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Journal of Fish Biology (2003) 63, 1476–1490
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Feeding pattern and the visual light environment in
myctophid fish larvae
A. S A B A T É S *, A. B O Z Z A N O
AND
I. V A L L V E Y
Institut de Cie`ncies del Mar (CMIMA-CSIC), Passeig Marı´tim de la Barceloneta
37–49, 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 100 m, though distribution of
M. punctatum extends to 150 m 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 of M. 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
# 2003 The Fisheries Society of the British Isles
avoiding a possible overlap in their trophic niche.
Key words: feeding; fish larvae; Mediterranean; Myctophidae; vision.
INTRODUCTION
A widespread consensus exists that the magnitude of recruitment in fishes is
determined during the egg and larvae period, with larval feeding success being a
key factor for growth and larval survival (Heath, 1992; Legget & DeBlois,
1994). High growth and survival reduce the vulnerability of the larvae to
predators 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]
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FEEDING PATTERN IN MYCTOPHID FISH LARVAE
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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 environmental
light conditions represent a key factor in feeding success. The intensity and the
spectral quality of light affect larval feeding capabilities by altering prey search
behaviour, reactive distances and ultimately feeding success itself (Batty, 1987;
Huse, 1994). The response of fish larvae to particular light characteristics is species
specific 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 distinct
diel pattern (Connaughton et al., 1996; Conway et al., 1998; MacKenzie et al.,
1999; Hillbruger & Kloppmann, 2000) related to light intensity, with speciesspecific timing of peak feeding and duration of feeding periods. Even different
populations from the same species show different types of foraging, growth and
survival in relation to the light intensity (Puvanendran & Brown, 1998). These
studies, however, have tended to concentrate on species that mainly inhabit surface
waters during the whole of their life cycle. Consequently, the larvae of deep-sea
fishes have received less attention (Sabatés & Saiz, 2000).
Among the deep-sea fishes, the myctophids constitute an important component of the oceanic ecosystems due to their high abundance and universal
distribution in all the oceans (Gjosater & Kawaguchi, 1980). Their larvae are
very abundant in plankton, achieving up to 50% of all the larvae collected in
samples from the open sea (Moser & Ahlstrom, 1974) and, therefore, playing a
very important role in the planktonic food chain. In addition to their high
abundance, the myctophid larvae exhibit a high diversity of morphological
traits (Moser, 1981). The shape and proportions of the different parts of the
body, as well as the shape and size of the eye, vary markedly in the different
species and throughout larval development. This wide variety of morphological
characters and larval adaptations causes interspecific variations in their locomotive abilities and visual capabilities that might result in different feeding
strategies (Sabatés & 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 are
characterized by having elongated eyes, unlike the species of the subfamily
Lampanyctinae 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 is
relatively deep: B. glaciale occurs between depths of 40 and 110 m (Röpke,
1989), whereas M. punctatum larvae have a wider distribution range, between
25 and 150 m (John & Ré, 1995; Olivar et al., 1998). The larvae of both species
are visual predators since they feed during the day (Sabatés & 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 overlapping depth distribution, and to try to account for a visual feeding behaviour
in an environment where light could be a limiting factor.
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 1476–1490
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A . S A B A T É S E T A L .
MATERIALS AND METHODS
FIELD SAMPLING
The research detailed here was part of a wider study on mesoscale features in plankton
distribution in the western Alboran Sea (western Mediterranean) carried out from 14 to
24 September 1999. The sampling was undertaken at three fixed stations located in a
transect perpendicular to the coast (36 000 –36 230 N; 4 140 –4 160 W). A different station
was sampled each day at dawn, noon and dusk, and each station was visited three times
during the cruise. No night fishing was carried out because a preliminary study, undertaken on the same species, demonstrated that the larvae did not feed during the night
(Sabatés & Saiz, 2000). The fish larvae were collected with a bongo net with a mouth
opening 60 cm in diameter and a mesh-size of 333 mm. Fishing was carried out from a
maximum depth of 200 m to the surface, at a ship speed of 37 km h1 (2 knots). Plankton
samples were preserved in 5% buffered formalin.
