotaxis and high barokinesis, which would result in upward movement. During ascent, a larva would ultimately detect light and decreasing hydrostatic pressure, and in turn exhibit negative phototaxis, positive geotaxis, and low barokinesis, resulting in downward movement and an eventual return to deeper water. Light acclimation level would set the upper and lower limits of the depth regulatory window, and this can change with ontogeny. In an ecological context, larval depth distributions vary over ontogeny to facilitate larval transport and ultimately recruitment to the adult habitat (see Section 3 below). Likewise, controlling depth is one mechanism for predator avoidance in a featureless pelagic habitat (Johnsen, 2014). Zooplankton routinely undergo diel vertical migration (DVM) behavior, most commonly involving daytime residence at deeper depths where less light is available to facilitate visual predation or to cause photo-damage in the larvae. At night, these organisms then swim into shallower water to feed on higher quantity and quality food under the cover of darkness (reviewed in Forward, 1988; Cohen and Forward, 2009; Ringelberg, 2010; Williamson et al., 2011). 2.4.2. Other focal species As with xanthids and panopeids, all other brachyuran zoeal larvae studied to date show negative geotaxis at early zoeal stages, shifting to positive geotaxis (or no geotaxis) by the megalopae stage (Table 1). In several species, such as the blue crab Callinectes sapidus (Sulkin et al., 1980; Sulkin and Van Heukelem, 1982) and the Asian shore crab Hemigrapsus sanguineus (Park et al., 2004; Cohen et al., 2015), this transition is well-studied and is evident in later zoeal stages. For these species, strong negative geotaxis in newly hatched ZI larvae and consequent aggregation in surface waters results in their export from the estuary and toward the continental shelf. It is here that larval development occurs and DVM is evident in later developmental stages, with megalopae returning to estuaries (see Section 3). In H. sanguineus negative geotaxis in Z1 larvae overwhelms responses to both light (Cohen et al., 2015) and hydrostatic pressure to which these larvae are weakly sensitive (step increase threshold for high barokinesis = 75 mbar; Park et al., 2004). Early stage C. sapidus zoeae are similar to H. sanguineus in only having high barokinetic responses upon large pressure changes (step decrease threshold for low barokinesis = 17 mbar; Forward and Buswell, 1989; see also Sulkin et al., 1980). They differ, however, in that C. sapidus zoeae display weak negative phototactic responses when tested in simulated natural light fields (Forward and Buswell, 1989). In both cases, larval behavioral responses to gravity, pressure, and/or light facilitate export from the estuary, and changes in these behaviors with ontogeny ultimately support the negative feedback model of depth regulation, and return of megalopae to estuaries (see Section 3). Early stage fiddler crab zoeae (Uca pugilator and U. pugnax) represent

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yet another scenario, where no phototactic response was evident, but larvae do exhibit high barokinesis upon step decreases in pressure (threshold = 3–5 mbar; Forward and Buswell, 1989). Their vertical distribution during larval development is controlled by endogenous rhythms rather than responses to exogenous environmental factors (see Section 3). 2.5. Effects of salinity and temperature on larval behavior 2.5.1. General aspects Initial study of effects of environmental factors on brachyuran larvae coincided with development of laboratory culture techniques in the mid-20th century (Costlow and Bookhout, 1959). Early work investigated tolerance of larvae to variation in salinity and temperature and included stage-specific impacts on duration, growth, and survival (e.g., Costlow et al., 1966). This line of research continued through the ensuing decades and eventually incorporated more sophisticated inquiry into the underlying physiology and biochemistry (e.g., Torres et al., 2011). In addition, the availability of culture techniques allowed investigators to determine effects of salinity and temperature on vertical swimming behavior. 2.5.2. Discontinuities in salinity and temperature The vertical position of any water parcel is controlled by its density, which varies directly with salinity and inversely with temperature. In stratified water columns, a more-dense deep layer is separated from a less-dense surface layer by discontinuities in salinity, temperature, and (consequently) density. These disjunctions are respectively termed haloclines, thermoclines, and pycnoclines. Because these clines lie in the vertical plane, they inherently affect vertical migration of planktonic organisms (Harder, 1968). Relevant work with crab larvae dates to the early 1970s and involved construction of haloclines in laboratory water columns wherein larvae were stimulated to swim upward or downward, often by the introduction of light (Table 2). These studies considered effects of low salinity, per se, as well as the difference in salinity across the halocline (ΔS). In a seminal study of this genre, Sulkin and van Heukelem (1982) worked with the blue crab Callinectes sapidus and found that temporary accumulation of zoeae at the halocline increased as a function of ΔS. Complete inhibition of swimming through the halocline, however, did not occur until ΔS reached 10‰, which is beyond the magnitude that usually occurs in nature, and the authors concluded that haloclines have little effect on vertical swimming of C. sapidus larvae in the natural environment. A later study with the fiddler crab Uca pugnax provided corroborating results and showed no inhibition of upward swimming until ΔS reached unrealistic levels N 5‰ (O'Connor and Epifanio, 1985). Similar investigations have addressed vertical swimming in the vicinity of temperature discontinuities. Sulkin et al. (1983) constructed realistic laboratory thermoclines (ΔT = 10 °C) and observed movement of panopeid zoeae (Eurypanopeus depressus) from the colder bottom layer (15 °C) to the warmer upper layer (25 °C). Results showed no difference in the proportion of larvae swimming into the upper layer when compared to control conditions without thermoclines. There was a qualitative difference in swimming behavior, however, when larvae encountered the discontinuity, which resulted in temporary aggregation of larvae at the thermocline before passing through. Likewise, Kelly et

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al. (1982) showed that newly hatched zoeae of the deep-sea crab Chaceon quinquedens were able to swim through a strong thermocline on the way to warm surface waters where they apparently complete larval development. In addition, McConnaughey and Sulkin (1984) found no inhibition of vertical migration when early-stage C. sapidus larvae were acclimated to 15 °C and then challenged with a 10 °C thermocline. In contrast, larvae acclimated to 17.5 °C failed to penetrate a gradient of 10 °C. This result suggests that larvae were avoiding the very warm surface layer (27.5 °C) rather than responding to the thermocline, itself. There is also a small body of field work that is relevant to these issues. Epifanio (1988a) compared diel patterns in vertical distribution of two portunid crabs (Callinectes sapidus and Ovalipes ocellatus) in a stratified water column near the mouth of Delaware Bay (USA). Results showed that C. sapidus zoeae remained near the surface regardless of diel phase, while O. ocellatus migrated to the surface at night and sank to the thermocline (ΔT ≈ 10 °C) during the day. These respective distributions would yield contrasting dispersal patterns with O. ocellatus more likely to be retained and Callinectes sapidus more prone to dispersal. Discontinuities in salinity, temperature, and density also occur in the horizontal plane where they are known as fronts. These structures consist of horizontal boundaries between water masses of different density and are common in estuaries and in the adjacent coastal ocean (Garvine and Monk, 1974). Water movement near a front includes convergent circulation where dense water sinks at the discontinuity and is replaced by convergent surface flow from both sides of the boundary (Garvine, 1974). This allows accumulation of buoyant material at the front itself. Epifanio (1987) reported very high abundance of panopeid crab larvae (Neopanope sayi) near a tidal front at the mouth of Delaware Bay and proposed a conceptual model that was based on upward swimming by the larvae rather than buoyancy. The basic premise of the model was corroborated by a more elaborate follow-up study, although the distribution of larvae relative to the front was deeper than expected (Clancy and Epifanio, 1989). More recent work has used a combined observational and modeling approach to investigate the distribution of larvae near fronts. For example, Tilburg et al. (2009) studied the plume emanating from Delaware Bay and found patches of early-stage C. sapidus larvae throughout the main body of the plume, while late-stage larvae were restricted to frontal regions along the offshore edge. Further analysis of the same plume data, showed similar bimodal distributions of early-stage versus latestage larvae of two other species, Hemigrapsus sanguineus and Uca pugnax (Epifanio et al., 2013). Results of a coincident modeling study generally concurred with observations, and the authors concluded that frontal regions provide a mechanism for retention of larvae near the natal estuary. 2.5.3. Small changes in magnitude Small changes in salinity and temperature can occur rapidly in conjunction with turbulent mixing in the water column and can have effects on larval behavior. For example, increases in salinity during flood tides induce upward swimming by Callinectes sapidus megalopae, which facilitates rapid transport from the coastal ocean to nursery areas within the estuary (Tankersley and Forward, 1994; Tankersley et al., 1995; Forward et al., 1994). In addition, Latz and Forward (1977)

Table 2 Behavioral response of brachyuran crab larvae to haloclines and thermoclines. Yes = larvae swim through. No = larvae do not swim through. Haloclines shown in ‰. Thermoclines shown in °C. Dashes signify no data. Species

2.5‰

5‰

10‰

10 °C

Time line of research

Chaceon quinquedens Callinectes sapidus Eurypanopeus depressus Callinectes sapidus Uca pugnax

– Yes – – Yes

– Yes – – Yes

– No – – No

Yes – Yes Yes –

Kelly et al. (1982) Sulkin and Van Heukelem (1982) Sulkin et al. (1983) McConnaughey and Sulkin (1984) O'Connor and Epifanio (1985)

