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RE V I E W
Ontogeny of behaviour in larvae of marine demersal fishes
Jeffrey M. Leis
Received: 13 May 2010 / Revised: 22 July 2010/ Accepted: 23 July 2010 / Published online: 3 September 2010
The Ichthyological Society of Japan 2010
Abstract The development of behaviours that are rele-
vant to larval dispersal of marine, demersal fishes is poorlyunderstood. This review focuses on recent work that
attempts to quantify the development of swimming, ori-
entation, vertical distribution and sensory abilities. These
behaviours are developed enough to influence dispersal
outcomes during most of the pelagic larval stage. Larvae
swim in the ocean at speeds similar to the currents found in
many locations and at 315 body lengths per second
(BL s-1), although, based on laboratory measurements,
species from cold environments swim slower than those
from warm environments. At least in warm-water species,
larvae swim in an inertial hydrodynamic environment for
most of their pelagic period. Unfed swimming endurance is
[10 km from about 810 mm, and reaches more than
50 km before settlement in several species. Larval fishes
are efficient swimmers. In most species, a large majority of
larvae have orientated swimming in the ocean, but the
precision of orientation does not improve with growth.
Swimming direction of the larvae frequently changes
ontogenetically. Vertical distribution changes ontogeneti-
cally in most species, and both ontogenetic ascents and
descents are found. Development of schooling is poorly
understood, but it may influence speed, orientation and
vertical distribution. Sensory abilities (hearing, olfaction,
vision) form early, are well developed and are able to
detect cues relevant to orientation for most of the pelagic
larval stage. All this indicates that the passive portion of
the pelagic larval duration will be short, at least in most
warm-water species, and that behaviour must be taken into
account when considering dispersal, and in particular in
dispersal models. Although quantitative information on theontogeny of some behaviours is available for a relatively
small number of species, more research in this field is
required, especially on species from colder waters.
Keywords Connectivity Dispersal Orientation
Swimming Vertical distribution
Introduction
A large majority of marine teleost fish species, regardless
of whether they occupy pelagic or demersal habitats as
adults, have a pelagic larval stage. During this pelagic
larval stage, which may last days to months, several
important processes take place. First, the larvae grow,
increasing greatly in size and weight (Houde 1989), but
perhaps more importantly, most somatic and behavioural
development takes place during the larval period (Moser
1981). New structures and behaviours appear, both may be
modified, and some disappear. Finally, at least in demersal
species, most dispersal takes place during the pelagic larval
stage, thus setting the spatial scale for population structure
and connectivity.
Larval fishes begin the pelagic portion of their life his-
tory with limited behavioural abilities, but by the time they
settle, their ability to swim, orientate and detect sensory
cues is well developed (Leis 2006; Montgomery et al.
2006). The ontogeny of these behavioural abilities has
important implications for both dispersal and survival
during the larval stage, yet we know little about the
development of behaviour in marine larval fishes. Research
on behavioural development in larval marine fishes has
traditionally focused on feeding and vertical distribution
J. M. Leis (&)
Ichthyology, Australian Museum, 6 College St, Sydney,
NSW 2010, Australia
e-mail: [email protected]
123
Ichthyol Res (2010) 57:325342
DOI 10.1007/s10228-010-0177-z
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(Miller et al. 1988; Pearre 2003). More recently, behav-
iours relevant to dispersal, particularly swimming and
orientation, have received attention (Leis 2006). Sensory
abilities have been less studied, yet a knowledge of the
capacity of larvae to detect and respond to sensory cues,
including those produced by predators, is critical to
understanding how larvae survive and disperse in the sea
(Kingsford et al. 2002; Arvedlund and Kavanagh 2009).Thus far, the majority of research has been on structural
rather than functional development of sense organs, and
little has been quantitative (Arvedlund and Kavanagh
2009).
This review concentrates on the ontogeny of behaviours
and sensory abilities that are relevant to the dispersal of
demersal fish species: swimming, orientation, vertical dis-
tribution, vision, hearing and olfaction. It emphasises
recent research results, attempts to put these into context,
and points out directions for future research. The traditional
view was that the behavioural abilities of marine fish larvae
are so feeble as to be irrelevant to dispersal, but theresearch reviewed here shows this view to be wrong, and
wrong for a large portion of the pelagic larval stage, not
just when larvae are ready to settle. The emphasis in the
present paper is on larvae of marine demersal fishes,
especially those of rocky and coral reefs. Masuda (2009)
provides an excellent recent review of the ontogeny of
behaviour in larvae of pelagic fishes. Earlier reviews dealt
with some aspects of the ontogeny of larval behaviour,
often feeding, but few marine demersal species were
included (Blaxter 1986, 1991; Boehlert and Mundy 1988;
Miller et al. 1988; Noakes and Godin 1988), and much
research has taken place in the last 20 years.
With the exception of studies of vertical distribution
based on samples taken with plankton nets or midwater
trawls, nearly all research on the behavioural ontogeny of
demersal fishes has been done with reared larvae. Ideally,
results based on reared larvae should be checked using wild
larvae (e.g. Smith and Fuiman 2004; Faria et al. 2009).
This is seldom possible due to the difficulty of obtaining
wild larvae over a range of developmental stages, but it
may be possible to obtain wild settlement-stage larvae with
light traps, passive nets or seines, and use them in behav-
ioural comparisons of part of the pelagic larval phase (e.g.
Clark et al. 2005; Leis et al. 2007). Yet, in only a few
studies were comparisons made between the behaviour of
reared larvae and wild settlement-stage larvae of the same
or a related species, and comparisons involving younger
larvae are very rare.
Generally, size has been found to be a better predictor of
swimming ability than age (Leis 2006), so in this paper,
size will be used as a proxy for developmental stage in
preference to age. However, nearly all studies of swimming
ontogeny have utilised reared larvae, and reared larvae may
frequently have a wider range of growth rates than wild
larvae. Therefore, in wild larvae, size may or may not be a
better proxy than age: this simply has not been tested.
Some published works report size as standard length (SL),
whereas others report total length (TL). No attempt has
been made here to convert TL to SL, and this will introduce
a small amount of additional variation into the figures. In
this paper, speed is reported as cm s-1, except wherelabelled as body lengths per second (BL s-1). Regression
statistics reported in Table 2 are from the publications cited
in Table 1.
The nomenclature of early life-history stages of fishes is
complex, with many different systems of terminology and
no consensus on the most appropriate. I do not attempt to
distinguish between larvae and juveniles, but for this
review adopt an ecological perspective of ontogeny of
behaviour in marine, demersal fishes that includes all post-
hatch stages prior to settlement that are subject to pelagic
dispersal. To avoid awkward phrasing, and for simplicity, I
refer to the young fish considered here as larvae, butacknowledge that some terminologies might refer to them
by other labels.
Swimming
Various methods of measuring swimming ability provide
vastly different measures, ranging from laboratory raceway
measures of time (or distance) swum until exhaustion and
maximum swimming speed potential to the speed at which
larvae actually swim in the ocean (Leis 2006; Fisher and
Leis 2009). Therefore, it is important to be clear about what
is being measured and to avoid mixing different measures.
