Feeding pattern and the visual light environment in ...calocean.icm.csic.es/sites/default/files/PDF/11JFishBiol_(2003... · Feeding pattern and the visual light environment in myctophid

Feeding pattern and the visual light environment in

myctophid fish larvae

A. SABATES*, A. BOZZANO AND I. VALLVEY

Institut de Ciencies del Mar (CMIMA-CSIC), Passeig Marıtim de la Barceloneta37–49, 08003 Barcelona, Spain

(Received 29 January 2003, Accepted 10 September 2003)

The trophic spectrum and feeding pattern of two myctophid larvae, Benthosema glaciale and

Myctophum punctatum, were analysed in relation to changes in daily light intensity. The larvae

of both species live relatively deep, occurring in the first 100m, though distribution of

M. punctatum extends to 150m depth. The present study, carried out in the western Mediterranean

(Alboran Sea), indicated that the larvae of the two species exhibit different foraging strategies.

Both started to feed at dawn, but while feeding ofM. punctatum was high at dawn and dusk, the

feeding of B. glaciale remained high throughout the day. The light intensity profiles taken

during the day indicated that at the depths where the species dwelt, light intensity was enough

to provoke a feeding response. The larvae of these species, in contrast to the majority of fish

larvae, had an enhanced sensitivity due to their pure rod-like retina, an adaptation for foraging

at low light intensities. Both species showed an ontogenetic change in their diet: B. glaciale

preflexion larvae fed mainly on copepod eggs and nauplii, while postflexion larvae consumed

calanoid copepodites; M. punctatum larvae showed a more diversified diet, composed of larger

prey items. The stalked and elongated eye of M. punctatum larvae would enable the detection of

a greater range of prey in terms of shape and size. In addition, the retina of this species was

characterized by a higher summation ratio and longer photoreceptors, indicating a preference

for dimmer environments. This could explain the decreasing feeding activity of M. punctatum

during the high light intensity of the middle daylight hours. As a clear relationship existed

between feeding pattern and light intensity in these myctophid larvae, the visual characteristics

of each species could help to explain the different strategies of foraging behaviour, therefore

avoiding a possible overlap in their trophic niche. # 2003 The Fisheries Society of the British Isles

Key words: feeding; fish larvae; Mediterranean; Myctophidae; vision.

INTRODUCTION

A widespread consensus exists that the magnitude of recruitment in fishes isdetermined during the egg and larvae period, with larval feeding success being akey factor for growth and larval survival (Heath, 1992; Legget & DeBlois,1994). High growth and survival reduce the vulnerability of the larvae topredators that feed on small prey with limited mobility (Houde, 1987; Legget &DeBlois, 1994). Various factors contribute to feeding success, such as the

*Author to whom correspondence should be addressed. Tel.: þ34 932309500; fax: þ34 932309555;

email: [email protected]

Journal of Fish Biology (2003) 63, 1476–1490

doi:10.1046/j.1095-8649.2003.00259.x,availableonlineathttp://www.blackwell-synergy.com

1476# 2003TheFisheries Society of theBritish Isles

concentration and type of food (Hunter, 1981), turbulence (MacKenzie et al.,1994; Dower et al., 1997), temperature (Paul, 1983) and light conditions (Blaxter,1986; Miner & Stein, 1993).Although larvae of some fish species have non-visual senses for feeding (Blaxter,

1969; Batty & Hoyt, 1995), most fish larvae are visual predators (Blaxter, 1986;Batty, 1987; Davis & Olla, 1995; Porter & Theilacker, 1999) and environmentallight conditions represent a key factor in feeding success. The intensity and thespectral quality of light affect larval feeding capabilities by altering prey searchbehaviour, reactive distances and ultimately feeding success itself (Batty, 1987;Huse, 1994). The response of fish larvae to particular light characteristics is speciesspecific and varies with the age of the larva or development stage (Puvanendran &Brown, 1998). It has been reported that fish larval feeding often follows a distinctdiel pattern (Connaughton et al., 1996; Conway et al., 1998; MacKenzie et al.,1999; Hillbruger & Kloppmann, 2000) related to light intensity, with species-specific timing of peak feeding and duration of feeding periods. Even differentpopulations from the same species show different types of foraging, growth andsurvival in relation to the light intensity (Puvanendran & Brown, 1998). Thesestudies, however, have tended to concentrate on species that mainly inhabit surfacewaters during the whole of their life cycle. Consequently, the larvae of deep-seafishes have received less attention (Sabates & Saiz, 2000).Among the deep-sea fishes, the myctophids constitute an important compon-