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found that a small decrease in salinity (~ 1‰) induced reversal in the signs of phototaxis (from positive to negative) and geotaxis (from negative to positive) in Rhithropanopeus harrisii zoeae. The consequent effect on vertical distribution would be a descent in the water column. In contrast, Forward (1990) observed an ascent in the water column when R. harrisii or Neopanope sayi larvae were exposed to small decreases in temperature (b 0.5 °C) over a period of several minutes. In combination, these behaviors could function in regulation of depth by the larvae. The responses were generally short-lived, however, and initial behavioral patterns were recovered in ~5 min (Latz and Forward, 1977). Moreover, the results of earlier investigations were mixed and had shown no effect of natural temperature variation on the sign of geotaxis or phototaxis C. sapidus (Sulkin and Van Heukelem, 1982), but a reversal in the sign of geotaxis in R. harrisii (Ott and Forward, 1976). 3. Role of larval behavior in transport 3.1. General aspects The larvae of brachyuran crabs are relatively strong swimmers. Zoeae are capable of sustained speeds on the order of 0.5–1.5 cm s−1, and megalopae of some species can swim for extended periods at speeds N5.0 cm s− 1 (for reviews see Sulkin, 1984; Queiroga and Blanton, 2005; Epifanio, 2007). While these swimming speeds are inconsequential in horizontal current fields (Fig. 3), they take on critical importance in the vertical dimension where ambient currents are typically weak and often turbulent, rather than directional (Epifanio and Garvine, 2001). For example, a zoeal larva swimming upward at an apparent speed of 1.0 cm s−1 would cover ~225 m in a 6.2-hour, flood-tide phase, easily traversing the entire water column in most estuaries and on the continental shelf. It is also important to consider that crab larvae are negatively buoyant in sea water with passive sinking rates that range from b0.5 cm s− 1 in early-stage zoeae to N1.5 cm s− 1 in megalopae (e.g., Sulkin, 1984; Arana and Sulkin, 1993; Park et al., 2004). So, the apparent swimming speed when measured in the vertical plane is in fact the difference between the actual swimming speed and the actual sinking speed, and larvae obtain vertical displacement in the water column when they simply stop swimming and sink passively. A zoeal larva sinking at 0.2 cm s−1 would traverse ~45 m during a 6.2-h, ebb-tide phase, again representing a substantial portion of the water column in most estuarine and coastal environments. These factors have important effects on horizontal transport of larvae.

Fig. 3. Typical horizontal current speeds in estuarine and coastal environments compared to swimming speeds of crab and fish larvae. Estuarine current refers to barotropic tidal flow. From Queiroga and Blanton (2005).

3.2. Horizontal currents Horizontal currents in estuarine and coastal waters exhibit vertical shear in velocity wherein maximum current speed is at the surface and minimum speed is at the bottom (Epifanio and Garvine, 2001; Queiroga and Blanton, 2005). This phenomenon occurs regardless of direction of flow (e.g., ebb-tide current versus flood-tide current) and is caused by frictional interaction between the current and the bottom. Currents in estuarine and coastal waters are generated by a variety of agents and differ greatly in strength and in the frequency at which the velocity varies. It is the interaction between larval swimming behavior in the vertical plane and the frequency at which a current varies at any given depth that controls the net displacement of larvae in the horizontal dimension (Epifanio and Garvine, 2001). The majority of work on transport of brachyuran larvae has been carried out in estuarine and coastal waters (e.g., Epifanio, 1988b, 1988c; Forward and Tankersley, 2001; Naylor, 2006). Horizontal currents in these environments fall into three general categories depending on their respective forcing agents and are classified as tidally driven, wind-driven, or buoyancy-driven (for detailed discussion, see Epifanio and Garvine, 2001; Queiroga and Blanton, 2005; Whitney and Garvine, 2005). Tidally driven currents (in the context of our review) are a consequence of differences in sea level as the tidal wave progresses over any particular point in space, and they vary at higher frequency than wind-driven or buoyancy-driven currents. In areas that experience semi-diurnal tides, the duration of one complete tidal cycle is 12.4 h, and the frequency is represented as 0.08 cycles h−1. Water movements that vary at lower frequency are called subtidal currents. For example, wind-driven currents along the east coast of North America typically depend on the movement of continental weather systems, and frequency is characterized in units of cycles day−1, rather than cycles h−1 (Garvine et al., 1997). In contrast, buoyancy-driven currents depend on seasonal differences in precipitation and vary at even lower frequencies, best characterized as cycles week−1 or even cycles month−1. Flow in these three categories occurs simultaneously, and net circulation consists of the tidal, wind-driven, buoyancy-driven components, along with any interactions that the components produce. Tidal currents in estuaries typically flow at much higher speed than subtidal currents, and maximum velocity at the surface often exceeds 1.5 m s−1 (Sanders and Garvine, 1996). This can cause extensive horizontal displacement of larvae during the flood or ebb phase of the tidal cycle. But the oscillating nature of tidal flow reverses this movement during the subsequent phase, and the net displacement over one complete cycle at any given depth is small and approaches zero when averaged over several cycles (Epifanio and Garvine, 2001). This means that tidal flow itself has little effect on the horizontal displacement of larvae that remain at constant depth anywhere in the water column. Vertically integrated mean flow in an estuary, however, is seaward on time scales greater than a single tidal cycle because of riverine input at the head of the estuary, and the buoyancy of this input drives a slow seaward flow near the surface with compensating landward flow near the bottom (Pape and Garvine, 1982). Nevertheless, larvae that move up in the water column during flood phase and down during ebb phase can achieve landward transport in an estuary on the order of km day− 1. Likewise, larvae that move up in the water column during ebb phase can cover similar distances in a seaward direction. This type of horizontal movement is termed selective tidal stream transport (Forward et al., 2003a; Forward and Cohen, 2010) and can be partitioned into flood tide transport (FTT) or ebb tide transport (ETT) Flow at subtidal frequency becomes more important in the coastal ocean outside of estuaries where the interaction of buoyancy-driven and wind-driven currents controls horizontal movement of larvae. An example of this process occurs in the southern Middle Atlantic Bight (along the east coast of North America) where strong, buoyant flow emanates from three large estuaries and, because of Coriolis deflection, carries larvae along-shelf in a southward direction (Epifanio and

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Garvine, 2001; Tilburg et al., 2005; Whitney and Garvine, 2005). In contrast, across-shelf flow of surface water in this region is dominated by wind forcing, in particular by the along-shore component of wind blowing over the continental shelf (Tilburg and Garvine, 2003; Whitney and Garvine, 2005). Northward blowing winds create an upwelling circulation that is characterized by offshore flow of surface water, depression of coastal sea level, and subtidal flow out of estuaries. In contrast, southward blowing winds create a downwelling circulation that is characterized by onshore flow of surface water, a rise in coastal sea level, and subtidal flow of shelf water into estuaries (Epifanio and Garvine, 2001). 3.3. Effects of behavior on larval transport Larvae of estuarine and coastal crabs often display a pattern of vertical migration that either facilitates retention near adult populations or augments export to the open continental shelf. The discussion below concentrates on five taxa that have been subjected to particularly intense scrutiny concerning these processes. Summary information for these taxa appears in Table 3. 3.3.1. Mud crabs in the family Panopeidae Our first example is the white-fingered mud crab, Rhithropanopeus harrisii, which is an obligate estuarine species that occurs throughout the meso- and oligohaline regions of estuaries along the east and Gulf coasts of North America (Forward, 2009). Early life history consists of four zoeal stages and a megalopal stage, and results of field surveys show that larvae are retained near adult populations within the estuary (Forward, 2009). The mechanism for retention is an endogenous rhythm of upward swimming during flood tides and descent during ebb tides. This circatidal rhythm is strongly expressed in field-collected zoeae and is probably entrained by exposure to tidal cues during the

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egg-brooding process (Cronin and Forward, 1979, 1983). Additional study has revealed a pattern of diel vertical migration (DVM) superimposed on the tidal rhythm (Forward et al., 1984; Cronin and Forward, 1986). DVM is not endogenous, but instead relies on proximate cues associated with changes in the ambient light field (see Section 2; Forward et al., 1984; Forward, 1985; Cronin and Forward, 1988). Retentive behavior has been inferred for a number of other brachyuran taxa based on indirect evidence including: (1) preferential occurrence of larvae during the flood phase (Dittel et al., 1991; Garrison, 1999; Kunze et al., 2013); (2) exclusive distribution of larvae within the estuary as compared to the adjacent shelf (Steppe and Epifanio, 2006); or (3) deep distribution of larvae in the estuarine water column (e.g., Sandifer, 1975; Dittel and Epifanio, 1982). 3.3.2. Blue crabs In contrast, the blue crab Callinectes sapidus exports newly hatched larvae to the continental shelf where they pass through seven zoeal stages before they return to the estuary as megalopae. The species occurs in estuaries along the east coast of the Americas from Long Island (USA) to Argentina (Epifanio, 2007). Adults range throughout the estuary, and ovigerous females utilize ebb tide transport (ETT) to expedite migration to spawning grounds near the estuarine mouth (Darnell et al., 2010). Release of larvae occurs nightly throughout the breeding season around the time of nocturnal high tide, and there is no lunar or spring/neap periodicity to spawning intensity (Tilburg et al., 2008). Newly hatched larvae swim to the surface, and zoeae maintain a nearsurface position throughout the developmental period (Epifanio, 1988a; Natunewicz and Epifanio, 2001). This is accomplished by upward swimming to compensate for the negative buoyancy of the larvae, and there is no evidence for circa-tidal or diel periodicity in the process (Lopez-Duarte and Tankersley, 2007a). Upward swimming behavior

Table 3 Types of apparent vertical migration displayed by brachyuran crab larvae. Categories are inferred from field investigations. FloodNocturnal = nocturnal rhythm superimposed on flood-tidal rhythm. Dashes signify no data. Modified from Queiroga and Blanton, 2005. Species

Early zoeae

Late zoeae

Megalopae

Time line of research

Callinectes sapidus

Ebb

Constant surface

Nocturnal flood

Cancer magister

Nocturnal

Nocturnal

Nocturnal

Carcinus maenas

Ebb

Nocturnal

Nocturnal on shelf Flood in estuary

Rhithropanopeus harrisii

FloodNocturnal

FloodNocturnal

FloodNocturnal

Uca spp.

