Behavioural responses of infective-stage copepodids of the salmon louse (Lepeophtheirus salmonis, Copepoda:Caligidae) to host-related sensory cues.

The salmon louse (Lepeophtheirus salmonis [Krøyer]) is an ectoparasitic copepod that causes disease in farmed Atlantic salmon (Salmo salar) and may play a role in the decline of some wild salmonid populations. Controlling lice infestations is a major cost for the salmon industry; this has stimulated the pursuit of alternative approaches to controlling them. One such approach involves determining, and then disrupting, the sensory cues used by the parasite to find its host. In this context, we examined the behavioural responses of lice copepodids to light flicker-simulating light reflecting from the sides of the salmon host and/or the shadows cast by fish passing overhead-and water-soluble chemicals released from the skin of the salmon. From these observations, we estimate that visual cues such as those presented here would operate at relatively long range (metres to tens of metres). A diffuse host-related olfactory cue stimulated swimming, however, it remains unclear whether olfactory cues provide directional information. The observations presented herein could be used to disrupt the link between the parasite and host fish, using a large number of traps deployed at a distance from a salmon farm, for example, thereby reducing sea lice infestation pressure.

Early ontogeny of the Atlantic halibut Hippoglossus hippoglossus head.

An ontogenetic sequence of Atlantic halibut Hippoglossus hippoglossus larvae, reared in intensive culture conditions, was cleared and stained and histologically processed to determine normal cranial chondrification for specimens ranging from 0 to 41 days post-hatch (dph). Twenty-six cranial cartilaginous structures were described, at daily intervals post-hatch. The ontogenetic trajectory, composed of alternating steps and thresholds, was interpreted as saltatory. In comparison with other flatfishes, H. hippoglossus exhibits delayed onset of chondrification. From 9 dph onwards, the ontogenetic trajectory resembles more than that of the turbot Psetta maxima than that of the common sole Solea solea or the summer flounder Paralichthys dentatus and winter flounder Pseudopleuronectes americanus. Hippoglossus hippoglossus with the gaping-jaw malformation, common in intensively cultured individuals of this species, were examined histologically. The reason larvae cannot close their mouth, as their yolk-sac resorbs, seems to be related to the fusion of the interhyal to the hyosymplectic and ceratohyal with which it is normally articulated.

Foraging behaviour of larval cod (Gadus morhua) at low light intensities.

The ability to forage at low light intensities can be of great importance for the survival of fish larvae in a pelagic environment. Three-dimensional silhouette imaging was used to observe larval cod foraging and swimming behaviour at three light intensities (dusk ~1.36 × 10-3 W/m2, night ~1.38 × 10-4 W/m2 and darkness ~3.67 × 10-6 W/m2) at 4 different ages from 6 to 53 days post-hatch (dph). At 6 dph, active pursuit of prey was only observed under dusk conditions. Attacks, and frequent orientations, were observed from 26 dph under night conditions. This was consistent with swimming behaviour which suggested that turn angles were the same under dusk and night conditions, but lower in darkness. Cod at 53 dph attacked prey in darkness and turn angles were not different from those under other light conditions. This suggests that larvae are still able to feed at light intensities of 3.67 × 10-6 W/m2. We conclude that larval cod can maintain foraging behaviour under light intensities that correspond to night-time at depths at which they are observed in the field, at least if they encounter high-density patches of prey such as those that they would encounter at thin layers or fronts.

Chemoreception in the salmon louse Lepeophtheirus salmonis: an electrophysiology approach.

The search for effective and long-term solutions to the problems caused by salmon lice Lepeophtheirus salmonis (Krøyer, 1837) has increasingly included biological/ecological mechanisms to combat infestation. One aspect of this work focuses on the host-associated stimuli that parasites use to locate and discriminate a compatible host. In this study we used electrophysiological recordings made directly from the antennule of adult lice to investigate the chemosensitivity of L. salmonis to putative chemical attractants from fish flesh, prepared by soaking whole fish tissue in seawater. There was a clear physiological response to whole fish extract (WFX) with threshold sensitivity at a dilution of 10 . When WFX was size fractionated, L. salmonis showed the greatest responses to the water-soluble fractions containing compounds between 1 and 10 kDa. The results suggest that the low molecular weight, water-soluble compounds found in salmon flesh may be important in salmon lice host choice.