ent of the oceanic ecosystems due to their high abundance and universaldistribution in all the oceans (Gjosater & Kawaguchi, 1980). Their larvae arevery abundant in plankton, achieving up to 50% of all the larvae collected insamples from the open sea (Moser & Ahlstrom, 1974) and, therefore, playing avery important role in the planktonic food chain. In addition to their highabundance, the myctophid larvae exhibit a high diversity of morphologicaltraits (Moser, 1981). The shape and proportions of the different parts of thebody, as well as the shape and size of the eye, vary markedly in the differentspecies and throughout larval development. This wide variety of morphologicalcharacters and larval adaptations causes interspecific variations in their loco-motive abilities and visual capabilities that might result in different feedingstrategies (Sabates & Saiz, 2000).The glacier lanternfish Benthosema glaciale (Reinhardt) and the spotted

lanternfish Myctophum punctatum Rafinesque are two species of Myctophidae,both included in the subfamily Myctophinae. The larvae of this subfamily arecharacterized by having elongated eyes, unlike the species of the subfamilyLampanyctinae that have rounded eyes (Moser & Ahlstrom, 1974). In addition,the larvae of M. punctatum have their eyes placed on short stalks (Moser &Ahlstrom, 1970). The vertical distribution of the larvae of both species isrelatively deep: B. glaciale occurs between depths of 40 and 110m (Ropke,1989), whereas M. punctatum larvae have a wider distribution range, between25 and 150m (John & Re, 1995; Olivar et al., 1998). The larvae of both speciesare visual predators since they feed during the day (Sabates & Saiz, 2000).The aim of this study was to determine the diet and daytime feeding

behaviour of B. glaciale and M. punctatum larvae, which have a partially over-lapping depth distribution, and to try to account for a visual feeding behaviourin an environment where light could be a limiting factor.

FEEDING PATTERN IN MYCTOPHID FISH LARVAE 1477

# 2003TheFisheries Society of theBritish Isles, Journal of FishBiology 2003, 63, 1476–1490

MATERIALS AND METHODS

FIELD SAMPLING

The research detailed here was part of a wider study on mesoscale features in planktondistribution in the western Alboran Sea (western Mediterranean) carried out from 14 to24 September 1999. The sampling was undertaken at three fixed stations located in atransect perpendicular to the coast (36�000–36�230 N; 4�140–4�160 W). A different stationwas sampled each day at dawn, noon and dusk, and each station was visited three timesduring the cruise. No night fishing was carried out because a preliminary study, under-taken on the same species, demonstrated that the larvae did not feed during the night(Sabates & Saiz, 2000). The fish larvae were collected with a bongo net with a mouthopening 60 cm in diameter and a mesh-size of 333mm. Fishing was carried out from amaximum depth of 200m to the surface, at a ship speed of 3�7 kmh�1 (2 knots). Planktonsamples were preserved in 5% buffered formalin.

Surface incident irradiance was continuously measured with a pyranometer connectedto a Li-Cor LI-1000 data logger. In addition, vertical profiles of photosynthetically activeradiation (PAR, 400–700 nm) were obtained with a Li-Cor spherical quantum sensorattached to a Seabird 25 CTD system. Light intensity profiles were measured from thesea surface down to a depth of 50m at 0900, 1030 and 1700 hours (GMT) on differentoccasions during the cruise. In the present study, only profiles corresponding to thehighest environmental light intensity were considered. The extinction coefficient K wascalculated using Beer’s Law: Iz¼ I0 � e�kz, where Iz is the intensity of light at depth z, I0 isthe intensity of light at the surface and k is the extinction coefficient. In order to obtainlight intensity profiles for the whole depth distribution range of the Myctophidae larvaestudied (to 150m), the extinction coefficient k was calculated for depths >50m using theregression curve obtained for the values measured with the Li-Cor sensor, and the resultwas applied to extrapolated light intensity down to 150m. The light intensity profile at0700 hours was obtained from the surface irradiance value (218�5mmol s�1m�2) meas-ured by the pyranometer connected to the Li-Cor LI-1000 data logger.