All studies have found a wide variation in swimming
performance at any size. In the present paper, the plotted
values are mean swimming performance for each 1 mm
increment in size.
Most authors have ignored possible differences between
day and night in swimming behaviour. Further, when
attempting to apply the results of their studies that typically
measured swimming speed over only short periods, they
have implicitly assumed that the larvae actively swim
constantly in the ocean, or at least that the proportion of
time spent swimming does not change temporally. Labo-
ratory studies (reviewed in Leis 2006) show that many
factors can influence either the proportion of time spent
swimming or the swimming speed itself, including food
density, time since feeding, and laboratory tank size. These
laboratory studies were based on a measure called routine
speed; that is, speed measured in a laboratory container
without any intentional intervention by the investigator.
Routine speed returns swimming speeds that are much
lower than those found by other methods (see Fisher and
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Leis 2009), and for that reason, studies of routine speed
will not be included here except for the important work of
Fisher and Bellwood (2003). They found that larvae of five
species (families Apogonidae and Pomacentridae) swam
constantly during the day, but at night younger larvae
swam only about 15% of the time, increasing to about
6080% at the end of the pelagic period, with a mean of34% across the full larval period. At night, individual lar-
vae were either active and swam constantly as during the
day, or were inactive and hung in the water without
swimming. Late in the larval phase of an anemonefish,
active larvae swam nearly twice as fast at night as during
the day (inactive individuals were not included in this
calculation). These ontogenetic and daynight differences
in speed and proportion of time spent swimming in the
laboratory indicate that in the ocean, day and night
swimming behaviours are unlikely to be equivalent, and
that the proportion of time spent swimming may vary
ontogenetically. These behaviours will be difficult to studyin the ocean, but more research is undoubtedly required.
In this section, an attempt is made to compare swim-
ming performance among taxa and among the environ-
ments occupied by the study species (e.g. tropical vs.
temperate). However, because not only the species but also
the families and in some cases the orders of fishes differ
among environments, the comparisons are confounded
taxonomically. That is, it is not possible to determine if any
differences revealed in these comparisons are due to
taxonomic differences or to environmental differences, or
to some combination of the two. In reality, this may not
matter, because when considering the influence of behav-
iour on larval dispersal and how this may differ among
locations or environments, it is only relevant to examine
the taxa that naturally occur in the location or environment
in question. In this context, the only meaningful compari-son is not just between different environments, but between
the combination of environments and the species that occur
in them; for example, the comparison of temperate species
in the temperate environment versus tropical species in the
tropical environment.
The present paper focuses on research that addresses
ontogeny of performance rather than ontogeny of mor-
phology. It would be very useful to predict swimming
performance from morphology, but few studies have cor-
related the two. Kohno and co-workers (Kohno et al. 1983;
Taki et al. 1987; Narisawa et al. 1997; Doi et al. 1998;
Kohno and Sota 1998) described the development of finsand body shape in reared larvae of a variety of marine
demersal fishes, and related morphology to qualitative
descriptions of swimming ability in the laboratory (e.g.
less active swimming, rush and manoeuvrability,
complete swimming ability). But, without quantitative
information on speed or endurance, it is difficult to apply
these descriptive measures to questions of dispersal, or to
predict swimming performance from larval morphology.
Fisher and Hogan (2007) were able to predict the critical
Table 1 Demersal marine fish taxa for which the ontogeny of swimming speed has been studied in larvae
Order Family Habitat Critical
speed
In situ
speed
Endurance Reference
Gonorynchiformes Chanidae Tropical 1 Leis et al. (2007)
Gadiformes Gadidae Cool-temperate 1 Guan et al. (2008)
Perciformes Apogonidae Tropical 1 1 Fisher et al. (2000)
Perciformes Carangidae Tropical 2 1 1 Leis et al. (2006b, 2007)Perciformes Ephippidae Tropical 1 1 Leis et al. (2007, 2009a)
Perciformes Leiognathidae Tropical 1 1 1 Leis et al. (2007, 2009b)
Perciformes Lutjanidae Tropical 1 1 Leis et al. (2007, 2009a)
Perciformes Percichthyidaea
Warm-temperate 1 1 Clark et al. (2005)
Perciformes Polynemidae Tropical 1 1 1 Leis et al. (2007, 2009b)
Perciformes Pomacentridae Tropical 2 2 Fisher et al. (2000)
Perciformes Sciaenidae Warm-temperate 2 1 1 Clark et al. (2005),
Leis et al. (2006a),
Faria et al. (2009)
Perciformes Serranidae Tropical 3 2 Leis et al. (2007, 2009a)
Perciformes Sparidae Warm-temperate 2 2 1 Clark et al. (2005),
Leis et al. (2006a)
Scorpaeniformes Cottidae Cool-temperate 1 Guan et al. (2008)
Pleuronectiformes Pleuronectidae Cool-temperate 1 Ryland (1963)
Values are the number of species studieda
Adults of the study species live in rivers and upper estuaries, but larvae are found in coastal and estuarine environments of SE Australia
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speed (Ucrit, see below) of wild, settlement-stage larvae
from a few morphological measures, including body size
(they had measures of both morphology and speed for 100
mostly tropical species). Settlement-stage larvae have very
well developed fins, musculature and other swimming
structures that are absent or incompletely developed in
smaller larvae, and Fisher and Hogan (2007) rightly caution
that predictions based on their model are unlikely to applyto smaller, less developed larval stages. That is, the Fisher
Hogan model is likely to be applicable only to swimming at
the end of the larval stage and not to the ontogeny of
swimming. Clearly, however, this approach has potential,
even if a different relationship between morphology and
speed might be found in species from colder environments.
An attempt to predict Ucrit from size alone for larvae of four
cold-temperate marine species (a gadiform, a salmoniform,
a scorpaeniform, and a pleuronectiform; Guan et al. 2008)
found a significant relationship between total length
(mm) and speed [Ucrit = 0.79 TL - 2.03, R2 = 0.90,
P\ 0.0001. Note that Guan et al. (2008) wrote dah (daysafter hatch) instead of TL, but this is an error; P. Snelgrove,
personal communication]. The slow speeds of these cold-
water species compared to tropical species (see Fig. 1) serve
as reminder that any such relationship is almost certain to be
temperature and taxon dependent.
Putting larval-fish swimming speeds into an ecological
context is not always easy, and different approaches have
been attempted. The concept of effective speed (mean-
ing a swimming speed on average at least as fast as the
average current in a particular location; Leis and Stobutzki
1999) can leave the mistaken impression that larvae that
are slower than the effective speed will have little influence
on dispersal. In reality, sustained swimming at almost any
speed has the potential to influence dispersal outcomes, in
part depending on the direction that is swum. For example,
swimming at speeds that are slower than local currents but
normal to the current direction, which is frequently parallel
to depth contours in continental shelf waters, can oftenenable larvae to reach a coastal settlement habitat when
passive larvae would not (e.g. Porch 1998). Several larval-
fish modelling exercises (reviewed in Leis 2006) have
concluded that speeds of 23 cm s-1 are able to influence
dispersal outcomes, leading to the concept of influential
speed, which is much lower than effective speed. The
important point in the context of dispersal is whether larvae
are able to swim ecologically meaningful distances or
speeds relative to their larval duration. But, once again,
what is ecologically meaningful is context dependent.