Ebb

Ontogenetic

Flood

Provenzano et al. (1983) Epifanio et al. (1984) Epifanio (1988c) DeVries et al. (1994) Tankersley and Forward (1994) Tankersley et al. (1995) Forward et al. (1997) Welch et al. (1999) Welch and Forward (2001) Epifanio and Natunewicz (2001) Hobbs et al. (1992) Jamieson and Phillips (1993) McConnaughey et al. (1992) McConnaughey et al. (1994) McConnaughey et al. (1995) Roegner et al. (2007) Zeng and Naylor (1996a) Zeng and Naylor (1996b) Queiroga et al. (1997) Queiroga (1996) Queiroga (1998) Marta-Almeida et al. (2006) Queiroga et al. (2007) dos Santos et al. (2008) Cronin and Forward (1982) Cronin and Forward (1986) Kunze et al. (2013) Epifanio et al. (1988) Forward et al. (1994) Petrone et al. (2005) Lopez-Duarte and Tankersley (2007a) Lopez-Duarte and Tankersley (2007b) Morgan and Anastasia (2008) Lopez-Duarte and Tankersley (2009) Lopez-Duarte et al. (2011)

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also permits entrainment of larvae in frontal regions along the edge of the estuarine plume, which allows retention of some larvae near the natal estuary, regardless of dispersive transport in the main stream of the plume (Tilburg et al., 2009). Outside the convergent circulation, the larvae are distributed as discrete patches on a scale of one to two km. Genesis of patches apparently depends on communal release of larvae by spatially aggregated females (Natunewicz and Epifanio, 2001). Patches occur on the inner continental shelf and are transported by a combination of buoyancy-driven and wind-driven processes (Natunewicz and Epifanio, 2001). These include: (1) dispersive transport of zoeae associated with buoyancy-driven flow; (2) retentive transport of zoeae linked to wind-driven, upwelling circulation; and (3) re-invasive transport of megalopae back to the estuary via wind-driven, downwelling circulation (for details, see Epifanio, 1995; Epifanio and Garvine, 2001; Epifanio, 2007; Epifanio and Tilburg, 2008). Along the east coast of North America, reinvasion of the estuary by blue crab megalopae occurs as discrete pulses linked to downwelling events (Epifanio and Garvine, 2001). Upon entering the estuary, megalopae rise in the water column during nocturnal flood tides and descend during all other tides (Little and Epifanio, 1991; DeVries et al., 1994; Olmi, 1994). Control of this behavior is exogenous and is elicited by rising levels of salinity and hydrostatic pressure (Tankersley and Forward, 1994; Tankersley et al., 1995; Forward et al., 1997a). The upward swimming response, however, is muted during daylight flood tides by the inhibitory effect of light (Forward and Rittschof, 1994). In contrast, the larvae respond to turbulence during nocturnal flood tides and continue to swim as long as the level of turbulent kinetic energy exceeds the behavioral threshold (Welch et al., 1999; Welch and Forward, 2001). When turbulence falls below this threshold, the megalopae cease swimming and descend in the water column. This suite of behaviors provides a basis for rapid passage up the estuary via flood tide transport (FTT). 3.3.3. Fiddler crabs Fiddler crabs in the genus Uca also export their larvae to the continental shelf. There are three species of Uca native to salt marshes along the temperate Atlantic coast of North America (Williams, 1984). The three species have similar life histories that include five zoeal stages and a megalopal stage (Dittel and Epifanio, 1982). Zoeal larvae are exported to the inner continental shelf and return to the estuary as megalopae (Epifanio et al., 1988; Jones and Epifanio, 1995; Epifanio et al., 2013). Larvae are released in summer during biweekly (i.e., spring tidal) spawning events near the time of nocturnal high tide (Forward, 1987a; Christy, 2011), and newly hatched zoeae are distributed in discrete patches (Petrone et al., 2005). Net seaward movement in estuaries with semidiurnal tides depends on an endogenous, circatidal rhythm in swimming activity, and there appears to be a secondary, circalunidian rhythm that is expressed in estuaries that experience diurnal tides (Lopez-Duarte and Tankersley, 2007a, 2007b; Morgan and Anastasia, 2008; Lopez-Duarte and Tankersley, 2009). In either case, larvae move upward in the water column during ebb tides and descend during flood tides with consequent downstream transport via ETT. Endogenous, circatidal rhythms have been observed in 15 species of Uca collected from a variety of habitats and tidal systems in North and Central America, and the strength of expression varies directly with distance from the respective habitats to the coastal ocean (Lopez-Duarte et al., 2011). The movement of Uca larvae on the continental shelf is less well known, and the mechanisms for along-shelf displacement of zoeae or across-shelf transport of megalopae (back to the estuary) are unclear. Results of early studies showed an ontogenetic change in distribution of zoeae with advanced stages deeper in the water column, which suggests slow landward transport via the gravitational circulation of the estuary (Dittel and Epifanio, 1982; Pape and Garvine, 1982; Epifanio et al., 1988). More recent work, however, has found dense patches of

advanced zoeae high in the water column (Petrone et al., 2005) and associated with retentive physical features like convergent fronts (Epifanio et al., 2013) or coastal null zones (Steppe and Epifanio, 2006). Eventual settlement of Uca megalopae in estuarine habitat occurs as discrete events interspersed throughout the spawning season, but again the forcing agents for across-shelf transport into the estuary are unclear (Jones and Epifanio, 1995; Ogburn and Forward, 2009). In contrast the mechanism for landward transport, once the megalopae enter the estuary, is well known and involves an endogenous circatidal rhythm with maximum swimming activity during flood tides. This pattern of behavior results in rapid movement of megalopae from the estuarine mouth to settlement sites farther upstream via FTT (Tankersley and Forward, 1994). 3.3.4. Dungeness crabs The Dungeness crab Cancer magister is another brachyuran species in which larval development occurs in the coastal ocean (Rasmuson, 2013). Adults range from Alaska to central California, and habitat includes soft sediments on the inner continental shelf and in estuaries. Larval development consists of five zoeal stages and a megalopal stage, and duration varies from five to ten weeks, depending on temperature (Sulkin and McKeen, 1989). Early work indicated that both zoeae and megalopae undergo DVM on the continental shelf with maximum abundance near the surface at night (Lough, 1976; Reilly, 1983; Jamieson and Phillips, 1993). More contemporary work, however, has reported crepuscular migration with maximum surface abundance in early evening and in the dark hours before dawn (Park and Shirley, 2005). In either case, the larvae descend in the water column during daylight hours. There has been a great deal of study of the horizontal transport of Dungeness zoeae and megalopae on the continental shelf, but there is no consensus concerning the principal agents that drive larval trajectories (Rasmuson, 2013; Sorochan and Quijon, 2014). Initial investigations reported early-stage zoeae on the continental shelf and advanced stages in the open ocean, as much as 150 km offshore (Lough, 1976; Reilly, 1983; Jamieson and Phillips, 1993). But the generality of this distribution was discounted in later work that argued for retention of zoeae and megalopae on the inner shelf (McConnaughey et al., 1992, 1994) and attributed across-shelf transit of megalopae to wind-driven processes (McConnaughey et al., 1995). Analysis of a five-year plankton survey off the northwest coast of the USA led to a similar conclusion concerning horizontal distribution of C. magister larvae (Hobbs and Botsford, 1992). That analysis included a simple transport model that predicted net onshore movement of vertically migrating megalopae due to wind-driven surface flow at night and Ekman transport during the day (Hobbs et al., 1992). But studies of settlement of Dungeness megalopae in estuarine environments have come to an entirely different conclusion. For example, results of high-frequency sampling over a nearly four-year period in Coos Bay, Oregon (USA) found no correlation between settlement and mean daily wind stress (Roegner et al., 2007). Instead, settlement varied in phase with maximum amplitude spring tides (when the spring phase was lagged by several days). The authors speculated that delivery of megalopae from the adjacent coastal ocean to the estuarine study site was driven by the onshore propagation of internal tidal bores associated with breaking internal waves (Pineda, 1995, 1999). 3.3.5. Shore crabs The European shore crab Carcinus maenas also exports larvae to the continental shelf. Native range includes the Atlantic coasts of Europe and North Africa, but invasive populations occur throughout the Atlantic and Pacific basins (Edgell and Hollander, 2011). Regardless of location, mature adults occur in a variety of habitats in the lower estuary. Early life history includes four zoeal stages and a single megalopa stage, and larval duration varies from four to seven weeks, depending on temperature (Dawirs, 1985). The mechanism for seaward transit of