LABORATORY ANALYSIS

In the laboratory, all fish larvae were sorted from the bongo samples. The bulk of theselarvae corresponded to mesopelagic species from the family Myctophidae, with B. glacialeand M. punctatum being most abundant, since they represented 53% of the total fishlarvae collected.

Gut contents analysis was conducted on both species. Prior to dissection, the fishlarvae standard length (LS) was measured (to the nearest 0�1mm) from the tip of thesnout to the end of the notochord in preflexion and flexion larvae, and from the tip of thesnout to the posterior margin of the hypural plate in postflexion larvae. For the study ofthe gut contents, a maximum of 40 individuals per sample was analysed. The digestivetract, including the stomach and gut, were dissected with fine needles and any prey itemsfound were identified and counted.

Feeding incidence, the proportion of feeding larvae, and the mean number of fooditems per gut (using only feeding larvae) were calculated per each larval size range.Differences in mean number of prey between size groups were tested using one-factorANOVA. One-way ANOVA was also performed to analyse the effect of daytime onfeeding incidence. If significant differences were found, a Tukey–Kramer multiple com-parison test was used to identify group differences.

Histological analysis of the retinal structure was carried out on two postflexion larvaeof B. glaciale (7�2 and 7�3mm LS) and M. punctatum (9�7 and 10�3mm LS). The sizesrepresented a similar development stage in both species, since notochord flexion takesplace at c. 6mm in B. glaciale, while in M. punctatum it occurs at larger sizes, c. 7�8mm.The individuals, fixed on board, were stored in 70% alcohol. The dorso-ventraland rostro-temporal eye diameters were measured under light microscopy prior toembedding. No correction was applied for fixation shrinkage. The individuals were

1478 A. SABATES ET AL .

# 2003TheFisheries Society of the British Isles, Journal of FishBiology 2003, 63, 1476–1490

subsequently dehydrated in an ethanol series and embedded in Historesin (Leica).Transverse semi-thin sections (2 mm) were cut on a Reichert-Jung microtome and stainedwith methylene blue and basic fuchsin. For both species, the lenses were measured in thesections until they reached their maximum diameter, and in these sections (five for eachlarva) measurements of the retina were taken using an Optimas 6.0 image analyser.Photoreceptor cell type was examined under light microscopy. In each section obtainedfrom the dorso-temporal area of the retina, 15 measurements were taken for all theretinal layers: photoreceptor outer segment (OS), outer nuclear layer (ONL), innernuclear layer (INL), inner plaxiform layer (IPL) and ganglion cell layer (GCL). Anystatistical differences between intra- and interspecific retinal measurements were deter-mined by a t-test.In the four larvae examined, photoreceptors and ganglion cells were counted in the

dorso-temporal retina under light microscopy at �1000 magnification. In order to limitthe error due to the retinal curvature, counts were made in two linear transects of 50mmin three serial sections far from the optic disc. Cell density was calculated using Van derMeer & Anker (1986) equation: density¼ 106m [( tþ d� 2f ) w]�1 cells permm2, where mis the mean number of cells counted, t is the section thickness, d is the mean diameter ofthe cells, f is the thickness of the smallest cell fragments counted ( f¼ 0�1d ) and w is thewidth of the sampled strip.

RESULTS

The stomach contents were examined from a total of 542 B. glaciale and 186M. punctatum larvae. The size frequency distributions for the dissected larvaeof both species are shown in Fig. 1. The range of sizes was between 2–10mm inB. glaciale and 3�5–14mm in M. punctatum.

FEEDING INCIDENCE AND DIET COMPOSITION

In general, the feeding incidence was relatively low during the samplingperiod. Nevertheless, in both species the incidence increased with larval growth(Fig. 2), and it was 100% in the largest sized M. punctatum larvae examined. InB. glaciale, the average number of prey items per larva was quite constant(mean� S.D. 1�2� 0�5) up to 8mm LS, and increased significantly (2�6� 1�6) inthe 8–10mm larvae (ANOVA, d.f.¼ 3 and 115, P< 0�001) (Fig. 3). InM. punctatum, the average number of prey items per larva increased progres-sively as development progressed (from 1�2� 0�4 to 2�2� 1�8). Nevertheless, nosignificant differences were observed among the size ranges considered(ANOVA, d.f.¼ 5 and 38, P¼ 0�35) (Fig. 3), probably due to the high vari-ability in the number of prey (one to seven per larva) detected in the largestlarvae examined.The diet composition analysis of both species showed that the preflexion