Critical speed
Critical speed (Ucrit) is a laboratory raceway measure of
potential swimming ability: speed is increased incremen-
tally in short (25 min) steps until the larva can no longer
swim against the current (Brett 1964; Fisher et al. 2000).
Critical speed is a very useful standard comparative mea-
sure of the prolonged swimming speed of fishes, but it is
not the speed at which larval fishes swim in the ocean
(Fisher and Leis 2009). Critical speed is relatively easy to
Fig. 1 Ontogeny of critical
speed (Ucrit) in larvae of marine
demersal fishes. Plotted values
are family means of up to three
species for 1 mm size
increments. Sources of data are
shown in Table 1. Solid dark
symbols are tropical taxa.
Hollow symbols are warm-
temperate taxa. Solid medium,
larger symbols with thick
borders are cool-temperate taxa.
Straight broken lines
correspond to relative speeds in
body lengths per second
(BL s-1)
328 J. M. Leis
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measure, hence there is more information on the ontogeny
of Ucrit than for other measures of swimming performance.
The ontogeny of critical speed has been reported for 22
marine species in 15 families (Table 1). Most of the species
are tropical (n = 13), but five are warm-temperate in dis-
tribution, and four are from cool-temperate environments
(Table 1). Ontogenetic data on critical speed are summa-
rised in Fig. 1. The plotted points are family values (meansof 23 species in six families, and single species values for
nine families).
It can be seen from Fig. 1 that critical speed increases
with size, although it appears that at least two families
(Lutjanidae, Polynemidae) and perhaps three more (Ser-
ranidae, Leiognathidae, Pomacentridae) have a decrease
or at least a levelling offin critical speed at the largest
sizes; i.e. at about the size at which the larvae settle. A
post-settlement decrease in critical speed was documented
in pomacentrids (Stobutzki and Bellwood 1994), so per-
haps this should be expected as part of the transition
between pelagic and demersal environments. Therefore, adeparture from a positive relationship between size and
speed is possible at larger sizes, and attempts to predict
swimming speeds of pelagic larvae from those of recently
settled individuals should be done with great caution [for
example, see Nilsson et al. (2007) regarding physiological
changes associated with settlement].
Aside from the decrease in speed at larger sizes noted
above, most species show a relatively linear increase of
speed with size over the pelagic stage (although few studies
have measured Ucrit for the youngest larvae), and further,
the most common pattern is for the relative speed (i.e.
speed in body lengths per second, BL s-1) to remain
approximately constant (Fig. 1). Notable exceptions are the
tropical families Lutjanidae and Serranidae, where small
larvae have exceptionally large spines in the dorsal and
pelvic fins (Leis and Carson-Ewart 2004). Smaller larvae of
these families are much slower than similar-sized larvae of
other families, and their critical speed does not exceed
5 cm s-1 until about 79 mm (Fig. 1), after the excep-
tionally large fin spines have reached maximum relative
size and are becoming relatively smaller. From about 7 to
9 mm, serranid and lutjanid larvae increase rapidly in
speed with size (23 cm s-1 per 1 mm increase in size),
and as settlement approaches, they are among the fastest
larvae tested.
The ontogeny of critical speed has strong phylogenetic
and environmental influences. Larvae of taxa that are
distributed in cool-temperate waters (Pleuronectidae,
Gadidae, Cottidae) have some of the slowest reported
critical speeds, and consistently swim at about 5 (BL s-1)
over the size ranges tested (Fig. 1). In addition, Guan et al.
(2008) plot (their fig. 5) but do not formally analyze Ucrit
data from two other species of cool temperate fishesan
osmerid and a pleuronectidwhich have size versus speed
relationships similar to the other cool-temperate taxa in
Fig. 1. Larvae of taxa distributed in warm-temperate
waters (Sciaenidae, Sparidae, Percichthyidae) are more
variable in the development of critical speed. Larvae of
such taxa are initially relatively slow (510 cm s-1), but at
sizes larger than 5 mm, sciaenids remain at 10 BL s-1,
whereas sparids and percichthyids larger than 78 mm canswim at 1520 BL s-1. Aside from the serranids and lut-
janids mentioned above, larvae of tropical taxa are fast
throughout development, with critical speeds faster than
10 cm s-1 and with most species swimming at
1520 BL s-1 for much of their larval phase (pomacentids
reach almost 30 BL s-1). On a per-size basis, larvae of
pomacentrids are among the fastest swimmers, although
percichthyids and carangids are faster than pomacentrids at
certain sizes (Fig. 1).
In addition to the data summarised above that cover a
substantial portion (but not all) of the pelagic larval phase,
information on Ucrit at hatching is available for a few coral-reef fishes (six pomacentrids, two apogonids, one blenniid
and one acanthurid, only the last of which has pelagic eggs;
Fisher 2005). These just hatched larvae (1.54.5 mm TL) of
ten species had Ucrit values as high as 4 cm s-1 (up to
14 BL s-1) and 2 cm s-1 on average. Among these ten
species, speed increased at a rate of 1.24 cm s-1 for each
1 mm increase in hatching size. Larvae smaller than
2.25 mm at hatching (two pomacentrids and the acanthurid)
had speeds that were virtually zero, whereas the species
larger than 2.25 mm at hatching swam at speeds of
24 cm s-1. Based on these limited data, it appears that
most species that spawn nonpelagic eggs have swimming
speeds that are shown by modellers to influence dispersal
outcomes (Leis 2006) from the time they hatch. By
assuming that the among-species increase in speed with size
applied throughout the larval phase, Fisher (2005) predicted
that the larvae of most of the 11 families considered would
have critical speeds of at least 13 cm s-1 (the mean current
speed at Lizard Island, Great Barrier Reef) for more than
50% of their larval phase. Fishers prediction was not very
different from the empirical data in Fig. 1.
Comparisons of critical speed to ambient currents are
problematical because larvae seldom swim at their critical
speed in the ocean, and, of course, current speeds vary
widely among locations and times. However, average
current speeds of 1015 cm s-1 are common in many
coastal environments (Fisher 2005), which means that
larvae of many tropical and warm temperate species are
capable of effectively opposing currents from sizes of 5 to
10 mm, and influencing their dispersal when considerably
smaller. Cool-temperate species, in contrast, did not reach
an average critical speed of 10 cm s-1 over the measured
size range (Fig. 1).
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Much interest has been expressed about when fish larvae
move from swimming in a viscous hydrodynamic envi-
ronment to an inertial one, because it is thought that it is
too energetically costly to swim any significant distance in
a viscous environment. Early work considered that the
transition from viscous to inertial swimming began at a
Reynolds number (Re) of 30 and was largely complete
when the Reynolds number reached 200 (Webb and Weihs
1986), but it is now considered that these values should be
closer to 300 and 1,000, respectively (see Leis 2006). The
value of Re is inversely dependent on the viscosity of seawater, and is therefore temperature dependent, because
viscosity is higher at lower temperatures. For temperatures
above 20C, fish larvae swimming at the critical speed
(Fig. 1) will reach Re 300 by 58 mm, depending on the
species. Therefore, for most of the pelagic larval phase,
larvae in warmer water will be capable of swimming in a
largely inertial hydrodynamic environment. In contrast,
because of their slower speed, and the increased viscosity
of cold water, larvae of cool-temperate species will not
reach Re 300 until 1011 mm.