Surface incident irradiance was continuously measured with a pyranometer connected
to a Li-Cor LI-1000 data logger. In addition, vertical profiles of photosynthetically active
radiation (PAR, 400–700 nm) were obtained with a Li-Cor spherical quantum sensor
attached to a Seabird 25 CTD system. Light intensity profiles were measured from the
sea surface down to a depth of 50 m at 0900, 1030 and 1700 hours (GMT) on different
occasions during the cruise. In the present study, only profiles corresponding to the
highest environmental light intensity were considered. The extinction coefficient K was
calculated using Beer’s Law: Iz ¼ I0 ekz, where Iz is the intensity of light at depth z, I0 is
the intensity of light at the surface and k is the extinction coefficient. In order to obtain
light intensity profiles for the whole depth distribution range of the Myctophidae larvae
studied (to 150 m), the extinction coefficient k was calculated for depths >50 m using the
regression curve obtained for the values measured with the Li-Cor sensor, and the result
was applied to extrapolated light intensity down to 150 m. The light intensity profile at
0700 hours was obtained from the surface irradiance value (2185 mmol s1 m2) measured 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 these
larvae corresponded to mesopelagic species from the family Myctophidae, with B. glaciale
and M. punctatum being most abundant, since they represented 53% of the total fish
larvae collected.
Gut contents analysis was conducted on both species. Prior to dissection, the fish
larvae standard length (LS) was measured (to the nearest 01 mm) from the tip of the
snout to the end of the notochord in preflexion and flexion larvae, and from the tip of the
snout to the posterior margin of the hypural plate in postflexion larvae. For the study of
the gut contents, a maximum of 40 individuals per sample was analysed. The digestive
tract, including the stomach and gut, were dissected with fine needles and any prey items
found were identified and counted.
Feeding incidence, the proportion of feeding larvae, and the mean number of food
items 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-factor
ANOVA. One-way ANOVA was also performed to analyse the effect of daytime on
feeding incidence. If significant differences were found, a Tukey–Kramer multiple comparison test was used to identify group differences.
Histological analysis of the retinal structure was carried out on two postflexion larvae
of B. glaciale (72 and 73 mm LS) and M. punctatum (97 and 103 mm LS). The sizes
represented a similar development stage in both species, since notochord flexion takes
place at c. 6 mm in B. glaciale, while in M. punctatum it occurs at larger sizes, c. 78 mm.
The individuals, fixed on board, were stored in 70% alcohol. The dorso-ventral
and rostro-temporal eye diameters were measured under light microscopy prior to
embedding. No correction was applied for fixation shrinkage. The individuals were
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FEEDING PATTERN IN MYCTOPHID FISH LARVAE
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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 stained
with methylene blue and basic fuchsin. For both species, the lenses were measured in the
sections until they reached their maximum diameter, and in these sections (five for each
larva) measurements of the retina were taken using an Optimas 6.0 image analyser.
Photoreceptor cell type was examined under light microscopy. In each section obtained
from the dorso-temporal area of the retina, 15 measurements were taken for all the
retinal layers: photoreceptor outer segment (OS), outer nuclear layer (ONL), inner
nuclear layer (INL), inner plaxiform layer (IPL) and ganglion cell layer (GCL). Any
statistical differences between intra- and interspecific retinal measurements were determined 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 limit
the error due to the retinal curvature, counts were made in two linear transects of 50 mm
in three serial sections far from the optic disc. Cell density was calculated using Van der
Meer & Anker (1986) equation: density ¼ 106 m [( t þ d 2f ) w]1 cells per mm2, where m
is the mean number of cells counted, t is the section thickness, d is the mean diameter of
the cells, f is the thickness of the smallest cell fragments counted ( f ¼ 01d ) and w is the
width of the sampled strip.
RESULTS
The stomach contents were examined from a total of 542 B. glaciale and 186
M. punctatum larvae. The size frequency distributions for the dissected larvae
of both species are shown in Fig. 1. The range of sizes was between 2–10 mm in
B. glaciale and 35–14 mm in M. punctatum.
FE E D I N G I N C I D E N C E A N D DI E T C O M P O S I T I O N
In general, the feeding incidence was relatively low during the sampling
period. Nevertheless, in both species the incidence increased with larval growth
(Fig. 2), and it was 100% in the largest sized M. punctatum larvae examined. In
B. glaciale, the average number of prey items per larva was quite constant
(mean S.D. 12 05) up to 8 mm LS, and increased significantly (26 16) in
the 8–10 mm larvae (ANOVA, d.f. ¼ 3 and 115, P < 0001) (Fig. 3). In
M. punctatum, the average number of prey items per larva increased progressively as development progressed (from 12 04 to 22 18). Nevertheless, no
significant differences were observed among the size ranges considered
(ANOVA, d.f. ¼ 5 and 38, P ¼ 035) (Fig. 3), probably due to the high variability in the number of prey (one to seven per larva) detected in the largest
larvae 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 nauplii
of copepods (which represented >50% of the composition of the diet) (Fig. 4).