B. glaciale larvae were feeding mainly on small sized prey, such as eggs and naupliiof copepods (which represented >50% of the composition of the diet) (Fig. 4).Copepodites and cladocerans, however, also represented an important part ofthe diet. In the flexion and postflexion larvae, >6mm, the most abundant preywere calanoid copepodites and the larvae of other crustaceans. Adult copepodsand ostracods also appeared in the diet, while the proportion of nauplii andcladocerans decreased noticeably. In the preflexion M. punctatum larvae, thediet was not particularly varied and was dominated by calanoid copepodites. Inthe flexion and postflexion larvae, >7�5mm, the diet was more diversified, with



cyclopoid copepodites, ostracods and other crustaceans appearing, although themain component of the diet were the calanoid copepodites (Fig. 4).

DAYTIME FEEDING PATTERNS

The light intensity profiles taken at 0700, 0900, 1030 and 1700 hours (GMT)from the surface down to a depth of 150m are shown in Fig. 5. At a depthof 80m, where the distribution ranges of both species overlap, the light inten-sity was 0�2� 10�2mmol s�1m�2 at 0700 hours and 4 mmol s�1m�2 at 1030hours, whereas in the afternoon, at 1700 hours, it decreased again to5� 10�2 mmol s�1m�2.The feeding incidence at different times of the day in relation to the light

intensity is shown in Fig. 6. Both species had different feeding patterns inrelation to the light intensity. In B. glaciale, the feeding incidence was relatively

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FIG. 1. Length frequency distribution of (a) Benthosema glaciale and (b) Myctophum punctatum larvae

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high at dawn, remained high during the day, at high light intensities, anddecreased slightly at dusk. No significant differences were observed, howeverin the feeding incidence at different times of day (ANOVA, d.f.¼ 3 and 8,P¼ 0�75). The M. punctatum larvae showed a high incidence at dawn, whichdecreased noticeably at high light intensities and then increased again towardsthe end of the day. Significant differences were found in the incidence of feeding

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FIG. 3. Relationship between feeding incidence and standard length in (a) Benthosema glaciale and

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FIG. 4. Per cent frequency of total prey type consumed by (a) Benthosema glaciale preflexion larvae

(2–6mm) and flexion and postflexion larvae (>6mm) and (b) Myctophum punctatum preflexion

larvae (3–7�5mm) and flexion and postflexion larvae (>7�5mm).

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FIG. 5. Vertical profile of light irradiance at 0700 (&), 0900 ( ), 1030 (n) and 1700 (*) hours GMT. ,

the threshold feeding sensitivity (1�85� 10�3 mmol s�1m�2) for teleosts fish larvae proposed by

Blaxter (1986).



in relation with daytime (ANOVA, d.f.¼ 3 and 8, P¼ 0�013). The correspond-ing Tukey post-hoc pair-wise comparison of probabilities showed that theincidence of feeding at dawn (0700 hours) and at noon (1200 hours) weresignificantly different (P¼ 0�016).

HISTOLOGICAL ANALYSIS OF THE RETINAL STRUCTURE

Although both species had elongated eyes, those of M. punctatum werenarrower and placed on short stalks. Both species showed a conical choroidtissue at the ventral surface of the eye, but it was more developed inM. punctatum. The measurements of eye and lens diameter are indicated inTable I and they show that the eye of M. punctatum was at least 13% longerthan the eye of B. glaciale.The retinae of B. glaciale andM. punctatum were characterized by one layer of

photoreceptors that had a thin elongated outer segment ( c. 1�6 mm in width), nodifference in shape between them and darkly staining nuclei (Fig. 7). Accordingto Welch & Pankhurst (2001), these characteristics correspond presumably torod-like photoreceptors. In addition, an inward (towards the lens) invaginationof pigment epithelium was evident in both species.

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FIG. 6. Mean� S.E. feeding incidence of (a) Benthosema glaciale and (b) Myctophum punctatum larvae at

different times of the day, and mean� S.E. incident irradiance during the sampling period.