In situ speed
Much less information is available on the ontogeny of
swimming of larvae in the ocean, or in situ speed (Leis and
Carson-Ewart 1997), and because of the difficulties
involved in working with very small larvae (\56 mm), in
situ speed data are available for a narrower range of larval
sizes than for Ucrit. Measurements of the development of
swimming speed in the ocean are available for ten species
of eight families (Table 1): three species (two families) are
warm-temperate and seven species (six families) are
tropical.
The relationship between size and speed is more com-
plex and variable for in situ speed than it is for critical
speed (Fig. 2). For nine of the ten species above, there is a
positive linear relationship between size and in situ speed,
the exception being the lutjanid Lutjanus malabaricus, for
which there was not a significant relationship between size
and in situ speed. In situ speeds are lower than critical
speeds, with values generally between 3 and 15 BL s-1. Aswith the critical speed, some species decreased in speed at
larger sizes: Epinephelus coioides, Eleutheronema tetra-
dactylum and Caranx ignobilis. The three warm-temperate
species had relative speeds of 38 BL s-1, and values for
the tropical species ranged widely from about 2 to
18 BL s-1, encompassing the speeds of the warm-tem-
perate species, but generally being higher. At any size,
warm-temperate species were slower by 410 cm s-1 than
tropical species. Unfortunately, no in situ studies of larvae
of cool-temperate species are available.
In situ speed was nearly always slower than critical
speed (Fisher and Leis 2009), but the ratio of the twovaried with species (Table 2). It is not generally possible to
measure both critical and in situ speed in the same indi-
vidual, so comparisons between the two measures are
based on mean values within 1 mm size increments. In half
of the ten species above, there was a significant positive
correlation between size-specific measures of critical and
in situ speed, but the slope of that relationship varied
widely among species, from 0.19 to 2.28 (Table 2). The
overall mean of the ten species-specific ratios of in situ
Fig. 2 Ontogeny of in situ
speed in larvae of marine,
demersal fishes. Plotted values
are species means for 1 mm size
increments. Sources of data are
shown in Table 1. Solid dark
symbols are tropical taxa.
Hollow symbols are warm-
temperate taxa. Straight broken
lines correspond to relative
speeds in body lengths per
second (BL s-1
)
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speed to critical speed (based on 1 mm size increments)
was 0.57 (SE = 0.065, and 95% CI = 0.410.72), but thevalues for individual species ranged from 0.29 to 0.91. This
mean value is similar to the 0.5 ratio determined from
studying settlement-stage larvae (Leis and Fisher 2006).
Clearly, larvae in the ocean do not swim as fast as they are
able, and a value of about 50% of the critical speed seems a
reasonable central value for in situ speed. However, the
wide range of values among individual species and within
families suggests that caution should be applied when
using the central value to predict in situ speed in taxa for
which no data on in situ speed are available.
The ratios of in situ speed to critical speed seem to differ
among taxa from different environments. In warm-tem-perate species, the ratios are relatively low, with a narrow
range of values: 0.29, 0.31 and 0.43, median 0.31 (n = 3).
The tropical species have a wider range of values
(0.390.91, n = 7), and a much higher median (0.65). The
medians are significantly different (Wilcoxon rank-sum
test, P\0.05). This suggests that the relationship between
critical speed and in situ speed may differ between envi-
ronments, temperatures, or taxa, and that tropical species
may swim closer to their potential speed (i.e. Ucrit) in the
ocean than do temperate species. If true, then comparisons
of critical speed between different environments may not
be informative about possible differences in swimming
speeds in the ocean. An additional dimension of cross-
environment (or temperature) comparisons is the observa-
tion that in gadids and cottids, temperature influences the
trajectory of larval critical swimming speed development,
but that the relationship is species-specific (Guan et al.
2008). Until now, relatively little attention has been paid to
the influence of temperature on the development of
swimming abilities in larvae. Further research in this area
is needed (see, for example, Munday et al. 2009).
Larvae swim in the ocean at 515 BL s-1 throughout
most of their pelagic period (Fig. 2), and they swim atspeeds considered by dispersal modellers to be influen-
tial for dispersal outcomes (i.e. more than 3 cm s-1) for
most of their pelagic period (Leis 2006). Mean in situ
speed reaches 10 cm s-1 at 818 mm, depending on spe-
cies. At 10 cm s-1, larvae are swimming as fast as average
currents in many coastal areas. As noted in the original
publications (Table 1), most larvae for which there are data
on in situ swimming abilities were swimming at Reynolds
numbers larger than 300, and thus out of a hydrodynamic
environment dominated by viscous forces, but it is
important to keep in mind that all such species are from
warm-temperate or tropical environments.A recent study of the influence of schooling on orien-
tation in settlement-stage larval fishes showed that larvae
in groups swam about 10% faster than individual larvae
(J.-O. Irisson, personal communication). So, it is possible
that the ontogeny of schooling may interact with the
ontogeny of swimming behaviour to produce faster than
expected speeds when larvae begin to school.
Endurance
Critical speed and in situ speed are typically measured over
minutes, yet the larval stage lasts for days to months, so it
is important to know when during ontogeny larvae are
capable of swimming over periods and distances that are
ecologically meaningful. The time or distance over which
larvae can swim is called endurance, and is typically
reported as kilometres swum rather than as hours swum.
Swimming endurance is measured by forcing unfed larvae
to swim to exhaustion in a laboratory raceway at a constant
speed (Stobutzki and Bellwood 1997). In most published
Table 2 Comparison of in situ speed (IS) to critical speed (U) in studies that included a range of developmental sizes of fish larvae
Family Species IS Slope 95% CI P Overall
mean IS/U
Habitat
Carangidae Caranx ignobilis 0.45 U ? 1.45 -0.2 to 1.1 0.13 NS 0.52 Tropical reef
Ephippidae Platax teira 1.66 U - 8.18 0.7 to 8.8 0.016 0.87 Tropical reef
Leiognathidae Leiognathus equulus 2.28 U - 2.17 1.4 to 5.0 0.002 0.65 Tropical non-reef
Lutjanidae Lutjanus malabaricus 0.24 U ? 9.03 -0.1 to 0.7 0.080 NS 0.63 Tropical reef Polynemidae Eleutheronema tetradactylum 0.34 U ? 5.00 -0.2 to 1.1 0.098 NS 0.91 Tropical non-reef
Sciaenidae Argyrosomus japonicus 0.26 U ? 0.38 0.1 to 0.4 0.009 0.31 Warm-temperate
Serranidae Epinephelus coioides 0.55 U ? 2.26 0.2 to 1.1 0.012 0.67 Tropical reef
Serranidae Epinephelus fuscoguttatus 0.69 U - 8.03 -0.3 to 7.9 0.068 NS 0.39 Tropical reef
Sparidae Acanthopagrus australis 0.19 U ? 3.80 -0.0 to 0.4 0.081 NS 0.29 Warm-temperate
Sparidae Pagrus auratus 0.92 U - 10.80 0.6 to 1.3 0.003 0.43 Warm-temperate
The P value is for the null hypothesis that the slope of the regression line is not different from zero.NS not significant
Sources of data and statistical analyses are given in Table 1
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studies, the speed was the same for all developmental
stages, but in some (e.g. Fisher et al. 2000), speed was
scaled to body size. Although this provides a standard
value that can be compared across taxa or developmental
stages, measuring endurance swimming in this way is
problematical for several reasons. First, it is very unlikely
that larvae in the ocean actually swim to exhaustion.