The effect of light on the settlement of the salmon louse, Lepeophtheirus salmonis, on Atlantic salmon, Salmo salar L.

The salmon louse, Lepeophtheirus salmonis, is an ectoparasitic copepod that infests both wild and farmed salmonid fish. Salmon lice are a major disease problem in the farming of Atlantic salmon, Salmo salar L., and the possibility of salmon lice playing a role in the decline of wild anadromous stocks has also been raised. Lepeophtheirus salmonis can detect a range of stimuli (pressure/moving water, chemicals and light) in the external environment. However, the response thresholds to various stimuli, and the spatial and temporal scales over which they operate in the context of host location, are largely unknown. In this context, we attempted to determine whether salmon lice copepodids settle onto hosts more effectively, or at different locations on the fish's body, under different qualities of light. Lice settlement trials were conducted under three lighting conditions; L1: unpolarized under ultraviolet A (UVA)-through visible; L2: unpolarized without UVA (control); L3: 100% linearly polarized without UVA. A dark control was also conducted. No statistically significant difference in lice settlement was found. While changes in light intensity are involved in host detection at spatial scales on the order of metres, the results presented here suggest that it is not the primary sensory modality underlying host location at smaller spatial scales (cm to mm).

Foraging and prey-search behaviour of small juvenile rainbow trout (Oncorhynchus mykiss) under polarized light.

Several fish species appear to be polarization sensitive, i.e. to be able to discriminate a light source's maximum plane of polarization from any other plane. However, the functional significance of this ability remains unclear. We tested the hypothesis that polarized light improves the prey location ability of free-swimming rainbow trout (Oncorhynchus mykiss) in laboratory aquaria. We found that prey location distances increased while the vertical component of prey location angle decreased under polarized compared with unpolarized (diffuse) illumination. The average frequency distribution of the horizontal component of prey location angle was more bimodal under polarized than unpolarized illumination. These results indicate that polarization sensitivity enhances prey location by juvenile rainbow trout.

Ontogenetic changes in visual sensitivity of the parasitic salmon louse Lepeophtheirus salmonis.

The salmon louse, Lepeophtheirus salmonis, is an ectoparasitic copepod of salmonid fishes whose life cycle involves two broadly defined, free-living larval stages, the nauplius and the copepodid. After settling on a host, the copepodid goes through various transformations to become a mobile adult. We recorded swimming responses of free-swimming salmon lice at the naupliar, copepodid and adult stages to the onset (ON) and offset (OFF) of lights of varying spectral irradiance and polarization. Nauplii showed a prominent swim-up OFF response across the spectrum 352-652 nm, but no ON response. Copepodids exhibited a swim-up ON response and a passive (sinking) OFF response across the same spectral range. Adults showed active swim-up responses to both ON and OFF stimuli, although the OFF response was proportionately stronger. The spectral range of the adult ON and OFF responses was the same as that of the copepodids and slightly greater than that of the nauplii, which did not exhibit responses at 652 nm. The absolute sensitivity of copepodids under white light (approx. 10(-13) photons m(2) s(1)) was higher than that of nauplii (approx. 10(-17) photons(-1) m(2 )s, OFF response) and that of adult female lice (approx. 10(-14) photons(-1)m(2)s). This suggests that the naupliar visual system is best suited for detection of shadows (e.g. the host) under a bright light field (daylight hours), while copepodids and adults may be more specialized for host detection at crepuscular periods and during the night, when light levels are low. None of the developmental stages responded to the rotation of the plane of polarized light or exhibited any difference in directed response when polarized light was used in place of diffuse light.

Wavelength-dependent polarization orientation in Daphnia.