Copepodites and cladocerans, however, also represented an important part of
the diet. In the flexion and postflexion larvae, >6 mm, the most abundant prey
were calanoid copepodites and the larvae of other crustaceans. Adult copepods
and ostracods also appeared in the diet, while the proportion of nauplii and
cladocerans decreased noticeably. In the preflexion M. punctatum larvae, the
diet was not particularly varied and was dominated by calanoid copepodites. In
the flexion and postflexion larvae, >75 mm, the diet was more diversified, with
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A . S A B A T É S E T A L .
90
(a)
80
70
60
50
40
30
20
Frequency
10
0
30
2
3
4
5
6
7
8
3
4
5
6
7
9
10 11 12 13 14
(b)
25
20
15
10
5
0
2
8
9
10 11 12 13 14
LS (mm)
FIG. 1. Length frequency distribution of (a) Benthosema glaciale and (b) Myctophum punctatum larvae
examined.
cyclopoid copepodites, ostracods and other crustaceans appearing, although the
main 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 150 m are shown in Fig. 5. At a depth
of 80 m, where the distribution ranges of both species overlap, the light intensity was 02 102 mmol s1 m2 at 0700 hours and 4 mmol s1 m2 at 1030
hours, whereas in the afternoon, at 1700 hours, it decreased again to
5 102 mmol s1 m2.
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 in
relation to the light intensity. In B. glaciale, the feeding incidence was relatively
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FEEDING PATTERN IN MYCTOPHID FISH LARVAE
5
1481
9
(a)
4
3
Prey number
2
10
68
30
4–6
6–8
1
0
2–4
5
8–10
10–12
(b)
12–14
11
4
3
5
2
3
7
2–4
4–6
14
9
6–8
8–10
1
0
10–12
12–14
LS (mm)
FIG. 2. Relationship between prey number (mean S.D.) and standard length in (a) Benthosema glaciale
and (b) Myctophum punctatum larvae. Sample size per length group is indicated.
high at dawn, remained high during the day, at high light intensities, and
decreased slightly at dusk. No significant differences were observed, however
in the feeding incidence at different times of day (ANOVA, d.f. ¼ 3 and 8,
P ¼ 075). The M. punctatum larvae showed a high incidence at dawn, which
decreased noticeably at high light intensities and then increased again towards
the end of the day. Significant differences were found in the incidence of feeding
100
(a)
80
60
Per cent feeding
40
20
0
100
2–4
4–6
6–8
8–10
10–12
12–14
(b)
80
60
40
20
0
2–4
4–6
6–8
8–10
10–12
12–14
LS (mm)
FIG. 3. Relationship between feeding incidence and standard length in (a) Benthosema glaciale and
(b) Myctophum punctatum larvae.
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 1476–1490
A . S A B A T É S E T A L .
Cladocera
Cyclopoid
copepodites
Calanoid
copepodites
Prey
Crustaceans
Cladocera
Cyclopoid
copepods
Calanoid
copepods
Cyclopoid
copepodites
Calanoid
copepodites
Eggs
Copepod
nauplii
Postflexion
Others
Ostracoda
Crustaceans
Cladocera
Cyclopoid
copepods
Calanoid
copepods
Copepod
nauplii
Eggs
Others
Cladocera
Cyclopoid
copepod
Calanoid
copepod
Cyclopoid
copepodites
Calanoid
copepodites
Cyclopoid
copepodites
Calanoid
copepodites
Preflexion
(b)
40
35
30
25
20
15
10
5
0
Postflexion
Copepod
nauplii
40
35
30
25
20
15
10
5
0
40
35
30
25
20
15
10
5
0
Preflexion
Copepod
nauplii
Eggs
40 (a)
35
30
25
20
15
10
5
0
Eggs
Per cent frequency prey consumed
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Prey
FIG. 4. Per cent frequency of total prey type consumed by (a) Benthosema glaciale preflexion larvae
(2–6 mm) and flexion and postflexion larvae (>6 mm) and (b) Myctophum punctatum preflexion
larvae (3–75 mm) and flexion and postflexion larvae (>75 mm).