Second, larvae that are able to feed have more-or-less
open-ended endurance, and can grow and develop while
swimming (Fisher and Bellwood 2001; Leis and Clark
2005). Third, any fixed raceway speed is arbitrary, and
endurance (distance swum) is inversely proportional to
swimming speed (Fisher and Bellwood 2002). Finally, like
critical speed, laboratory endurance measures are not
directly applicable to the ocean, and there are no in situ
measures of endurance with which to calibrate labora-
tory measures of endurance. Endurance values do, how-
ever, provide some indication of when larvae are able to
swim meaningful distances in the ocean. Because of the
relatively long time it takes to measure endurance in fish
larvae (larvae of some reef fishes can swim for a week or
more before exhaustion), there are only a few studies of the
ontogeny of swimming endurance. Much more data are
available on the endurance of settlement-stage larvae (see
Leis 2006; Fisher and Leis 2009).
The ontogeny of endurance swimming has been studied
in only nine species of eight families (Table 1, Fig. 3). In
all cases, endurance in larvae smaller than 7 mm was small
(\4 km). Between 7 and 10 mm, endurance started to
increase, with values of 515 km, but it was often variable
among individuals of a species (Fig. 3). By the time larvae
reached the size of settlement (assuming it is more than
10 mm), endurance values in excess of 20 km were com-
mon, and may reach 50 km or more. There is no obvious
difference in endurance between warm-temperate and
tropical species, except that tropical species attain greater
endurance prior to settlement, primarily because many
settle at larger size. There are no endurance data for cool-
temperate species. Clearly, at sizes larger than 710 mm,
the endurance swimming abilities of larvae can be
remarkably large.
All studies of ontogeny of endurance were done with
reared larvae. It is likely that endurance measured in this
standard way is strongly influenced by larval condition or
body reserves. It is also likely that reared larvae will often
have greater reserves than wild larvae due to optimal
feeding conditions in rearing containers. If so, this could
lead to higher endurance estimates for reared larvae than
wild larvae. Unfortunately, there are few comparisons of
reared and wild larvae for endurance, and all involve set-
tlement-stage larvae, but there is at least one example
where reared larvae of a pomacentrid had greater endur-
ance than wild larvae (Leis and Clark 2005).
Orientation
Without orientation, swimming by larvae will act primarily
to increase diffusion, and influence dispersal outcomes by
increasing the area that larvae pass over or through, thus
increasing the possibility of finding a suitable habitat
by chance. The two types of orientation should not be
Fig. 3 Ontogeny of endurance
swimming in larvae of marine
demersal fishes. Plotted values
are species means for 1 mm size
increments. Sources of data are
shown in Table 1. Solid dark
symbols are tropical taxa.
Hollow symbols are warm-
temperate taxa
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confused: (1) within-individual trajectories (that is, the
orientation of individual larvae), and (2) among manyindividual trajectories (that is, the orientation of many
larvae, based on the mean bearing of individuals). Orien-
tation has been studied only by in situ techniques. Until
recently, the only way of doing this was by diver obser-
vations of larvae in the ocean (Leis et al. 1996), but a new
technique using a drifting in situ chamber (or DISC; Paris
et al. 2008; Irisson et al. 2009) offers great potential to
complement and extend diver observations.
Significant within-trajectory orientation is found in the
large majority of individual larvae of most species that have
been studied (Table 3). This means that individual larvae of
most species do not swim randomly in the ocean. The pre-
cision of orientation (i.e. the straightness of a trajectory), can
be expressed by a statistic called r (the length of the mean
vector; see Batschelet 1981), which ranges from 0 (fully
random) to 1 (entirely linear). When values of r are plotted
against size of larvae, there is no obvious ontogenetic trend
in the precision of orientation (Fig. 4). Although individual
trajectories are usually significantly different from random
swimming, the within-trajectory precision is frequently low.
This means that net velocity (the combination of speed and
direction that takes into account the variation in swimming
direction) is usually noticeably slower than the nominal insitu swimming speed. For example, for the four species
studied by Leis et al. (2009a), net speed was 6283% of the
nominal in situ speed, and as expected, this ratio was cor-
related with r (ratio of net speed to nominal in situ
speed = 1.11 9 r- 0.08, R2 = 0.625).
Larvae of species that live in non-reef habitats as adults
apparently have lower orientation precision than do larvae
of reef species (Leis et al. 2009b; Fig. 4), but this has been
tested in only a few species. The four tropical reef species
in Fig. 4 have a mean r of 0.593 (SE = 0.024, n = 84),
which is significantly greater (P = 0.003, t test on arcsine-
transformed data) than the mean r of the two tropical
species that live on muddy or sandy bottom as adults
(mean = 0.477, SE = 0.032, n = 42).
Ontogeny of orientation in situ has been studied in the
larvae of only ten species: three species of warm-temperate
fish and seven species of tropical fish (four of which live on
reefs as adults and one carangid that is reef-associated;
Table 3). Larvae as small as 5 mm have been studied in
situ. The percentage of larvae with (within trajectory)
directional swimming was 6790% in nine of the species,
Table 3 Studies of ontogeny of orientation of marine fish larvae
Family: species Size range
(mm SL)
Proportion (%)
of individuals
significantly
orientated
Among-individual
orientation
Ontogenetic changes in
orientation
Adult habitat
Carangidae:
Caranx ignobilis
8.518.0 67 Yes; location
dependent
No Tropical reef-
associated
Ephippidae:
Platax tiera
6.010.0 82 Yes No Tropical reef
Leiognathidae:
Leiognathus equulus
7.513.6 29 No No Tropical soft bottom
Lutjanidae:
Lutjanus malabaricus
12.023.0 9 0 Yes, only small
larvae
Bimodal directionality in small
larvae, none in large larvae
Tropical reef
Polynemidae:
Eleutheronema tetradactylum
7.521.0 75 Yes, only small
larvae
Smallest larvae to NE (to shore),
others not directional
Tropical soft bottom
Sciaenidae:
Argyrosomus japonicus
5.014.0 72 No Higher among-individual
precision with size
Warm-temperate
estuary and reef
Serranidae:
Epinephelus coioides
9.020.5 74 Yes, some size
groups
Small larvae to N; medium to S;
large to N
Tropical inshore reef
Serranidae:
Epinephelus fuscoguttatus
13.020.5 71 No overall Medium larvae to shore (NW);
large parallel to shore (SE)
Tropical reef
Sparidae:
Pagrus auratus
7.09.5 74 Yes, only large
larvae
Only large larvae had significant
among-individual orientation
Warm-temperate
estuary and reef
Sparidae:
Acanthopagrus australis
7.012.0 84 Yes Small larvae to shore (NW),
large parallel to shore (NE)
Warm-temperate
estuary and reef
Tropical species were studied off southern Taiwan (Leis et al. 2006b, 2009a, b)
Warm-temperate species were studied off southeastern Australia (Leis et al. 2006a)
For E. fuscoguttatus, significant orientation was not found in either medium or large larvae, possibly due to low sample size, but the swimming
directions of the two size groups were significantly different
Vertical distribution of the same species was also studied
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and only 29% in Leiognathus equulus. The last species
lives as an adult in soft-bottom habitats, and the authors of
the study (Leis et al. 2009b) suggested that the larvae of
such species may have less of a need for orientated
swimming than do species that live on coral reefs. In none
of these ten species was there an ontogenetic trend in
within-trajectory orientation precision either in the r sta-
tistic (Fig. 4) or in the proportion of individual larvae that
had within-trajectory orientation. So, it seems that orien-
tation abilities are formed at a relatively early stage in
ontogeny (by 5 mm), and do not improve with growth orage thereafter. Very small larvae cannot be studied in situ
with diver observation methods, so we know nothing about
the orientation abilities of larvae smaller than about 5 mm,
and for some species, the smallest individuals studied are
considerably larger. It is reasonable to assume that orien-
tation abilities are poor at hatching and improve between
hatching and 5 mm, but they do not seem to improve
thereafter. There are, however, differences in orientation
precision among species.