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newly hatched zoeae involves an endogenous circatidal rhythm wherein larvae swim up in the water column during ebb tides and descend during flood tides (Zeng and Naylor, 1996a). This behavior is synchronized at hatching and is maintained through several tidal cycles under constant conditions in the laboratory (Zeng and Naylor, 1996b, 1996c). As with Uca, this rhythm in swimming activity provides the behavioral foundation for rapid downstream movement via ETT. But in contrast to Uca, the movement of C. maenas larvae on the continental shelf has been intensively studied. Early survey work on the Atlantic shelf off the Iberian Peninsula in Europe showed high abundance of early-stage larvae in coastal surface waters with progressive offshore movement of advanced stages to the mid-shelf region and deeper in the water column (Queiroga, 1996). More recent studies in the same geographical area confirmed the horizontal distribution of zoeae, and high-frequency sampling found evidence for DVM in both zoeae and megalopae (dos Santos et al., 2008). The occurrence of DVM provides a mechanism for inshore retention of larvae in areas like the Iberian coast where across-shelf flow during frequent upwelling events is seaward at the surface and landward near the bottom (Marta-Almeida et al., 2006; Queiroga et al., 2007). By undergoing DVM, the larvae reduce the extent of across-shelf transport in either direction, and because the source of larvae is estuarine, the net distribution is skewed toward the inner shelf. The eventual supply of megalopae to Iberian estuaries varies in phase with the fortnightly spring/neap cycle, which may reflect the greater flux of water during high-amplitude spring tides (Amaral et al., 2007). The supply is also increased by wind-driven, downwelling circulation during periods of relaxed upwelling (Queiroga et al., 2006). In either case, the supply of megalopae in the estuarine water column appears to be decoupled from actual settlement on the bottom, which occurs in conjunction with neap tides, rather than spring tides (Queiroga et al., 2006). Reasons for the decoupling are not clear, and it is not known if the phenomenon is general or restricted to C. maenas in European habitats (Amaral et al., 2007). Regardless, the behavior of C. maenas megalopae, once inside the estuary, has been inferred from field distributions and involves an apparent circatidal rhythm with upward swimming during flood tides and descent on ebb tides (Queiroga, 1998). 3.4. Transport models The use of mathematical models provides a powerful tool for isolating effects of factors that govern larval dispersal in complicated flow regimes (e.g., Metaxas and Saunders, 2009; Corell et al., 2012; Drake et al., 2013). For example, realistic simulation models allow researchers to turn off one physical process (e.g., buoyancy-driven flow or wind-driven flow) in order to focus on the effects of some other physical process (e.g., tidal circulation). Likewise, an investigator could run a model simulation with or without larval swimming behavior in order to isolate the effect of a biological process like DVM. In short, the availability of mathematical models allows researchers to conduct experiments or observations in the virtual world that would be impossible in the real world (e.g., Tilburg et al., 2008). In addition, these models allow researchers to generate surrogate data sets that link available real-world field observations. There are two kinds of transport models: empirical models (e.g., Hill, 1990) and numerical prediction models (e.g., North et al., 2008). Empirical models are based on observed relationships between forcing factors (e.g., tide, wind, or river discharge) and current velocity. Thus, empirical models require extensive sets of coincident data concerning forcing factors and currents in order to develop predictive algorithms. In contrast, numerical prediction models are based on the fundamental (i.e., firstprinciple) equations that govern the physical flow fields, including the response to factors such as wind stress and topography. In practical use, the results of hydrodynamic simulations are linked to particle transport models that create trajectories of simulated larvae in the

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flow field (Tilburg et al., 2007). This type of coupled model can track large numbers of larvae released simultaneously or sequentially at different locations in the model domain (Tilburg et al., 2005; Banas et al., 2009). Long-term investigation of blue crab larvae along the Middle Atlantic coast of the USA provides a good illustration of the use of models in transport studies (Table 4). Early work on that problem developed a two-dimensional, empirical model that assumed a near-surface distribution of zoeae on the continental shelf (Epifanio, 1988c; Garvine et al., 1997). Virtual zoeae were released in the coastal ocean near the mouth of Delaware Bay, and eventual transport of megalopae back to Delaware Bay was defined as recruitment. The empirical model was designed to test the tenets of a widely used conceptual model that explained the dispersive and retentive aspects of zoeal transport (Epifanio, 1995). The mathematical model allowed investigators to compare trajectories of simulated and actual patches of zoeae (Natunewicz and Epifanio, 2001) and to compare simulated and actual settlement of megalopae in juvenile habitat (Garvine et al., 1997). In both cases the mathematical model provided reasonable support for the conceptual model. Subsequent work used a three-dimensional, numerical prediction model with the same biological parameters and addressed issues such as: (1) recruitment of megalopae to juvenile habitat (Tilburg et al., 2005); (2) dynamics of larval patches (Tilburg et al., 2006); (3) retention of zoeae in coastal null zones (Tilburg et al., 2007); (4) temporal patterns in larval release (Tilburg et al., 2008); and (5) retention of zoeae in convergent fronts (Tilburg et al., 2009). Again, the results of model simulations were generally comparable to actual observations. Additional work with blue crabs employed a numerical prediction model farther south along the Atlantic coast in Pamlico Sound (Reyns et al., 2007). Model simulations incorporated known patterns of megalopal swimming behavior with consequent surface distribution during nocturnal flood tides (Forward et al., 1997a, 1997b). Results showed that simulated horizontal distribution of megalopae and early juveniles corresponded well to field observations when both wind and tides were included in the model runs, but the relationship was incoherent when simulations included only wind or only tide. Models also have been used to predict the spread of invasive crabs. For example, Tilburg et al. (2011) modeled potential dispersal of the Chinese mitten crab Eriochier sinensis in Delaware Bay where mature adults had been collected in previous investigations (Ruiz et al., 2006). The early life history of E. sinensis is well known, and there is extensive information on its larval tolerance to variation in physical factors like salinity and temperature (Dittel and Epifanio, 2009). There is no published information, however, concerning larval swimming behavior in this species. Nevertheless, the model was able to simulate and compare the effects of several behavioral scenarios on the settlement of E. sinensis in Delaware Bay and in the adjacent coastal ocean. Results determined that the pattern of vertical migration affects the magnitude of settlement, but not the location. In contrast, the timing and site of larval release had large effects on both location and magnitude. The authors concluded that there are no physical barriers to the spread of invasive populations of E. sinensis near the simulated study site. Banas et al. (2009) used a similar model to study potential settlement of invasive Carcinus maenas megalopae in Willapa Bay along the northwest coast of the USA. Results showed strong seasonal effects with maximum settlement of cohorts that were spawned during summer compared to spring. The study also demonstrated the dominant effect of hydrodynamics (compared to swimming behavior) in controlling larval trajectories. Models also have been used to study dispersal and recruitment of C. maenas larvae at respective meso-tidal and micro-tidal locations in the North Sea (Moksnes et al., 2014). In that investigation, field observations had determined that larvae from the meso-tidal site underwent vertical migration at tidal frequency, while those from the micro-tidal location migrated at diel frequency. Results of attendant modeling

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Table 4 List of mathematical models used to simulate transport of brachyuran crab larvae. Surface = constant distribution of larvae near the surface. Diel = vertical migration at diel frequency. Tidal = vertical migration at tidal frequency. Ontogenetic = constant shallow distribution of early-stage larvae and constant deep distribution of late-stage larvae. Slash marks indicate comparison of different simulated behaviors. Species

Type

Subject

Simulated behavior

Citation

Callinectes sapidus

Empirical

Dispersal and recruitment Patch trajectories

Surface Surface

Garvine et al. (1997) Natunewicz and Epifanio (2001)

Dispersal and recruitment Patch dynamics Horizontal distribution Larval retention Patterns of larval release Convergent fronts Across-shelf transport Invasive species Dispersal and recruitment Invasive species Patch genesis

Surface Surface Diel/tidal Surface Surface Surface Diel Diel Diel/tidal Diel/tidal/ontogenetic Surface

Tilburg et al. (2007) Tilburg et al. (2006) Reyns et al. (2007) Tilburg et al. (2007) Tilburg et al. (2008) Tilburg et al. (2009) Hobbs et al. (1992) Banas et al. (2009), Moksnes et al. (2014) Tilburg et al. (2011) Petrone et al. (2005)

Numerical prediction

Cancer magister Carcinus maenas

Empirical Numerical prediction

Eriochier sinensis Uca spp.