The ability to detect and use the polarization of light for orientation is widespread among invertebrates. Among terrestrial insects, the retinula cells that are responsible for polarization detection contain a single visual pigment, either ultraviolet or short (blue) wavelength sensitive. With the exception of a few aquatic insects, the visual pigments underlying polarization sensitivity in aquatic invertebrates have yet to be determined. Here we report that polarotaxis in Daphnia pulex, a freshwater crustacean, is wavelength dependent and most likely mediated by two visual pigments with absorbance maxima in the middle (green) and long wavelength (red) parts of the spectrum. This contrasts with the response of a closely related species, D. magna, in which polarotaxis is wavelength independent and based on a single middle wavelength visual pigment. The visual systems in Daphnia are the first among crustaceans shown to utilize a middle wavelength pigment for polarization detection and, in the case of D. pulex, the first shown to use more than one visual pigment for such a purpose.

The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxine.

Small (< 30 g) juvenile rainbow trout (Oncorhynchus mykiss) possess retinal photoreceptor mechanisms sensitive to ultraviolet (UV), short (S), middle (M), and long (L) wavelengths. During normal development, UV photosensitivity is lost progressively until, by approx. 60 g, individuals are no longer sensitive in the UV. This shift in spectral sensitivity is associated with the disappearance of small accessory corner cones (ACCs) from the retinal photoreceptor cell mosaic: the UV cone mechanism is lost. Exposing small (< 16 g) rainbow trout to the thyroid hormone thyroxine (T4) for a period of 6 weeks induced a precocial loss of the UV cone mechanism that was indistinguishable from the events that occur during normal development. Six weeks after termination of hormone treatment, the same individuals that had lost their UV photosensitivity after exposure to T4 once again possessed a peak in spectral sensitivity at 360 nm. ACCs had reappeared in the retinae of these fish. After 6 weeks of exposure to thyroxine, large (> 90 g) juvenile rainbow trout, which had lost their UV photoreceptor mechanism during normal development, were once again UV photosensitive and ACCs were found in their retinae. These results imply that the UV photoreceptor mechanism, although lost at one point during development, can reappear at another time during the life history of the same individual. Thyroid hormones appear to be involved in both the loss and reappearance of UV photosensitivity.

Optic nerve response and retinal structure in rainbow trout of different sizes.

This study presents evidence of ultraviolet (UV) sensitive, ON center ganglion cells in the fish retina. We determined the spectral sensitivity of ON and OFF responses from the optic nerve mass potential in small (18.0 - 28.5 g) and large (59.5-835 g) rainbow trout, with special reference to UV sensitivity. Under a mid+long-wavelength adapting background, the ON response of small fish revealed the presence of a UV cone mechanism (lambda max 390 nm) which was absent in large specimens. Under similar background conditions, the OFF response of both small and large fish showed one sensitivity peak, dominated by inputs from an M-cone mechanism. An almost complete absence of the accessory corner cones from the retinal mosaic was correlated with the loss of UV sensitivity.

Thyroxine induces a precocial loss of ultraviolet photosensitivity in rainbow trout (Oncorhynchus mykiss, Teleostei).

Small (< 30 g) juvenile rainbow trout (Oncorhynchus mykiss) possess retinal photoreceptor mechanisms sensitive to ultraviolet (UV), short (S), middle (M) and long (L) wavelengths. During normal development, the sensitivity peak of the UV cone mechanism (360 nm) shifts towards the S-wavelengths (to an intermediate lambda max of 390 nm) until, at approx. 60 g, individuals are no longer sensitive in the UV (only a S-wavelength peak at 430 nm remains). This shift in spectral sensitivity is associated with the loss of small accessory corner cones from the retinal photoreceptor cell mosaic. Treating small (< 30 g) rainbow trout with thyroid hormone induced a precocial loss of UV photosensitivity and an associated change in the retinal photoreceptor cell mosaic, identical to the events that occur during normal development.

Correlation between histological and behavioral measures of visual acuity in a zooplanktivorous fish, the white crappie (Pomoxis annularis).