In seven of the ten species, among-trajectory orientation
was found; i.e. the frequency distribution of the mean
orientations of individual larvae was significantly different
from random. Ontogenetic changes in among-trajectory
orientation were also found in seven of the ten species
(Table 3). Ontogenetic changes ranged from a simple
increase in the precision of among-individual orientation
(one species) to clear changes in the direction in which the
larvae were swimming (three species, e.g. Fig. 5). In two
species, the smallest larvae studied showed significant
orientation while larger larvae did not, and in one species
only the largest larvae had directional (among trajectory)
swimming. One might expect ontogenetic improvement in
orientation; e.g. that orientated swimming would be more
common or more precise in larger larvae. However, the
opposite (apparent ontogenetic deterioration in orientation
ability) was just as common. With only ten species studied,
the variety of ontogenetic changes in among-individual
orientation is somewhat surprising. So, it seems that each
species must be considered individually, and it is premature
to generalise about the ontogeny of among-individual
orientation.
Ontogenetic changes in orientation imply several thingsabout the sensory cues used for orientation. If orientation
changes with development, then as larvae grow, either the
cues used for orientation change, sensory abilities change,
the motivation to respond to cues changes, or perhaps all
three changes occur.
The available studies of orientation ontogeny (Table 3)
have some limitations. The ontogeny of orientation has
been studied in more than one location for very few spe-
cies, and because location-dependent orientation has been
found in settlement-stage larvae of some species (e.g. Leis
and Carson-Ewart 2003), an assumption that the orientation
will be spatially consistent may not be justified. In some
cases, the number of larvae studied in some of the size
classes was low, which can be problematical given the
generally low overall precision of the among-trajectory
orientations of larvae of many species. All four of the
studies used reared larvae, and none were able to compare
results to anything other than wild settlement-stage larvae
of related species. All of these studies were based on
observing larvae for at most 10 min at a time, which is a
small proportion of the pelagic larval duration. It is unclear
Fig. 4 Ontogeny of precision
of directional swimming (length
of the mean vector) in larvae of
marine demersal fishes. This
shows a lack of any ontogenetic
trend in within-individual
orientation. Plotted values are
species means for 1 mm size
increments. Solid dark symbols
are tropical reef taxa. Solid
medium symbols with thick
black borders are tropical non-
reef taxa. Hollow symbols are
warm-temperate taxa. Symbols
above the broken horizontal line
represent an orientation that is
significantly different from
uniform for points based on
(typically) 10 min of
observation (n = 21). Sources
of data are shown in Table 3
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whether the results from such short-term studies can be
scaled up to longer periods. Clearly, there is room for
further study of the ontogeny of orientation in larvae in
marine fishes. Especially needed are studies that examine
the consistency of orientation patterns over time and at
different locations, directly test if the behaviours of reared
and wild larvae differ, and expand taxonomic coverage.
Based on the available studies, several broad statements
can be made that seem to apply across most of the pelagic
larval period of larvae of demersal fishes from warmer
waters. Most individual larvae swim directionally, and
within-individual orientation precision does not improve
with growth. Among-individual orientation is common, but
may not be very precise. Ontogenetic changes in among-
individual orientation are common, and orientation variesamong species.
A species with an overall among-trajectory orientation is
able to have the greatest influence on dispersal. Yet a
species in which only within-trajectory orientation is
present can have an increased probability of finding set-
tlement habitat if the larvae maintain their within-trajectory
orientation over time (Huebert and Sponaugle 2009), and
larvae of such a species will have dispersal outcomes very
different from passive drift with the currents.
Schooling
There are reasons to expect that larvae in groups or schools
may have better orientation than individual larvae (Larkin
and Walton 1969; Simons 2004). A study that examined this
issue with settlement-stage pomacentrid larvae showed that
groups of about ten larvae had more precise orientation both
within-trajectories and among trajectories (J.-O. Irisson,
personal communication), thus supporting this expectation.
However, little is known about the ontogeny of schooling
in larvae of demersal fishes, or if schooling by larvae of
demersal species is even common. Two exceptions are the
mugilid Aldrichetta forsteri, which forms aggregations
when as small as 46 mm (Kingsford and Tricklebank
1991), and the gobiid Gobiosoma bosci, which begins to
shoal at about 6 mm (Breitburg 1991); in both species,
larvae of this size do not have complete fins. Some species
are known to school shortly before settlement, but most of
them also school following settlement (Leis and Carson-
Ewart 1998), so schooling at this stage may have more to do
with preparation for post-settlement existence than it does
with the pelagic stage.
In larvae of pelagic fishes, schooling begins after fin
formation is complete, and may not commence until well
into the juvenile stage: pelagic species began to school at
sizes ranging from 10 to 40 mm (Masuda 2009; Sabate
et al. 2010). Carangids school from 12 to 16 mm, and
although their fins are fully formed, this size did not cor-
respond to any change in sensory organs (Masuda 2009).
So, there seem to be a variety of patterns in the develop-
ment of schooling among pelagic fishes, and it is not
possible to generalise. Nor is it safe to assume that larvae
of demersal fishes are any different. More work is needed
on the ontogeny of schooling in fish larvae. This is
Fig. 5 Ontogenetic change in among-individual orientation in larvae
of a sparid, Acanthopagrus australis, in coastal waters 1 km from
shore. Above: small larvae (710 mm SL) swam on average in a
north-west direction toward shore (n = 18). Bottom: large larvae
(1012 mm SL) swam on average in a north-east direction parallel to
shore (n = 19). The bars represent the frequency distribution of the
mean swimming directions of individual larvae, and the thin radius
that penetrates the outer circle is the overall mean direction (after Leis
et al. 2006a). The two frequency distributions are significantlydifferent
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especially important, as schooling may strongly influence
other orientation and swimming abilities.