Numerical prediction Numerical prediction

efforts showed enhanced settlement resulting from tidal (versus diel) migration in the meso-tidal location, but no effect in the micro-tidal environment. The authors concluded that differences in observed behavior were hereditary and reflected adaptation to local hydrographic conditions. Additional modeling efforts have investigated the fate of fiddler crab larvae released into marsh creeks during mass spawning events near Delaware Bay (Petrone et al., 2005). Simulations were generally coherent with field observations at the study site and showed a change in shape of patches and a decrease in larval concentrations when patches exited the marshes and entered the main estuary. Simulations also showed that export of all larvae from a single spawning event required several tidal cycles. 4. Responses to chemical and tactile cues for settlement 4.1. General aspects Settlement and metamorphosis of brachyuran larvae is often facilitated by chemical and tactile cues that convey information about prospective juvenile habitat (Forward et al., 2001). These cues may be released into the ambient water by organisms living in the habitat or may be associated with the surface of living or inanimate substratum. Response to chemical cues differs fundamentally from response to light, hydrostatic pressure, or gravity in that chemical communication requires the actual movement of molecules from one individual to another (Thiel and Breithaupt, 2011). This results in a delay between emission of the cue and response by the receiving individual. Chemosensory organs in crustaceans are known as sensilla and are hair-like cuticular protrusions that contain sensory cells (Breithaupt and Thiel, 2011). Sensilla fall into two categories. The first includes structures that have both chemosensory and mechanosensory capability. These are important in handling stimuli that require direct contact with the substratum and are similar in chemical function to taste receptors in vertebrates. These sensilla are found on the mouthparts, periopods, and general body surface of adult crustaceans. The second category includes structures that have only chemosensory capability. These are termed aesthetascs and are usually concentrated on the antennae and antennules (Hallberg and Skog, 2011). Aesthetascs sense chemicals that have a remote source and have been transported to the sensory site by water movement. Aesthetascs are analogous to olfactory receptors in vertebrates. The majority of work on sensilla has concerned adult crustaceans, and there has been little study of the morphology, physiology, or ontogeny of sensilla in larval brachyurans. Likewise, the morphological sites of release of metamorphic cues produced by adult brachyurans has not been determined, but in many crustacean taxa, behavioral cues

are released as part of the general urine stream through excretory pores located at the anterior end of the organism (e.g., Kamio et al., 2014). Individuals can regulate the timing of urine release, which in turn provides some control over the release of cues. It is not known, however, if individuals can influence the quantity of cue in the urine at any particular point in time (Breithaupt, 2011). Regardless of these uncertainties, there is an extensive literature dealing with behavioral responses of crab larvae to chemical and tactile cues in the environment (Forward et al., 2001). Studies of settlement and metamorphosis in brachyurans have addressed a number cues including: (1) texture and physical nature of substratum; (2) presence or absence of biofilms; (3) dissolved chemicals emanating from juvenile habitat; (4) odors produced by conspecific adults; and (5) odors associated with co-occurring predators, prey organisms, or competitors (Forward et al., 2001). These investigations, while extensive, have utilized a small number of taxa that were chosen because of their convenience, specific habitat requirements, economic importance, or status as invasive species. In the following sections, the role of chemical and tactile cues in facilitating metamorphosis is discussed in some of these taxa (Tables 5 and 6). 4.2. Concept of competency Like other marine invertebrates, crab larvae eventually reach a point at which they are competent to undergo metamorphosis (Crisp, 1984). Brachyurans achieve competency during the megalopa stage, and this transition is marked by a progression in the molt cycle from intermolt to premolt status (Forward et al., 2001). It is during this period of competency that megalopae respond to environmental cues that accelerate or retard the process of metamorphosis. Thus, the effect of any putative cue can be quantified as the amount of time required to reach the metamorphic molt, once a larva has achieved competency. In studies of brachyuran larvae, this period is often called time to metamorphosis (TTM), and accurate measurement of this variable requires an initial determination of the point in time when larvae acquire competency. This determination can be difficult and time-consuming for field-caught megalopae wherein competency is assigned through visual inspection of each specimen under a microscope (Metcalf and Lipcius, 1992). Another way to assure competency is to use laboratory-reared megalopae as experimental subjects. This technique provides the exact age of each megalopa at the beginning of an experiment, and with appropriate preliminary data, assures that megalopae are exposed to experimental conditions as soon as they reach competency. Larvae of some marine invertebrates can delay metamorphosis for months and may even die in the absence of appropriate cues for settlement (Pechenik, 1990). In contrast, duration of the megalopal stage is measured on a scale of days for temperate and tropical species, and

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Table 5 Summary of responses by brachyuran crabs to water-soluble cues. The Studies column shows the number of relevant investigations that have been conducted on each species. The Conspecific column refers to odors produced by conspecific adults. The Other column refers to odors produced by adults of other species. Yes means that a cue elicits metamorphosis. No means that a cue does not elicit metamorphosis. A dash means that a cue has not been studied for a given species. Species

Family

Studies

Conspecific

Other

Substratum

Biofilm

Vegetation

Callinectes sapidus Hemigrapsus sanguineus Uca pugnax Panopeus herbstii Carcinus maenas Metacarcinus magister Dyspanopeus sayi Neohelice granulata Menippe mercenaria Necora puber Rithropanopeus harrisii Sesarma curacaoense Uca minax Uca pugilator Ucides cordatus

Portunidae Varunidae Ocypodidae Panopeidae Portunidae Cancridae Panopeidae Varunidae Menippidae Portunidae Panopeidae Sesarmidae Ocypodidae Ocypodidae Ucididae

8 8 5 3 2 2 1 2 1 1 1 1 1 1 1

No Yes Yes Yes No – Yes Yes No – Yes Yes – Yes Yes

– No No Yes – – No – No – No Yes – No No

Yes Yes Yes Yes Yes Yes – Yes Yes Yes – – Yes Yes Yes

– No – Yes – – – – – – – – – – –

Yes – No Yes Yes Yes – – Yes Yes – – – No –

megalopae may ultimately undergo metamorphosis regardless of cues. For most species that have been studied, TTM is shortened by only a few days in the presence of a cue (Forward et al., 2001). Nevertheless, the widespread response to cues among brachyuran species indicates that acceleration of metamorphosis is an adaptive process that is important in finding suitable juvenile habitat. 4.3. Examples of responses to chemical cues in brachyuran larvae 4.3.1. Blue crabs One species that has received especially intense study is the blue crab Callinectes sapidus. The larval ecology of C. sapidus is well known and has been the subject of recent reviews (Epifanio and Garvine, 2001; Epifanio, 2007; Epifanio and Tilburg, 2008). Mating occurs in the middle and upper reaches of estuaries, and inseminated females migrate to the estuarine mouth and adjacent coastal ocean where eggs are brooded and hatched. Zoeal development occurs on the continental shelf, and larvae return to the estuary as megalopae (see Section 3.3.2). Upon entering the estuary, megalopae face the challenge of finding structured nursery habitat (e.g., seagrass meadows or algal beds) where they settle and undergo metamorphosis. Because of the patchy distribution of these habitats, it is not surprising that chemical cues are involved in this process. Early study of effects of chemical cues on TTM in C. sapidus utilized field-caught megalopae. For example, Wolcott and DeVries (1994) collected megalopae from the inner shelf near the mouth of Chesapeake Bay and found that exposure to estuarine water decreased TTM compared to water from the site of collection. Forward et al. (1994)

corroborated these results and found that estuarine water reduced TTM compared to shelf water and that addition of eelgrass (Zostera marina) yielded further reduction in TTM. Exposure to odors from adult crabs, however, had no effect compared to shelf water alone, and the authors attributed this result to the cosmopolitan distribution of adult blue crabs in the estuary compared to the patchy distribution of nursery habitat, i.e., there is no selective advantage to settling near adults. In fact, there may be a major disadvantage to settling near adults and older juveniles because of the high incidence of inter-cohort cannibalism in this species (Moksnes et al., 1997). In a follow-up study of water-soluble cues, Forward et al. (1996) again found that metamorphosis was accelerated in estuarine water and determined that the active cue was b10 kDa in size. Further investigation indicated that exposure to natural humic acids extracted from estuarine water yielded a significant decrease in TTM, and a similar effect was obtained from commercial humic acid (Forward, 1997a, 1997b). The authors concluded that humic acids could serve as a general estuarine cue because of the strong inverse relationship between acid concentration and salinity. Additional laboratory study of habitat-specific cues tested effects of seagrass and benthic algae on metamorphosis (Brumbaugh and McConaugha, 1995; Forward et al., 1996). Results showed that watersoluble compounds produced by seagrasses decreased TTM as effectively as exposure to the grass itself and also found that abiotic mimics of the seagrasses had no effect at all. Moreover, the influence of benthic algae varied strongly among species with some taxa causing a significant reduction in TTM and others having no activity whatsoever. A related field investigation of settlement in C. sapidus showed similar results wherein megalopae settled preferentially on artificial substratum that

Table 6 Summary of responses by brachyuran crabs to tactile cues. The Studies column shows the number of relevant investigations that have been conducted on each species. The Mimic column refers to artificial vegetation. Yes means that a tactile cue elicits metamorphosis. A question mark means that the effect of a putative tactile cue has not been differentiated from the associated water-soluble cue. No means that a tactile cue does not elicit metamorphosis. A dash means that a tactile cue has not been studied for a given species. Species

Family

Studies

Substratum

Biofilm

Vegetation

Mimic

Callinectes sapidus Hemigrapsus sanguineus Uca pugnax Panopeus herbstii Carcinus maenas Metacarcinus magister Neohelice granulata Dyspanopeus sayi Menippe mercenaria Necora puber Rithropanopeus harrisii Sesarma curacaoense Uca minax Uca pugilator Ucides cordatus

Portunidae Varunidae Ocypodidae Panopeidae Portunidae Cancridae Varunidae Panopeidae Menippidae Portunidae Panopeidae Sesarmidae Ocypodidae Ocypodidae Ucididae