The whole retinal thickness, as well as the thickness of all the retinal layers,was measured in the four larvae examined. Since no significant differences wereobserved between the pairs of the same species, comparison between species wasperformed. The retinal thickness of M. punctatum measured 121�5� 26�5mm(mean� S.D.), which was 6% wider than the retina of B. glaciale that reached113�9� 24�8 mm. No significant difference, however, was detected between theretinal thickness of the two species. When interspecific comparisons were per-formed between the same retinal layer, significant differences were found only inthe photoreceptor outer segment (OS) (t-test, n¼ 300, P¼ 0�015) and in theganglion cell layer (GCL) (t-test, n¼ 300, P¼ 0�05). In M. punctatum, the meanOS length measured 32mm, which was 11% longer than B. glaciale, and theganglion cell layer measured 22mm, which was 10�5% wider than in B. glaciale.In both species, a specialized region of longer photoreceptors was observed in

the postero-ventral retina and significant differences (t-test, n¼ 300, P¼ 0�02)occurred in OS length between this region and the other retinal sectors. Inthis region, OS was 40 and 35mm in M. punctatum and B. glaciale, respectively.The photoreceptor density was higher in the M. punctatum retina(c. 1�9� 105 cellmm�2), while the ganglion cell density was similar in bothspecies (Table I), indicating an enhanced sensitivity of M. punctatum due tothe higher summation ratio of its retina.

DISCUSSION

The current study has demonstrated that the larvae of B. glaciale andM. punctatum show different foraging strategies regarding the types of prey

TABLE I. Morphological characteristics of the eye and the retina (mean� S.D.) in Benthosemaglaciale and Myctophum punctatum larvae

B. glaciale M. punctatum

LS (mm) 7�20 7�30 9�70 10�30Nasal-caudal eye diameter (mm) 0�46 0�48 0�46 0�46Dorso-ventral eye diameter (mm) 0�58 0�54 0�69 0�75Lens size (mm) 0�21 0�20 0�24 0�21Retina width (mm) 117�5� 1�8 118�4� 2�2 123�9� 2�0 126�4� 2�4Photoreceptor outer segment

(OS) (mm)29�2� 1�2 28�5� 1�6 32�8� 1�9 32�0� 0�7

Photoreceptor myoid (mm) 7�2� 0�5 6�4� 0�6 6�6� 0�4 6�3� 0�7Outer nuclear layer (ONL) (mm) 11�7� 1�3 11�1� 0�7 8�7� 1�1 9�1� 1�8Outer plexiform layer (OPL) (mm) 3�5� 0�3 3�1� 0�3 3�5� 0�4 3�9� 0�3Inner nuclear layer (INL) (mm) 20�5� 0�6 19�9� 0�8 21�4� 1�0 22�2� 0�7Inner plexiform layer (IPL) (mm) 21�5� 0�3 22�1� 0�4 23�2� 0�3 23�9� 0�3Ganglion cell layer (mm) 19�4� 2�4 20�5� 1�0 21�8� 1�8 22�9� 2�2Fibres (mm) 4�5� 0�3 4�8� 0�4 5�9� 0�2 6�1� 0�3Photoreceptor density (cellmm�2) 1�4� 105 1�7� 105 1�9� 105 1�9� 105

Ganglion cell density (cell mm�2) 2�5� 104 3�2� 104 2�9� 104 3�0� 104

Summation ratio (photoreceptors:ganglion cells)

5�5 5�2 6�3 6�5



and environment light intensity. The B. glaciale preflexion larvae primarily feedon copepod eggs and nauplii. The copepod nauplii are the most abundant preyitem in the first larval development phases of numerous fish species (Hunter,1981; Dagg et al., 1984), since these larval stages feed on the abundant andsmall sized prey. Although the copepod eggs were also found in importantproportions, it has been suggested that they can resist digestion inside thedigestive tract and for this reason their abundance can be overestimated(Conway et al., 1994). Unlike the larvae of B. glaciale, the preflexion larvae ofM. punctatum scarcely feed on copepod eggs and nauplii and their diet is mainlycomposed of larger sized prey, such as calanoid copepodites. Sabates & Saiz(2000) have already described that the larvae of different Myctophiformesspecies actively select certain sizes of prey and that this selection is related tomorphological interspecific differences, such as the mouth size, which is rela-tively large in M. punctatum larvae. As development progresses, the diet of thepostflexion larvae diversifies and their feeding preferences are directed towardslarger sized prey. This is especially evident in the M. punctatum larvae that havea diet composed of a high number of different prey types.The increase in feeding incidence, number of prey in gut and variety of prey