Sensory abilities
Orientation, whether vertically or horizontally, requires
the ability to detect and respond to cues. Therefore, thedevelopment of sensory abilities is intimately related to the
ability of larval fish to orientate. Reviews of sensory
abilities that are relevant to the orientation of fish and
invertebrate larvae provide a good overview (Kingsford
et al. 2002; Montgomery et al. 2006; Arvedlund and
Kavanagh 2009). In this review, the emphasis is on vision,
olfaction and hearing, because these are the senses that are
thought to have the most potential to be involved in the
orientation and dispersal of the larvae of marine demersal
fishes. Research on the ontogeny of these senses has
included only a limited range of species and families,
concentrating on pomacentrids. Therefore, the generality ofthe statements in this section remains to be tested. This
section focuses on work demonstrating actual sensory
function, rather than studies of structural development of
sense organs, because most studies of sensory organ
structure are not clearly informative about function (for a
more complete consideration of structural sense organ
development; see Arvedlund and Kavanagh 2009).
Vision is relevant to orientation via direct observation,
but is limited by underwater visibility to a few tens of
metres. Vision may be relevant to orientation over much
larger scales if a solar compass or some other celestial cue
is used. There is no direct evidence from marine larval
fishes of the latter, but circumstantial evidence exists for
the use of a solar compass by pomacentrid larvae (e.g. Leis
and Carson-Ewart 2003), and its use by juveniles and adult
salmon is well established (e.g. Quinn 1980).
Many species that spawn nonpelagic eggs (i.e. demersal
or brooded) hatch with functional eyes, but in most cases,
larvae that hatch from pelagic eggs do not have functional
eyes for one to a few days. Therefore, vision can be used
for orientation for most or all of the pelagic larval period.
Research on feeding behaviour in the laboratory suggests
the distance over which larvae can see and respond to food-
size objects is limited, on the order of mm to cm (Job and
Bellwood 1996, 2000), and therefore of limited use to
orientation by direct observation. However, calculations
based on retinal structure (Job and Bellwood 1996; Shand
1997; Lara 2001) and anecdotal field observations of
behaviour suggest that settlement-stage larvae can see
underwater as well as human divers can (Leis and Carson-
Ewart 2001). Little work has been done on the visual
abilities of larvae in the context of orientation, and even
less has addressed the ontogeny of such abilities.
By settlement, fish larvae have well-developed olfactory
abilities [see reviews by Kingsford et al. (2002) and
Arvedlund and Kavanagh (2009) and a recent paper by
Dixson et al. (2008)], but there is little information on the
ontogeny of olfaction in marine fish larvae. Embryonic
anemonefishes (Pomacentridae: Amphiprion spp.) imprint
on the smell of the anemone taxa upon which the larvae
subsequently settle, implying an olfactory sense while stillin the demersal egg (Arvedlund and Kavanagh 2009), and
larval anemonefish (Amphiprion percula) can detect by
smell alone both predatory and nonpredatory reef-fish
species within 24 h of hatching (Dixson et al. 2009). These
newly hatched larvae avoided water with the scent of adult
fishes, which, in the sea, would help them move from their
hatching location on the reef and into open water, where
predator threats are assumed to be lower (Johannes 1978).
This result indicates that larvae from nonpelagic eggs have
functional olfactory organs for their entire pelagic period,
and well before the nasal pit is roofed over, forming separate
nares (Kavanagh and Alford 2003). Whether anemonefishesare representative of other species with nonpelagic eggs
let alone those with pelagic eggsremains unknown, but
structurally, the olfactory organs of pomacentrids and a
lethrinid appear to be functional in newly hatched larvae
(Arvedlund and Kavanagh 2009). Arvedlund and Kavanagh
(2009) conclude that larvae of coral reef fishes develop
their olfactory organs rapidly (including olfactory receptor
neurons). Therefore, we can anticipate that olfaction could
be used in orientation for most or all of the pelagic larval
period.
Hearing abilities of fish larvae are well developed by
settlement (reviewed in Arvedlund and Kavanagh 2009).
The only work on the ontogeny of hearing abilities in
larvae of marine fishes shows that larvae as small as could
be studied (i.e. 810 mm) were able to hear, and that
hearing ability increased with size of larvae until settlement
(Wright 2006). However, a study of embryos of anemo-
nefishes (Amphiprion rubrocinctus and A. ephippium,
Pomacentridae) demonstrated a response to sound with
increased sensitivity as the eggs developed (Simpson et al.
2005), implying that, at least for species with demersal
eggs, larvae may have the ability to hear throughout their
pelagic period, and even before.
All three senses considered here are functional relatively
early in the pelagic larval phase, and are therefore poten-
tially useful in orientation over most of the larval phase.
Research on the ontogeny of sense organ function in
marine demersal fishes is limited, but shows that sense
organ performance increases with growth. However, the
distance over which each sense organ is effective for ori-
entation and how this changes with growth is generally
unknown, due to uncertainties about the actual cues that
larvae utilise (e.g. what frequencies of sound or what
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scent), how cue strength varies spatially and temporally,
and in spite of significant recent advances, how sense organ
performance varies ontogenetically. The field of the sen-
sory abilities of larval fishes is important, if difficult, to
advance.
Vertical distribution
The behaviours involved with horizontal swimming con-
sidered above can directly influence dispersal outcomes,
whereas vertical distribution behaviour can influence
dispersal only indirectly, through interaction with currents
that are vertically stratified with respect to velocity (e.g.
Lagardere et al. 1999; Forward and Tankersley 2001; Paris
and Cowen 2004). Vertical distribution and migrations
constitute the most studied aspect of larval fish behaviour,
and a huge literature exists. It has long been known that
larval fish distribution is seldom uniform vertically, and
ontogenetic changes in vertical distribution are well doc-umented in a range of species (Neilson and Perry 1990;
Leis 2006). Therefore, a broad review of vertical distri-
bution behaviour is not attempted here. Rather, some recent
examples of research on ontogenetic change in vertical
distribution using different methods will be emphasised. If
larvae do undertake ontogenetic vertical migrations, they
will be exposed differentially and in a time-dependent
manner to a range of physical and biological factors that
vary with depth. Many of these are relevant to dispersal.
The traditional means of studying vertical distribution is
by towed plankton nets or midwater trawls, and these
means have provided much valuable information. Many
net-based studies have revealed ontogenetic changes in
vertical distribution (e.g. Barnett et al. 1984), but some
have not (e.g. Boehlert et al. 1985). In a recent example, off
an island in the tropical oceanic Pacific, and using a
MOCNESS net within the upper 100 m, Irisson et al.
(2010) found that wild larvae of all five families (Apo-
gonidae, Acanthuridae, Holocentridae, Labridae, Serrani-
dae) with a significant ontogenetic change in vertical
distribution moved deeper with development (Fig. 6).