8 8 5 3 2 2 2 1 1 1 1 1 1 1 1

– Yes No ? ? ? No – Yes ? – ? No No No

– Yes – ? – – – – – – – – – – –

No – No ? ? ? – – ? ? – – – No –

No No No No – – – – – No – – – – –

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contained seagrass blades, but not on substratum that contained saltmarsh cord grass (Welch et al., 1997). Results of this study also showed that settlement was reduced by as much as 40% on substratum that contained potential predators, and related laboratory trials showed that megalopae avoided water that contained predator odors. These findings were corroborated by additional work, which showed strong selection by blue crab megalopae for seagrass and other complex substrata in field-deployed mesocosms and cages (Van Montfrans et al., 2003; Moksnes and Heck, 2006). Orientation of blue crab megalopae is also affected by chemical cues in the water column. Several studies (Diaz et al., 1999; Forward et al., 2003b) have used flume techniques to investigate the role of directional swimming in finding suitable nursery habitat. Results showed an increase in upstream swimming in response to rising concentrations of seagrass odor. In contrast, there was an increase in downstream swimming in response to chemical cues produced by potential predators like fiddler crabs and grass shrimp. These responses were intensified for megalopae that were in premolt stage (compared to intermolt). Overall results for blue crabs indicate that megalopae are able to discriminate between suitable and adverse settlement sites based on odors associated with the respective areas. In addition, blue crab megalopae are among the few species studied to date that fail to respond to odors from conspecific adults (Table 5). This indicates that the presence of adults is not a good indicator of the quality of prospective juvenile habitat for this species. 4.3.2. Mud crabs Mud crabs in the family Panopeidae are common estuarine species that occur in shallow habitat along the Atlantic and Gulf coasts of North America (Williams, 1984). Metamorphic cues for mud crabs have been studied in three species: Panopeus herbstii; Rhithropanopeus harrisii; and Dyspanopeus sayi. Larval development in mud crabs consists of four zoeal stages and a single megalopal stage. Larvae of estuarine species typically undergo vertical migration at tidal frequency, which facilitates retention within the estuary (see Section 3.3.1; Dittel and Epifanio, 1982; Cronin and Forward, 1983; Steppe and Epifanio, 2006). Megalopae, however, often need to find structured juvenile habitat in areas that are otherwise dominated by large expanses of muddy or sandy bottom. Work on this problem began in the 1990s when Weber and Epifanio (1996) investigated a number of potential cues that could enable settlement and metamorphosis in appropriate habitat. Results of the investigation showed that natural rock/shell substratum and rock-associated seaweed (Fucus vesiculosus) both induced metamorphosis, while natural sand substratum was entirely inactive. Likewise, structural mimics of preferred substratum failed to induce metamorphosis unless they were covered with biofilm from adult habitat. Megalopae also responded strongly to water-soluble cues produced by adult P. herbstii, and similar results were obtained for the mud crab Rhithropanopeus harrisii, which responded to odors from its own conspecific adults (Fitzgerald et al., 1998). Later investigation with P. herbstii corroborated these results and again demonstrated metamorphic cues associated with various aspects of juvenile and adult habitat (Andrews et al., 2001). These included natural rock/shell substratum, natural biofilm, and odor from adult conspecifics. Further analysis of the conspecific odor indicated that the metamorphic cue is a small, water-soluble molecule (b 1 kDa) that maintains its activity after freezing or boiling. Additional work with P. herbstii again showed strong metamorphic reaction to conspecific odor and also found a significant response to odor from a closely related mud-crab species (Dyspanopeus sayi). In contrast, odor from a more distantly related species (Uca pugnax), as well as odor from a potential prey species were entirely inactive (Rodriguez and Epifanio, 2000). A subsequent study with P. herbstii again showed strong metamorphic response to odor from conspecific adults, but failed to corroborate the positive response to odor from D.

sayi (Kopin et al., 2001). Likewise, metamorphosis was accelerated in D. sayi megalopae that were exposed to conspecific odor, but there was no significant response to odor produced by adult P. herbstii. A second part of the Rodriguez study provided a more intense investigation of the metamorphic cue associated with natural biofilm (Rodriguez and Epifanio, 2000). Results of combined field and laboratory experiments showed that the cue is associated with the bacterial component of the biofilm (rather than the algal component) and that biofilms gain potency as they age. Moreover, biofilms from different habitats varied greatly in their ability to induce metamorphosis. When glass microscope slides were incubated in adult habitat, odor from the resulting biofilm had a strong effect on metamorphosis. In contrast, slides that were incubated on adjacent sand flats were completely inactive. In general, the body of work with mud crabs shows strong metamorphic response to odors produced by conspecific adults and to water-soluble chemicals associated with natural substratum and particularly to biofilms from adult and juvenile habitat. These responses are especially adaptive in regions where the spatial distribution of hard substratum is patchy. 4.3.3. Fiddler crabs There are three species of fiddler crab native to salt marshes along the temperate Atlantic coast of North America (Williams, 1984), and habitat is partitioned according to salinity and sediment type (Miller and Maurer, 1973). Both Uca pugilator and Uca pugnax occur in high-salinity marshes (N15‰), but U. pugilator prefers coarser sediment. In contrast, Uca minax occurs in fine, muddy sediments associated with low-salinity marshes. The three species have similar life histories that include five zoeal stages and a megalopal stage. Zoeal larvae are exported to the inner continental shelf and return to the estuary as megalopae (see Section 3.3.3; Jones and Epifanio, 1995; Epifanio et al., 2013). Survival of newly metamorphosed juveniles depends on recognition of appropriate marsh habitat by settling megalopae. Laboratory investigation of this problem began with Christy (1989), who found a large reduction in TTM for U. pugilator megalopae reared over natural sediment compared to clean bottom with no sediment. In a following study with U. pugilator, O'Connor (1991) reported higher occurrence of metamorphosis in laboratory groups exposed to a combination of natural sediment and adult conspecifics compared to filtered sea water alone. These results were coherent with field observations in a North Carolina (USA) marsh, which showed that megalopae of U. pugilator and U. pugnax settled respectively in areas occupied by conspecific adults (O'Connor, 1993). In additional laboratory experiments, O'Connor and Gregg (1998) described a reduction in TTM among U. pugnax megalopae exposed to odor from adult conspecifics. There was no response, however, to odor from the congeneric fiddler crab, U. minax. Likewise, there was no reaction to odor from the common saltmarsh grass, Spartina alterniflora. In subsequent work in a Massachusetts (USA) marsh, O'Connor and Judge (1997) reported a threefold increase in the number of U. pugnax undergoing metamorphosis when held in field-deployed cages containing freshly collected marsh sediment compared to cages containing combusted, abiotic sediment from the same marsh. Results of that study also showed that sibling megalopae held in filtered sea water in the laboratory had no incidence of metamorphosis whatsoever during the same time period. Megalopae in field-deployed cages apparently had responded to a combination of water-soluble cues emanating from conspecific adults in the marsh and from some other agent within the natural sediment itself. Abiotic physical aspects of the sediment, however, were not involved in the process. Subsequent caging experiments corroborated these results and demonstrated an additive effect of cues from natural marsh sediment and from the overlying water column that presumably contained odors from adult crabs (O'Connor and Judge, 1999). Moreover, the authors found that response to cues was dose-dependent and that overall results were consistent in two

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different years and in marshes that differed in sediment-particle size. In contrast, there was no effect on metamorphosis when cages with natural sand sediment were deployed on a sand flat adjacent to the marsh study sites. In contrast, O'Connor and Van (2007) exposed U. pugnax to natural mud-flat sediments that had been incubated with conspecific adults and observed a significant increase in metamorphosis when compared to non-incubated control sediment. The authors concluded that cues produced by adult crabs were retained in the mud-flat sediment and had induced metamorphosis in megalopae exposed to the modified sediment. In related work with Uca minax, O'Connor and Judge (2004) again used caging techniques to monitor the incidence of metamorphosis among megalopae deployed along a 15-m transect extending from a marsh surface to an adjacent tidal river. Results showed maximum response in cages deployed over the marsh surface, intermediate response at distances of 2 and 5 m from the marsh, and no response at 15 m. The authors concluded that water-soluble cues for metamorphosis of U. minax originate in the marsh and decline sharply with distance away from the marsh. In addition, the investigators found high occurrence of metamorphosis in marsh-deployed cages that lacked sediment and thus concluded that any tactile cue associated with the process was secondary to the water-soluble cues. O'Connor (2005) took a different approach to the problem by investigating the response of U. pugnax megalopae to a proteinaceous extract derived from adult conspecifics. Results showed a dose-dependent reduction in TTM in groups of megalopae exposed to conspecific extract. Moreover, the extract remained potent when boiled and then frozen for periods as long as two years. There was no response, however, when U. pugnax megalopae were exposed to extract from the congeneric fiddler crab, U. minax. In addition, exposure to extract from the more distantly related mud crab, Dyspanopeus sayi, actually retarded development and increased TTM compared to control groups that were exposed to filtered sea water alone. Overall results for fiddler crabs show acceleration of metamorphosis in megalopae exposed to odors from adult conspecific crabs. This conspecific effect is consistent for each of the taxa studied, and odors from closely related species are always inactive. Fiddler crab megalopae also respond strongly to natural marsh sediment, and this effect appears to be independent of the physical characteristics of the sediment. This set of strong responses is particularly adaptive in species (like fiddler crabs) where the range of suitable adult and juvenile habitats is very narrow. The effect of water-soluble cues, however, declines sharply with distance from the source, and larvae are entirely unresponsive at distances beyond 15 m. Thus, it is unlikely that water-soluble cues are important in the long-distance location of suitable habitat by brachyuran megalopae. Rather, these cues are essential in discriminating among potential settlement sites only after megalopae have been transported (perhaps blindly) to the sites by ambient currents. 4.3.4. Asian shore crab The Asian shore crab, Hemigrapsus sanguineus, is a recent invader of the Atlantic coast of North America, and the role of metamorphic cues in facilitating the invasive process has been the subject of extensive research (Epifanio, 2013). The species is native to the temperate east coast of Asia (Sakai, 1976; Takahashi et al., 1985; Hwang et al., 1993) and was first observed in North America near Delaware Bay in the late 1980s (Williams and McDermott, 1990). The crab spread rapidly in its invasive locale (McDermott, 1991, 1998) and is now the dominant crab in rocky habitat along the east coast of the USA from Maine to North Carolina (Griffen et al., 2011). The Asian shore crab also occurs on the Atlantic coast of Europe, and invasive populations extend from the Cotentin Peninsula in France to Lower Saxony in Germany (Dauvin et al., 2009). The early life history of the species includes five zoeal stages and a megalopal stage (Epifanio et al., 1998). Results of behavioral studies suggest that newly hatched zoeae are exported to the coastal ocean and that advanced stages are transported shoreward as part of