ingested in both species as larval development progresses, is a common featurein fish larvae (Arthur, 1976; Anderson, 1994). Throughout ontogeny, the prey-searching ability of fish larvae and the capture efficiency increase as the mouthsize of the larva enlarge, as well as the motor and sensory capacities develop(Hunter, 1981; Young & Davis, 1990). This allows the larger sized fish larvae todiscriminate between a greater number of prey organisms and to select theirprey actively from a variety of prey items (Jenkins, 1987). The selectivity can beinfluenced by the encounter rates, prey visibility, capturability, fine scale dis-tribution of the predator and prey, and the preferences of the predator (Jenkins,1987). Due to the fact that the larvae are visual predators, their capacity todetect prey is closely related to the variability of light intensity during the dayand with the morphology of the eye.Previous studies have shown a distinct diel foraging pattern in larvae of

different fish species such as haddock Melanogrammus aeglefinus (L.), codGadus morhua L., blue whiting Micromesistius poutassou (Risso) or Japanese

(a)

(b)OS

OS

ONL10 µm 10 µm

FIG. 7. Light micrographs of the radial sections of the retina of (a) Myctophum punctatum (10�2mm LS)

and (b) Benthosema glaciale (7�2mm LS), showing the photoreceptor outer segments (OS) and the

outer nuclear layer (ONL).



Spanish mackerel Scomberomorus niphonius (Cuvier) in various geographicalareas (Kane, 1984; McLaren & Avendano, 1995; McLaren et al., 1997; MacKenzieet al., 1999; Shoji et al., 1999; Hillbruger & Kloppmann, 2000). These studiesconfirm that the highest incidences of feeding occur at or shortly after sunset.Active feeding at dusk would allow the fish larvae to store energy before theystop feeding during the night. Nevertheless, little is known about diel feedinghabits in larvae of mesopelagic species that are located at greater depths in thewater column. The present study has demonstrated that the fish larvae thatinhabit relatively deep waters are also subject to daily light cycles, showingdifferent diel periods for feeding incidence. In B. glaciale, the incidence offeeding increases at sunrise to reach a maximum at midday and then decreasesbefore sunset. On the other hand, the larvae of M. punctatum show a highincidence at dawn that decreases during midday, showing a new increasetowards the end of the day. Blaxter (1986) and Batty (1987) demonstratedthat for fish larvae whose feeding is visually mediated, a minimum light inten-sity in the water column is required to detect and capture prey organisms.Consequently, the vertical distribution of fish larvae will be determined by theexponential decrease in the light intensity by depth and the lower limit willbe determined by the minimum light intensity at which feeding is possible.This relationship will vary for every species. Blaxter (1986) indicated thatmost teleost larvae have a threshold feeding sensitivity at c. 0�1 lux(1�8� 10�3 mmol s�1m�2). Subsequent studies have indicated a feeding responseat a higher threshold light intensity level in larvae of striped trumpeter Latrislineata (Forster) (0�1–10mmol s�1m�2) (Cobcroft et al., 2001) and in larvae ofvarious tropical fish species (10 mmol s�1m�2) (Job & Bellwood, 2000). On theother hand, Huse (1994) observed low thresholds at 1�8� 10�3 mmol s�1m�2 inthe larvae of plaice Pleuronectes platessa L. and turbot Scophthalmus maximus(L.). All these studies, however, were carried out in controlled laboratoryconditions.In the present study, the levels of light observed in September between

depths of 40 and 80m, where the larvae of B. glaciale and M. punctatumare mainly located (Ropke, 1989; Olivar et al., 1998), are higher than1�8� 10�3 mmol s�1m�2 (0�1 lux) during the diurnal period. Values of1�8� 10�3 mmol s�1m�2 are reached at 0700 and 1700 hours for depths of 80and 120m, respectively. At midday, the intensity of available light at thesedepths is even higher and the value of 1�8� 10�3 mmol s�1m�2 is reached at235m. Consequently, it would be logical to assume that the larvae of the speciesstudied have a sufficient quantity of light to stimulate a visual response at thedepths they inhabit.In addition, the eyes of these fish larvae show a pure rod-like retina and a