Estimates of visual acuity in a pelagic freshwater zooplanktivorous fish, the white crappie (Pomoxis annularis, Centrarchidae), were made using a behavioral measure, the maximum observed prey pursuit distance (MxPD), and a histological measure, the density of cone cells in the retina. The greatest number of pursuits occurs in the 0-30 degrees wedge of the visual field; 87% of all pursuits occur in the first 40 degrees. The longest pursuits (200 mm) also occur in this area and generally get shorter from 0 to 180 degrees (from forward-directed) in the visual field. Consistent with the behavioral results, the largest number of cone photoreceptors (13,000/mm2) is found in the far temporal retina along the eye's horizontal meridian. Cone cell densities in the corresponding region of the nasal retina are approximately half this value. The number of cones decreases dorsally and ventrally from the horizontal meridian. Although the absolute values of visual acuity calculated from cone cell topography (i.e. MxPDs of 500 mm) are 2-3 times greater than those observed behaviorally (i.e. MxPDs of 200 mm), the trends in visual acuity across the visual field obtained from both measures are consistent. We suggest that overestimates of visual acuity obtained from cone cell counts alone result from this measure's not accounting for, among other properties of the nervous system, cone cell convergence onto ganglion cells and higher brain centers. Behavioral measures of visual acuity are, therefore, likely to yield a more accurate estimate of an animal's visual abilities.

Embryology, ethology and ecology of ontogenetic critical periods in fish.

Overviews of critical period concepts, as they appear at several biological levels, are presented. In embryology, critical periods generally refer to restricted periods in development during which undifferentiated groups of cells can be induced to differentiate. In neurobiology, critical periods are those during which neural circuits are particularly plastic and subject to molding by cellular processes and by experience. The ethological critical period concept advances the idea that an individual's behavioral characteristics can be more strongly influenced by a given event (some stimulus) at one stage of development than at others. For example, this is the period during which young birds imprint upon their parent(s) and learn their species' songs, or during which young salmon imprint to the odor of their home streams. The fisheries science critical period, an ecological concept, refers to a restricted time in the early life history of fish during which there is massive mortality. For many fish, this event is generally considered the primary factor controlling the size of the adult population. The cause of variable mortality between years is thought to be a result of differential food availability and predation during a critical stage in early fish larval development. At each biological level of the critical period, spatial and temporal overlap between the developing organism and specific environmental input is essential. It is likely that critical periods in embryology, neurobiology and ethology are causally interrelated in a hierarchical manner and that they can be manifested as ecological critical periods.(ABSTRACT TRUNCATED AT 250 WORDS)

Flexible search tactics and efficient foraging in saltatory searching animals.

Foraging is one of the most important endeavors undertaken by animals, and it has been studied intensively from both mechanistic-empirical and optimal foraging perspectives. Planktivorous fish make excellent study organisms for foraging studies because they feed frequently and in a relatively simple environment. Most optimal foraging studies of planktivorous fish have focused, either on diet choice or habitat selection and have assumed that these animals used a cruise search foraging strategy. We have recently recognized that white crappie do not use a cruise search strategy (swimming continuously and searching constantly) while foraging on zooplankton but move in a stop and go pattern, searching only while paused. We have termed thissaltatory search. Many other animals move in a stop and go pattern while foraging, but none have been shown to search only while paused. Not only do white crappie search in a saltatory manner but the components of the search cycle change when feeding on prey of different size. When feeding on large prey these fish move further and faster after an unsuccessful search than when feeding on small prey. The fish also pause for a shorter period to search when feeding on large prey. To evaluate the efficiency of these alterations in the search cycle, a net energy gain simulation model was developed. The model computes the likelihood of locating 1 or 2 different size classes of zooplankton prey as a function of the volume of water scanned. The volume of new water searched is dependent upon the dimensions of the search volume and the length of the run. Energy costs for each component of the search cycle, and energy gained from the different sized prey, were assessed. The model predicts that short runs produce maximum net energy gains when crappie feed on small prey but predicts net energy gains will be maximized with longer runs when crappie feed on large prey or a mixed assemblage of large and small prey. There is an optimal run length due to high energy costs of unsuccessful search when runs are short and reveal little new water, and high energy costs of long runs when runs are lengthy. The model predicts that if the greater search times observed when crappie feed on small prey are assessed when they feed on a mixed diet of small and large prey, net energy gained is less than if small prey are deleted from the diet. We believe the model has considerable generality. Many animals are observed to move in a saltatory manner while foraging and some are thought to search only while stationary. Some birds and lizards are, known to modify the search cycle in a manner similar to white crappie.