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the gravitational circulation of the estuary (Park et al., 2004; Cohen et al., 2015). In addition, H. sanguineus larvae that are entrained in frontal circulation near the mouth of an estuary are generally retained, while those in the mainstream of buoyancy-driven coastal currents are transported away from the natal estuary and may serve as agents for further invasion (Epifanio et al., 2013). The earliest report of metamorphic cues in H. sanguineus came from Andrews et al. (2001), who were actually studying metamorphosis in the native mud crab Panopeus herbstii. Results of that investigation showed accelerated metamorphosis of P. herbstii in response to odors from conspecific adults. Likewise, metamorphosis was stimulated by natural substratum, natural biofilm, and surprisingly by exudates from the Asian shore crab. Kopin et al. (2001) conducted a related set of experiments in which H. sanguineus megalopae were exposed to odors produced by conspecific adults and by two species of native mud crab (Panopeus herbstii and Dyspanopeus sayi). As expected, results showed a strong effect of conspecific odor on metamorphosis. Conversely, there was no response whatsoever to odor from either mud crab. Later work by O'Connor (2007) corroborated these results and again found strong response to conspecific adults. In a subsequent study, Steinberg et al. (2007) investigated the response of Asian shore crabs to odors produced by four other species of Hemigrapsus (from the Pacific coasts of Asia and North America) and by several unrelated crab taxa that share common habitat with H. sanguineus in those same locations. Results agreed with previous work in that megalopae again responded strongly to odor from conspecific adults. The cue, however, was highly specific, and H. sanguineus did not respond to odors from other species, regardless of taxonomic or geographic affinity. Ancillary work by Anderson and Epifanio (2009) provided similar results and showed positive response to cues produced by juvenile H. sanguineus as well as adults. In a related study, Rasch and O'Connor (2012) found no metamorphic response to odors from predatory fish that co-occur with H. sanguineus in North American habitat. Kopin et al. (2001) were the first to investigate the role of substratum cues in the metamorphosis of H. sanguineus. Their experiments showed significant response to pebbles from adult habitat, but did not distinguish between the water-soluble and tactile nature of the cue. In more recent work, Steinberg et al. (2008) grew natural biofilm on experimental substratum and observed accelerated metamorphosis in megalopae that had full access to the biofilm. Moreover, these authors used microscopic techniques to confirm and quantify the presence of bacteria in the biofilm. Related studies by Anderson and Epifanio (2009) again showed that H. sanguineus megalopae respond to biofilm associated with rocky intertidal habitat. But in contrast to results from P. herbstii, the cue did not appear to be water-soluble, and exposure to odor (alone) from active biofilm did not elicit a metamorphic response. O'Connor (2007) also studied the effects of biofilm and substratum on metamorphosis of H. sanguineus. Results indicated that megalopae generally reacted to complexity of substratum. Molting was accelerated by small pebbles (with or without biofilm) and by nylon mesh with pore sizes ranging from 500–5000 μm. Steinberg et al. (2008) found a similar response to tactile cues wherein texture of substratum had strong effects on metamorphosis. Megalopae responded to abiotic nylon mesh of medium texture (100 and 1000 μm), but there was no significant effect of exposure to 10 μm or 2000 μm mesh. These results suggest lower and upper thresholds of roughness, below and above which the substratum loses attractiveness. In a separate experiment, Steinberg et al. (2008) again showed that clean nylon mesh (1000 μm) facilitated metamorphosis, but also revealed an augmented effect when that material was covered with biofilm. This result is particularly interesting because there was no response to the same biofilm when established on a smooth plastic surface. Thus, the augmented effect depends on both the biochemical character of the biofilm and the textural character of the substratum. Further studies have characterized the water-soluble cue produced by adult H. sanguineus (Steinberg et al., 2008; Anderson et al., 2010).

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Results indicate a small molecule (b 12 kDa) that behaves like a protein or peptide (Anderson et al., 2010). For example, the cue was inactivated by trichloroacetic acid, which precipitated all protein from solution, and by treatment with enzymes (trypsin or proteinase K) that cleave the peptide chain. Quantitative analysis of protein in the exudate indicated a sensory threshold between 0.1 and 0.01 μg of protein ml− 1 of sea water. The calculated range, however, refers to total protein, and not the specific metamorphic molecule. So, the actual cue is probably detected by megalopae at even lower concentrations. There is a smaller body of work that deals with the effects of chemical cues on H. sanguineus under field conditions. For example, O'Connor and Judge (2010) used caging techniques (see above) to investigate effects of metamorphic cues and found high response of megalopae in cages moored near rocky habitat with an established adult population. Metamorphosis, however, was also stimulated in cages deployed in marsh environments that had few adult H. sanguineus. The authors speculated that broad response to habitat cues may have facilitated the invasion of American and European habitats by H. sanguineus. Anderson and Epifanio (2010) also used caging techniques to determine the response of H. sanguineus megalopae to natural water-borne cues near adjacent rocky and marsh habitats. Like the above study, the percentage of megalopae undergoing metamorphosis was greatest in cages that were closest to the adult population, but results differed from O'Connor and Judge by showing reduced metamorphosis in cages adjacent to the salt marsh. While reasons for disparate findings are not clear, both studies demonstrate that H. sanguineus megalopae respond strongly to water-soluble cues under field conditions. The overall results of the investigations discussed in this section confirm the importance of substratum-based cues in accelerating the metamorphosis of H. sanguineus and point to the critical role that suitable habitat plays in the survival of juvenile H. sanguineus. But within this broad response to physical texture, there is a narrower range of preferred settlement cues, which implies an optimal bottom texture that provides shelter for megalopae as they metamorphose to the juvenile stage. In addition, the ability to detect multiple substratum cues for settlement and metamorphosis is a clear advantage for range extension of bioinvasive species like H. sanguineus. Likewise, the strong response to water-soluble cues produced by conspecific adults is an advantage in recruiting megalopae to invasive populations that have already been established. 4.3.5. Miscellaneous taxa Additional work with other brachyuran species has yielded a variety of results. For example, Fernandez et al. (1993) reported greater incidence of metamorphosis of the Dungeness crab, Cancer magister, in laboratory plots of natural mud and oyster shell compared to eel grass or bare mud. Later studies in a laboratory flume also showed that Dungeness megalopae avoided odors from co-occurring predators like the shore crab, Hemigrapsus oregonensis (Banks and Dinnel, 2000). Lee et al. (2004) also used flume techniques and found differential settlement of the velvet swimming crab, Necora puber, in substrata of varying complexity. In another study, Gebauer et al. (1998) found that natural substratum from adult habitat decreased TTM in Neohelice granulata (formerly Chasmagnathus granulata), but there was no effect when megalopae were exposed to abiotic sediment that had identical grain size. Megalopae also responded to conspecific odor, and a combination of natural sediment and conspecific odor produced an augmented effect. Subsequent experiments with the semiterrestrial crab Sesarma curacaoense found strong response to odor from conspecific adults and moderate response to odor from the congeneric crab, Sesarma rectum (Gebauer et al., 2002). There was no significant effect, however, of odors produced by distantly related crab species. Likewise, mud from adult burrows elicited metamorphosis in the mangrove crab, Ucides cordatus, while mud from an adjacent stream-bank was entirely inactive (Diele and Simith, 2007). U. cordatus also responded to odor from conspecific adults, but there was no significant response to odors from a

