Detection: mechanoreception
Mechanosensory systems are well developed in pelagic copepods. Antennular (first antenna) mechanoreceptors are capable of exceptional performances in sensitivity to small movements and high frequencies (Yen et al. 1992; Lenz and Yen 1993; Hartline et al. 1996). Mechanoreceptors have been implicated in mediating responsiveness to presence of predators, to prey or food items and to potential mates. Mechanosensors have the advantage of allowing a fast response time. Detection of a predator often occurs at a distance. Copepods can detect and react to both predatory lunges (e.g. Drenner et al. 1978; Wright and O'Brien 1984; Kils 1992) and flow fields of a predator (Tiselius and Jonsson 1990; Yen and Fields 1992). Gill and Crisp (1985) showed that escape responses to a water-jet stimulus were elicited most effectively if presented to the front of the antennule. The distal tips were most sensitive to mechanical stimulation (Gill 1985). Behavioral thresholds for rapidly-developing fluid velocities are 30 mm s-1 or less, comparable to those for mechanoreceptor firing (Hartline et al. 1996). Referred to shear rate (0.015 s-1), this is two orders of magnitude more sensitive than for slowly-developing stimuli (obstacle in flow: Haury et al.1980; suction tube: Fields and Yen 1997b). In the latter situation, many, but not all, mechanosensitivities are greater for species inhabiting environments with lower ambient noise (Fields and Yen 1997b).
Decision: neurobiology of escape
A fundamental need of most startle reflexes is that the delay ("latency" or "reaction time") between the stimulus and the response be short (for general background, see Evasion Behavior page). As a result, the sensorimotor circuit underlying the triggering of such behavior is usually simple. In decapod crustaceans, the most direct circuit consists of a mechanosensory neuron synapsing onto a giant interneuron, which in turn makes electrical synapses with giant motor neurons innervating fast-flexor muscles of the abdomen to produce a tail-flip (review: Wine and Krasne 1982). Additional interneurons are involved in more complex behavioral regulation, including "habituation," the progressive waning of a response to repeated stimulation (e.g. Zucker et al. 1971). Among invertebrates, the physiological basis of habituation has been well-studied in annelids, molluscs and arthropods (e.g. Kandel and Kupferman 1970 for review), including crustaceans (e.g. Krasne 1969; Zucker et al. 1971). It results from plasticity at various sites within the neuromotor system. In many animals, plasticity at the sensory side dominates, leading to habituation being stimulus-specific. Motor-side plasticity in crustaceans is documented, however (Bruner and Kennedy 1970). Anatomical work by Lowe (1935) on Calanus finmarchicus and by Park (1966) on Epilabidocera amphitrites is consistent with neural circuitry found in decapods. The giant fiber system in these two calanoids receives anterior sensory input and innervates both the pereiopod remotor (power stroke) muscles and the dorsal longitudinal muscles responsible for turning movements (Lowe 1935). Given this circuitry and using high-performance values for conduction and synaptic delays in crustacean nervous system the minimum predicted reaction time is ca. 5 msec (Lenz and Hartline 1999).
Neural systems employ various innovations to speed reactions. Chemical synapses are slow (0.5 ms delay), so use of electrical synapses (0.2 ms) reduces delays at synaptic junctions. Such structures (identifiable as "gap junctions" in TEM) have not yet been described in copepods. Utilization of giant axons reduces axial resistance to ionic current and hence speeds nerve-impulse propagation. Giant axons, probably participating in escape responses, have been described anatomically and physiologically in some copepods (Lowe 1935; Park 1966; Yen et al. 1992; Hartline et al. 1996). Myelin is highly effective for reducing reaction times in vertebrates, but it rarely appears in invertebrates (Heuser and Doggenweiler 1966; Günther 1976). This tight, multilayered cellular wrapping of axons yields an order of magnitude gain in the speed of nerve impulse propagation compared to unmyelinated nerve, as well as great savings in energy and space (reviews: Bullock and Horridge 1965; Roots 1984; Morell 1984). At 200 m s-1, the myelinated giant interneurons of pelagic penaeid shrimp hold the record for impulse conduction speed in any animal including vertebrates (Kusano 1966).
The escape jump
Behavioral studies have resolved parts of the escape jump response (e.g., Storch 1929; Strickler 1975; Kerfoot et al. 1980; Browman et al. 1989; Svetlichnyy and Svetlichnyy 1986; Lenz and Hartline 1999).
During escape jumps, a copepod is propelled forward by the metachronal power strokes of the pereiopods, starting with the most posterior (Storch 1929; Strickler 1975; 1985). Each pair of pereiopods is powered by antagonistic promotor and remotor muscle groups (Lowe 1935; Park 1966; Boxshall 1992). Several investigators have used cinematographic methods to measure parameters of the escape responses to a variety of natural predators and predator mimics (Strickler 1975; 1985; Haury et al. 1980; Kils 1992; Browman et al. 1989; Buskey 1994; Trager et al. 1994; Fields and Yen 1997b). They have shown that copepods accelerate within milliseconds to jump speeds of over 500 body lengths per second (BL s-1). Using electrical stimulation to elicit rapid swims, Svetlichnyy (1987) measured maximum forces of 48 dynes generated during the powerstrokes of Calanus helgolandicus. Similar values have been obtained recently in Undinula vulgaris (Lenz and Hartline 1999).
When exposed to ongoing stimulation (e.g. turbulent conditions), copepod escape responses habituate. The value of habituation is that escape responses are energetically costly, and false responses may adversely affect an animal's fitness (e.g. Zaret 1980; Morris et al. 1985; Saiz et al. 1992). Habituation has well-defined characteristics that are similar across a great diversity of metazoans (e.g. Thompson and Spencer 1966 for review). In copepods, recovery of behavioral sensitivity following a single escape occurs within 15 seconds (Herren, Lenz and Hartline, unpublished data). Recovery of sensitivity by primary sensory neurons is much faster (ca. 1 sec: unpublished results). Repeated stimulation, as in turbulent conditions, can result in a more long-term habituation of escape responses (Haury et al. 1980; Marrasé et al. 1990, Hwang et al. 1994).
Copepod interactions with predators
Predation rates may be particularly high in the epipelagic regions of the open oceans, where predator diversity exceeds copepod diversity by a factor of 2 (Hayward and McGowan 1979). The escape jump of a copepod can effectively lower predator capture efficiencies as compared to non-evasive prey (e.g. Browman et al. 1989; Trager et al. 1994; Suchman and Sullivan 1998 ). However, among the calanoids, there are significant differences in predator-evasion strategies. Specifically, when accounting for the difference in the distribution patterns between the Calanoidea and the Auga[tiloidea, Hays et al. (1997) suggest that a superior escape ability, possibly caused by a difference in body form, could explain the ability of the Calanoidea to maintain their location in the epipelagic. In contrast, the Augaptiloidea vertically migrate to lower predation rates (Bollens et al. 1993; Hays et al. 1997).
Several predators are highly selective on specific copepod species and age groups. Examples include: scyphomedusae preying on Acartia adults but less so on copepodids (Narragansett Bay; Suchman and Sullivan 1998), whitings and sand gobies on Temora longicornus (North Sea; Munk and Nielsen 1994); and Euchaeta elongata and Sagitta elegans on Pseudocalanus newmani (Dabob Bay; Ohman 1986, Ohman and Wood 1996). In the latter case, periods of highest mortality rates in P. newmani correlated with the highest abundances of E. elongata and S. elegans. Thus, some calanoids may be preyed upon primarily by a few predators.