invagination of pigment epithelium indicating, firstly, a possible specializationfor scotopic vision and secondly the need to control the amount of light reach-ing the retina. Pure rod-like retinas were also observed by Pankhurst (1987) inthe larvae of the lanternfish Lampanyctodes hectoris (Gunther) which mainlydwell in the upper levels of the water column (0–20m depth) (Olivar et al.,1992). These larvae have photoreceptors with >50% shorter OS than the OSmeasured in the present study in deeper larvae of M. punctatum and B. glaciale.In addition, the summation ratio of 5�2 calculated in L. hectoris is fairly similar



to the summation ratio found in B. glaciale, but lower than the summation ratioof M. punctatum. This difference in scotopic sensitivity of M. punctatum couldallow this species to detect prey at higher depth or in dimmer light.In any case, pure rod retinae are very unusual in fish larvae, since the

majority of larvae have a pure cone retina in the first development phases(Blaxter & Staines, 1970). In clupeid species, such as the herring Clupeaharengus L. (Blaxter & Jones, 1967) and the South American pilchard Sardinopsmelanostictus (Jenyns) (Matsuoka, 1999), a pure cone retina up to 22 and 20mmLS, respectively has been reported. Pure rod retinae were found by Pankhurst(1984) in the larva of the European eel Anguilla anguilla (L.), and by Blaxter &Staines (1970) and Locket (1980) in some deep species, such as nine lepto-cephalus eels of 80mm, a deep-sea macruridae larvae of 17mm, and a 29mmindividual of the viperfish Chauliodus sloanei Bloch & Schneider. Therefore,presumably, a pure rod retina is a suitable adaptation for larvae that live in adim light environment. Deep-sea fishes, which remain at low levels of illumin-ation, have a pure rod retina in the adult phase and it might be assumed thatthe larvae of these species also have pure rod retina.Even if B. glaciale and M. punctatum do not show great differences in retinal

characteristics, specific features found in their visual system could explaincertain differences observed in their diet and feeding pattern. The stalked eyesof M. punctatum larvae permit them to scan a greater volume of water (Weihs &Moser, 1981) and its elongated form allows focused images to be projected onthe dorso-ventral parts of the retina. With these characteristics, therefore, thelarvae can detect a greater range of prey in terms of shape and size. In addition,the presence of longer photoreceptors and higher summation ratio in M. punctatummay indicate a preference for dimmer environments. It could explain thedecreasing feeding activity of this species in relation to a constraining higherlight intensity in the middle daylight hours. The decrease in feeding success athigh light intensities has been reported in other species, such as cod andhaddock (Huse, 1994; Downing & Litvak, 2001). According to Downing &Litvak (2001), high light intensities may create excessive reflectance that coulddiminish the contrast of prey in relation to the background.From the results of this study high sensitivity seems to be the main visual

characteristic of B. glaciale and M. punctatum in anticipation of migration todeeper waters where the adults of both species are found (Badcock & Merrett,1976). Both species show longer rod-like photoreceptor especially in the ventralsector of their retina. This retinal area receives light from above and longerphotoreceptors ensure a better visual sensitivity for an upward view. As Herring(1996) pointed out, the upward view is characteristic of fishes living in the upperfew hundred metres where light is highly directional. The ventral specializationof the retina could indicate that the main visual axis points in the dorsaldirection of the fishes, where these species can detect the contrast and themovement of their prey.In conclusion, there is a clear relationship between light intensity and feeding

behaviour in the two myctophid fish larvae studied. Taking into account thepartial overlap in their depth distribution, the visual capabilities could help toexplain the different strategies of foraging behaviour, therefore avoiding apossible overlap in their trophic niches.



The authors would like to thank C. Rodgers for kindly reviewing the final Englishversion. We thank two anonymous reviewers for their accurate and constructive criti-cisms on an earlier version of the manuscript. We thank M. Estrada for providingthe data on light intensity profiles. This work was supported by the European Unionin the framework of the MAST Program (MAS-CT96-0051) and by a Spanish grant(MAR 99-1202).

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