number of co-occurring crabs (Simith and Diele, 2008; Simith et al., 2013). In related work, the Florida stone crab, Menippe mercenaria, showed higher incidence of metamorphosis when exposed respectively to the brown alga Sargassum fluitans, rubble from nursery habitat, or biofilmcovered oyster shell (Krimsky and Epifanio, 2008). In contrast, there was no response to the seagrass Thalassia testudinum, even though juvenile stone crabs are often found in seagrass meadows under natural conditions. Likewise, the megalopae failed to respond to water-soluble chemicals from nursery substratum, although the rubble itself was highly active. Moreover, there was no response whatsoever to odors from adult conspecifics. Zeng et al. (1997) observed this same lack of response to adult odor in megalopae of the European green crab Carcinus maenas, and later flume experiments with this species showed preferential settlement in structured habitat (mussel, eelgrass, or algal beds) compared to sand bottom (Hedvall et al., 1998). 5. Summary and conclusions Our review has highlighted the importance of larval behavior in controlling growth, survival, dispersal, and settlement of brachyuran crab larvae in marine and estuarine environments. This behavior largely consists of swimming in the vertical plane within the water column and ultimately settling and undergoing metamorphosis in benthic habitat. Swimming behavior in larval crabs is regulated in large part by external cues detected in the water column. Gravity, light, and hydrostatic pressure are the primary cues because of their predictability in the environment. In aquatic systems, the gravitational field is uniform across depth with acceleration toward the center of the Earth. Likewise, hydrostatic pressure is a conservative variable, and its magnitude increases as function of depth. Brachyuran larvae detect the direction of gravity via statocysts, which also sense changes in hydrostatic pressure and angular acceleration. While still predictable, the underwater light field is far more variable than either gravity or hydrostatic pressure. In crab larvae, light for vision is detected by a pair of apposition compound eyes, with four properties of light (i.e., intensity, spectral composition, angular distribution, and polarization) having implications for larval behavior. Our synthesis of the literature shows that light often works in concert with gravity and hydrostatic pressure to generate behaviors in brachyuran larvae. Specifically, light provides controlling, initiating, and orienting agents for swimming behavior, while gravity functions as an orienting factor. Control of a behavior refers to the light/dark acclimation state of the larval vision system, which influences the ability to detect light stimuli in general and can influence responses to other cues such as hydrostatic pressure. Initiation of a behavior consists of direct stimulation by light and may involve the absolute light level or the relative magnitude or rate of change in irradiance. Orientation refers to direction of a behavior and may or may not involve light, even if light has played a controlling or an initiating role. In the absence of strong mixing in the water column, the vertical distribution of larvae results from negative buoyancy, which leads to a descent that is either reinforced or offset by behavioral responses. In this way, a passively sinking larva that experiences decreasing light intensity and increasing hydrostatic pressure responds behaviorally by exhibiting negative geotaxis and high barokinesis, which results in upward movement. During ascent, a larva ultimately detects increasing light intensity and decreasing hydrostatic pressure, and in turn exhibits negative phototaxis, positive geotaxis, and low barokinesis. This combination of behaviors results in downward movement and an eventual return to deeper water. Salinity and temperature also have effects on the behavior of brachyuran larvae, but larvae are relatively insensitive to variation in these factors within the bounds of physiological tolerance. Vertical migration in most species is not impeded by realistic laboratory haloclines or thermoclines, and reversals in the sign of phototaxis (induced by sudden changes in salinity or temperature) are short-lived. Nevertheless,

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predictable changes in salinity can serve as a cue for upward swimming during flood tides with consequent upstream transport of larvae. A common theme in the literature is the role of vertical swimming in the mediation of horizontal transport. The present review provides a brief tutorial that discusses the types of flow that occur in estuarine and coastal environments and explains the concepts of temporal frequency in flow regimes and vertical shear in current velocity. Our analysis of the literature has shown that: (1) brachyuran larvae are comparatively strong swimmers; (2) swimming can be arrhythmic or rhythmic; and (3) rhythms can be endogenous or exogenous. Arrhythmic swimming is associated with simple depth regulation, while rhythmic swimming is linked to retention of larvae in estuarine and coastal habitats, rapid transit of larvae via selective tidal stream transport, or diel vertical migration in coastal waters. Mathematical models have come on the scene in recent years and provide a powerful tool for isolating effects of factors that govern dispersal in complicated flow regimes. Our discussion has provided examples of different types of models and their application to different ecological problems involving brachyuran crabs. Like other marine invertebrates, crab larvae eventually reach a point at which they are competent to undergo metamorphosis. In brachyuran larvae, settlement and metamorphosis is often facilitated by chemical and tactile cues that convey information about prospective juvenile habitat. These cues may be released into the ambient water by organisms living in juvenile habitat or may be associated with the substratum itself. Chemosensory and mechanosensory structures in crustaceans are known as sensilla and are hair-like cuticular protrusions that contain sensory cells. In adult crustaceans, sensilla occur mainly on the mouthparts, antennae, antennules, and periopods, but there has been little study of the morphology, physiology, or ontogeny of these structures in brachyuran larvae. Brachyurans achieve competency during the megalopal stage, and it is during this period of competency that megalopae respond to chemical and tactile cues that accelerate or retard the process of metamorphosis. The body of work reviewed here provides strong evidence that watersoluble cues are an important component of the settlement-and-metamorphosis process in brachyuran crabs. There is a generally positive response to cues emanating from natural substratum associated with nursery habitat, and most species also respond strongly to odor from conspecific adults. Response to odors from other species is less common and usually occurs with odors produced by closely related taxa. Odors produced by co-occurring plant species are also important, and a positive response was seen in six of the seven species tested. Response to tactile cues has been less well documented because much of the available data fails to distinguish effects of the substratum itself from associated water-soluble cues. Tactile cues, however, have been demonstrated clearly for the Asian shore crab, Hemigrapsus sanguineus, where megalopae respond to texture of the substratum on a spatial scale of b1 mm. The generality of this tactile response is unknown, but it is unlikely that megalopae could discriminate among substrata on spatial scales N 1 mm, which approaches the size of the megalopae themselves. There are a number of general conclusions that emerge from our review. First, is the observation that brachyuran larvae are strong swimmers that are able to traverse the entire water column on a time scale of hours in most coastal and estuarine environments. Moreover, this swimming behavior occurs in response to the constancy in the Earth's gravity and to the depth-related variation in hydrostatic pressure and light. This set of circumstances permits larvae to undergo diel vertical migration with its attendant advantages concerning predator-prey interactions. Likewise, the strong swimming ability of brachyuran larvae allows them to take advantage of vertical shear in horizontal currents and to exert some control over their horizontal transport. This is particularly apparent in estuarine species that migrate vertically at tidal frequency wherein larval forms can cover kilometer-scale distances in a single tidal cycle. In contrast, larval transport in the coastal ocean is

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often dominated by physical factors, and swimming has a less important role in mediating horizontal movement. In addition, the results of recent modeling studies have shown that trajectories of larvae often depend strongly on the timing and location of larval release in both coastal and estuarine environments. And finally, the literature shows a common metamorphic response of brachyuran megalopae to chemical and physical cues associated with benthic juvenile habitat. These cues, however, are undetectable beyond a few meters from a settlement site and are not important until the megalopae have actually arrived at the site. Accordingly, the transport process itself is dominated by the interaction between vertical swimming behavior and physical processes in the water column, and is not mediated by chemical cues. Acknowledgements Preparation of this review was supported by funds from the Delaware Sea Grant College Program (RHCE6 DESG and RHCE21 DESG) and the School of Marine Science and Policy at the University of Delaware. C.C. Epifanio (Texas A&M University) provided helpful suggestions concerning mathematical modeling and fluid dynamics [SS]. References Amaral, V., Queiroga, H., Skov, M., Paula, J., 2007. Planktonic availability and settlement of Carcinus maenas megalopae at high temporal resolution in the lower Mira Estuary (SW Portugal). Mar. Ecol. Prog. Ser. 348, 239–248. Anderson, J.A., Epifanio, C.E., 2009. Induction of metamorphosis in the Asian shore crab Hemigrapsus sanguineus: characterization of the cue associated with biofilm from adult habitat. J. Exp. Mar. Biol. Ecol. 382, 34–39. Anderson, J.A., Epifanio, C.E., 2010. Response of the Asian shore crab Hemigrapsus sanguineus to a water-soluble metamorphic cue under natural field conditions. J. Exp. Mar. Biol. Ecol. 384, 87–90. 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Time to metamorphosis of blue crab Callinectes sapidus megalopae: effects of benthic macroalgae. Mar. Ecol. Prog. Ser. 129, 113–118. Campan, R., 1997. Tactic components in orientation. In: Lehrer, M. (Ed.), Orientation and Communication in Arthropods. Birkhäuser, Basel, pp. 1–40. Charpentier, C.L., Cohen, J.H., 2015. Chemical cues from fish heighten visual sensitivity in larval crabs through changes in photoreceptor structure and function. J. Exp. Biol. 218, 3381–3390. Christy, J.H., 1989. Rapid development of megalopae of the fiddler crab Uca pugilator reared over sediment: implications for models of larval recruitment. Mar. Ecol. Prog. Ser. 57, 259–265. Christy, J.H., 2011. Timing of hatching and release of larvae by brachyuran crabs: patterns, adaptive significance and control. Integr. Comp. Biol. 51, 62–72. Clancy, M., Epifanio, C.E., 1989. Distribution of crab larvae in relation to tidal fronts in Delaware Bay, USA. Mar. Ecol. Prog. Ser. 57, 77–82. 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