Log light intensity (µmol s–1 m–2)
–8
–6
–4
–2
0
2
4
6
8
0
20
40
Depth (m)
60
80
100
120
140
160
1.85 × 10–3 µmol s–1 m–2
FIG. 5. Vertical profile of light irradiance at 0700 (&), 0900 ( ), 1030 (n) and 1700 (*) hours GMT.
,
the threshold feeding sensitivity (185 103 mmol s1 m2) for teleosts fish larvae proposed by
Blaxter (1986).
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55
50
45
40
35
30
25
20
15
10
5
0
1200
1000
800
600
400
200
0
0400
55
50
45
40
35
30
25
20
15
10
5
0
1400
(a)
0600
0800
1000
1200
1400
1600
1800
2000
2200
1400
(b)
1200
1000
Irradiance (µmol s–1 m–2)
Per cent feeding
FEEDING PATTERN IN MYCTOPHID FISH LARVAE
800
600
400
200
0
0400
0600
0800
1000
1200
1400
1600
1800
2000
2200
Time (hours)
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.
in relation with daytime (ANOVA, d.f. ¼ 3 and 8, P ¼ 0013). The corresponding Tukey post-hoc pair-wise comparison of probabilities showed that the
incidence of feeding at dawn (0700 hours) and at noon (1200 hours) were
significantly different (P ¼ 0016).
H I S T O L O GI C A L A N A L Y S I S O F T H E R E T I N A L S T R U C T U R E
Although both species had elongated eyes, those of M. punctatum were
narrower and placed on short stalks. Both species showed a conical choroid
tissue at the ventral surface of the eye, but it was more developed in
M. punctatum. The measurements of eye and lens diameter are indicated in
Table I and they show that the eye of M. punctatum was at least 13% longer
than the eye of B. glaciale.
The retinae of B. glaciale and M. punctatum were characterized by one layer of
photoreceptors that had a thin elongated outer segment ( c. 16 mm in width), no
difference in shape between them and darkly staining nuclei (Fig. 7). According
to Welch & Pankhurst (2001), these characteristics correspond presumably to
rod-like photoreceptors. In addition, an inward (towards the lens) invagination
of pigment epithelium was evident in both species.
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A . S A B A T É S E T A L .
TABLE I. Morphological characteristics of the eye and the retina (mean S.D.) in Benthosema
glaciale and Myctophum punctatum larvae
B. glaciale
LS (mm)
Nasal-caudal eye diameter (mm)
Dorso-ventral eye diameter (mm)
Lens size (mm)
Retina width (mm)
Photoreceptor outer segment
(OS) (mm)
Photoreceptor myoid (mm)
Outer nuclear layer (ONL) (mm)
Outer plexiform layer (OPL) (mm)
Inner nuclear layer (INL) (mm)
Inner plexiform layer (IPL) (mm)
Ganglion cell layer (mm)
Fibres (mm)
Photoreceptor density (cell mm2)
Ganglion cell density (cell mm2)
Summation ratio (photoreceptors:
ganglion cells)
M. punctatum
720
046
058
021
1175 18
292 12
730
048
054
020
1184 22
285 16
970
046
069
024
1239 20
328 19
1030
046
075
021
1264 24
320 07
72 05
117 13
35 03
205 06
215 03
194 24
45 03
14 105
25 104
55
64 06
111 07
31 03
199 08
221 04
205 10
48 04
17 105
32 104
52
66 04
87 11
35 04
214 10
232 03
218 18
59 02
19 105
29 104
63
63 07
91 18
39 03
222 07
239 03
229 22
61 03
19 105
30 104
65
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 were
observed between the pairs of the same species, comparison between species was
performed. The retinal thickness of M. punctatum measured 1215 265 mm
(mean S.D.), which was 6% wider than the retina of B. glaciale that reached
1139 248 mm. No significant difference, however, was detected between the
retinal thickness of the two species. When interspecific comparisons were performed between the same retinal layer, significant differences were found only in
the photoreceptor outer segment (OS) (t-test, n ¼ 300, P ¼ 0015) and in the
ganglion cell layer (GCL) (t-test, n ¼ 300, P ¼ 005). In M. punctatum, the mean
OS length measured 32 mm, which was 11% longer than B. glaciale, and the
ganglion cell layer measured 22 mm, which was 105% 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, n ¼ 300, P ¼ 002)
occurred in OS length between this region and the other retinal sectors. In
this region, OS was 40 and 35 mm in M. punctatum and B. glaciale, respectively.
The photoreceptor density was higher in the M. punctatum retina
(c. 19 105 cell mm2), while the ganglion cell density was similar in both
species (Table I), indicating an enhanced sensitivity of M. punctatum due to
the higher summation ratio of its retina.
DISCUSSION
The current study has demonstrated that the larvae of B. glaciale and
M. punctatum show different foraging strategies regarding the types of prey
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FEEDING PATTERN IN MYCTOPHID FISH LARVAE
(a)
(b)
OS
OS
10 µm
ONL
10 µm
FIG. 7. Light micrographs of the radial sections of the retina of (a) Myctophum punctatum (102 mm LS)
and (b) Benthosema glaciale (72 mm LS), showing the photoreceptor outer segments (OS) and the
outer nuclear layer (ONL).
and environment light intensity. The B. glaciale preflexion larvae primarily feed
on copepod eggs and nauplii. The copepod nauplii are the most abundant prey
item in the first larval development phases of numerous fish species (Hunter,
1981; Dagg et al., 1984), since these larval stages feed on the abundant and
small sized prey. Although the copepod eggs were also found in important
proportions, it has been suggested that they can resist digestion inside the
digestive tract and for this reason their abundance can be overestimated
(Conway et al., 1994). Unlike the larvae of B. glaciale, the preflexion larvae of
M. punctatum scarcely feed on copepod eggs and nauplii and their diet is mainly
composed of larger sized prey, such as calanoid copepodites. Sabatés & Saiz
(2000) have already described that the larvae of different Myctophiformes
species actively select certain sizes of prey and that this selection is related to
morphological interspecific differences, such as the mouth size, which is relatively large in M. punctatum larvae. As development progresses, the diet of the
postflexion larvae diversifies and their feeding preferences are directed towards
larger sized prey. This is especially evident in the M. punctatum larvae that have
a 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 feature
in fish larvae (Arthur, 1976; Anderson, 1994). Throughout ontogeny, the preysearching ability of fish larvae and the capture efficiency increase as the mouth
size 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 to
discriminate between a greater number of prey organisms and to select their
prey actively from a variety of prey items (Jenkins, 1987). The selectivity can be
influenced by the encounter rates, prey visibility, capturability, fine scale distribution 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 to
detect prey is closely related to the variability of light intensity during the day
and 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.), cod
Gadus morhua L., blue whiting Micromesistius poutassou (Risso) or Japanese
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A . S A B A T É S E T A L .
Spanish mackerel Scomberomorus niphonius (Cuvier) in various geographical
areas (Kane, 1984; McLaren & Avendano, 1995; McLaren et al., 1997; MacKenzie
et al., 1999; Shoji et al., 1999; Hillbruger & Kloppmann, 2000). These studies
confirm 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 they
stop feeding during the night. Nevertheless, little is known about diel feeding
habits in larvae of mesopelagic species that are located at greater depths in the
water column. The present study has demonstrated that the fish larvae that
inhabit relatively deep waters are also subject to daily light cycles, showing
different diel periods for feeding incidence. In B. glaciale, the incidence of
feeding increases at sunrise to reach a maximum at midday and then decreases
before sunset. On the other hand, the larvae of M. punctatum show a high
incidence at dawn that decreases during midday, showing a new increase
towards the end of the day. Blaxter (1986) and Batty (1987) demonstrated
that for fish larvae whose feeding is visually mediated, a minimum light intensity in the water column is required to detect and capture prey organisms.
Consequently, the vertical distribution of fish larvae will be determined by the
exponential decrease in the light intensity by depth and the lower limit will
be determined by the minimum light intensity at which feeding is possible.
This relationship will vary for every species. Blaxter (1986) indicated that
most teleost larvae have a threshold feeding sensitivity at c. 01 lux
(18 103 mmol s1 m2). Subsequent studies have indicated a feeding response
at a higher threshold light intensity level in larvae of striped trumpeter Latris
lineata (Forster) (01–10 mmol s1 m2) (Cobcroft et al., 2001) and in larvae of
various tropical fish species (10 mmol s1 m2) (Job & Bellwood, 2000). On the
other hand, Huse (1994) observed low thresholds at 18 103 mmol s1 m2 in
the larvae of plaice Pleuronectes platessa L. and turbot Scophthalmus maximus
(L.). All these studies, however, were carried out in controlled laboratory
conditions.
In the present study, the levels of light observed in September between
depths of 40 and 80 m, where the larvae of B. glaciale and M. punctatum
are mainly located (Röpke, 1989; Olivar et al., 1998), are higher than
18 103 mmol s1 m2 (01 lux) during the diurnal period. Values of
18 103 mmol s1 m2 are reached at 0700 and 1700 hours for depths of 80
and 120 m, respectively. At midday, the intensity of available light at these
depths is even higher and the value of 18 103 mmol s1 m2 is reached at
235 m. Consequently, it would be logical to assume that the larvae of the species
studied have a sufficient quantity of light to stimulate a visual response at the
depths 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 specialization
for scotopic vision and secondly the need to control the amount of light reaching the retina. Pure rod-like retinas were also observed by Pankhurst (1987) in
the larvae of the lanternfish Lampanyctodes hectoris (Günther) which mainly
dwell in the upper levels of the water column (0–20 m depth) (Olivar et al.,
1992). These larvae have photoreceptors with >50% shorter OS than the OS
measured in the present study in deeper larvae of M. punctatum and B. glaciale.
In addition, the summation ratio of 52 calculated in L. hectoris is fairly similar
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 1476–1490
FEEDING PATTERN IN MYCTOPHID FISH LARVAE
1487
to the summation ratio found in B. glaciale, but lower than the summation ratio
of M. punctatum. This difference in scotopic sensitivity of M. punctatum could
allow 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 Clupea
harengus L. (Blaxter & Jones, 1967) and the South American pilchard Sardinops
melanostictus (Jenyns) (Matsuoka, 1999), a pure cone retina up to 22 and 20 mm
LS, 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 leptocephalus eels of 80 mm, a deep-sea macruridae larvae of 17 mm, and a 29 mm
individual of the viperfish Chauliodus sloanei Bloch & Schneider. Therefore,
presumably, a pure rod retina is a suitable adaptation for larvae that live in a
dim light environment. Deep-sea fishes, which remain at low levels of illumination, have a pure rod retina in the adult phase and it might be assumed that
the 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 explain
certain differences observed in their diet and feeding pattern. The stalked eyes
of 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 on
the dorso-ventral parts of the retina. With these characteristics, therefore, the
larvae 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. punctatum
may indicate a preference for dimmer environments. It could explain the
decreasing feeding activity of this species in relation to a constraining higher
light intensity in the middle daylight hours. The decrease in feeding success at
high light intensities has been reported in other species, such as cod and
haddock (Huse, 1994; Downing & Litvak, 2001). According to Downing &
Litvak (2001), high light intensities may create excessive reflectance that could
diminish 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 to
deeper waters where the adults of both species are found (Badcock & Merrett,
1976). Both species show longer rod-like photoreceptor especially in the ventral
sector of their retina. This retinal area receives light from above and longer
photoreceptors ensure a better visual sensitivity for an upward view. As Herring
(1996) pointed out, the upward view is characteristic of fishes living in the upper
few hundred metres where light is highly directional. The ventral specialization
of the retina could indicate that the main visual axis points in the dorsal
direction of the fishes, where these species can detect the contrast and the
movement 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 the
partial overlap in their depth distribution, the visual capabilities could help to
explain the different strategies of foraging behaviour, therefore avoiding a
possible overlap in their trophic niches.
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 1476–1490
1488
A . S A B A T É S E T A L .
The authors would like to thank C. Rodgers for kindly reviewing the final English
version. We thank two anonymous reviewers for their accurate and constructive criticisms on an earlier version of the manuscript. We thank M. Estrada for providing
the data on light intensity profiles. This work was supported by the European Union
in the framework of the MAST Program (MAS-CT96-0051) and by a Spanish grant
(MAR 99-1202).
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