Postflexion larvae of these families were on average 25 m
deeper than preflexion larvae. In contrast, three other
abundant families (Lethrinidae, Lutjanidae, Pomacentri-
dae) lacked ontogenetic changes, although pomacentrids
had a statistically nonsignificant upward movement. Irisson
et al. (2010) point out, however, that in most families,
many postflexion larvae were present in the surface layer in
spite of the apparent downward ontogenetic migration
(which they described as a spread), and that in contrast to
preflexion larvae, postflexion larvae were abundant at
depth as well as the surface. Irisson et al. (2010) noted that
studies using towed nets cannot provide information on the
movement of individual larvae, only on mass transfers of
populations that integrate the movement of many individ-
uals (Pearre 2003). They further note that what is inter-
preted from net tow data as ontogenetic migration might be
the result of the differential distribution of mortality, and
that in such a case, larvae may not actually move vertically.
This study clearly shows some of the advantages and
limitations of studying vertical distribution in the most
traditional way.
Another recent study of vertical distribution using nets
found ontogenetic changes in the effects of wind on the
vertical distribution of larval hake, Urophycis regia
(Gadidae; Hernandez et al. 2009). In this case, preflexion
larval hake actively avoided turbulent surface waters cre-
ated by strong winds. In contrast, postflexion hake larvae
had a higher dispersion when strong winds increased tur-
bulence in the upper water column, presumably because the
ability of larvae to maintain a preferred vertical distribution
was compromised as wind stress increased, and this
resulted in increased variance. Interestingly, no effect of
wind stress was found when the data for preflexion and
postflexion larvae were combined. Hernandez et al. (2009)
point out the complex effect of wind on larval distribution
and dispersal: wind-driven currents can affect the hori-
zontal distribution of fish larvae, whereas wind-induced
turbulence affects the vertical distribution of larvae, which
in turn influences horizontal movement of larval fish via
depth-stratified flow.
Observations of larvae by divers provide information on
vertical movement of individual larvae in the ocean, but
over only short time periods (minutes) and in the upper
portion of the water column (20 m), both of which are
Fig. 6 Ontogenetic descent in a community of larval fishes, as
revealed from a towed-net study in the tropical open ocean (from
Irisson et al. 2010, fig. 6, copyright Limnology and Oceanography,
used with permission). Each shape represents the probability density
function of the vertical centre of mass of the larval patch sampled
over the range 0100 m. The distribution of larvae has a deeper centre
of mass as larvae develop from the preflexion to the postflexion stage
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limitations of the method. Diver observation has docu-
mented both ontogenetic ascents and ontogenetic descents
over the upper 20 m by observing reared larvae of different
sizes and ages, although an individual larva was only
observed at one size or age (Fig. 7). Ontogenetic ascents
(n = 4) were as common as ontogenetic descents (n = 3)
among the nine species (of seven families; see Table 3 for
the taxa) studied, two of which exhibited no ontogenetic
change in vertical distribution (Leis et al. 2006a, 2009a, b).
Ontogenetic vertical migrations were about equal in mag-
nitude: ascents were 310 m, descents were 37 m (values
refer to the modal depth). Vertical movement by individual
larvae can be quantified by a measure such as amplitude
(the difference between the shallowest and greatest depth
achieved by an individual larva over the period of obser-
vation, usually 10 min). In these nine species, mean
amplitude ranged from 3 to 9 m. An ontogenetic increase
in amplitude was observed in only two species (a sciaenid
and a serranid), and values were 0.50.9 m for each 1 mm
increase in size of the larvae.
Vertical distribution behaviour and ontogenetic changes
in it can also be studied in the laboratory by various means.
For example, vertical movements and the influence of light
can be studied by placing larvae in a vertical cylindrical
tank either fitted with sensors to detect movement of the
larvae (Blaxter 1973) or not (Hurst et al. 2009). Or,
changes in vertical position can be initiated and quantified
by changes in pressure. The use of such a pressure appa-
ratus showed that in larvae of two of the four families
studied (Balistidae, Pomacanthidae), barokinesis behaviour
in the laboratory was a good predictor of the depth at which
the wild larvae were captured in the ocean (Huebert 2008).
Larvae of size 316 mm were used, and based on data
presented in the paper, no ontogenetic change was found in
the predicted depth (i.e. within families, predicted depth
was not correlated with size of larvae). Based on the cap-
ture depth, monacanthids did, however, have an ontoge-
netic descent between sizes of 6 and 20 mm of about
5080 m in open ocean conditions (Huebert 2008).
Generally speaking, fish larvae are capable of regulating
their vertical distribution from about the time they hatch, sovertical distribution behaviour can have an influence on
dispersal throughout the larval phase. It is clear that
ontogenetic changes in vertical distribution are common,
and that these occur at both an individual and a population
level. A recent study of the influence of schooling on ori-
entation in settlement-stage larval fish showed that larvae
in groups had more precise vertical distribution behaviour
(i.e. the depth-frequency distribution was more narrow)
than did individual larvae (J.-O. Irisson, personal commu-
nication). So, it is possible that the ontogeny of schooling
may interact with the ontogeny of vertical distribution
behaviour.Although it is clear that vertical distribution and onto-
genetic changes vary among species, there is conflicting
evidence about the consistency of vertical distribution
patterns among related species. For example, the towed-net
study of Irisson et al. (2010) concluded that vertical dis-
tribution patterns and their ontogeny were consistent
among species or genera within a family, whereas the
diver-observation studies, albeit on a different scale, found
within-family and within-genus differences in ontogenetic
patterns of vertical distribution. In the latter studies, larvae
of one sparid species had an ascent while another had a
descent (Leis et al. 2006a), and larvae of one species of
Epinephelus (Serranidae) had an ascent, whereas a second
Epinephelus species had no ontogenetic changes in vertical
distribution (Leis et al. 2009a). Vertical distribution studies
using towed nets concern larvae that are generally smaller
than those studied by diver observation, and this may
partially explain the differences. In any case, further study
of a wider variety of species is necessary before firm
conclusions can be reached.
Conclusion
A key conclusion from this review is that ontogeny of
behaviour differs among different species, and may even
differ between congeners. Thus, caution should be applied
in any attempt to substitute the behaviour of a different
species, for example in a dispersal model. In addition, the
limited data available indicate that behavioural ontogeny
may differ among different habitats. For example, larvae of
species from cool-temperate waters swim slower at any
size, and their swimming speeds increase at a slower rate
Fig. 7 Ontogenetic descent by larvae of a sciaenid, Argyrosomus
japonicus, in a warm-temperate coastal area (depth 1520 m). Larger
larvae occur deeper than do smaller larvae. Plotted values are the
mean depths of individual larvae as observed by divers for about
10 min. Data are from the diver observation study of Leis et al.
(2006a) [Figure from Leis (2006), used with permission]
338 J. M. Leis
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per increase in size than in larvae from warmer waters.
More work is needed, especially on larvae of species in
cool-temperate waters.
A recurrent theme is whether larvae of species with
demersal (and brooded) eggs have behavioural capabilities
that differ from species with pelagic eggs. The best evi-
dence comes from studies of swimming, and on a per-size
basis, there is no difference in critical speed or endurancebetween larvae from the two spawning modes. However,
larvae from demersal (and brooded) eggs generally hatch at
larger sizes and are more developed at hatching than larvae
from pelagic eggs (Moser 1996; Leis and Carson-Ewart
2004), so on a post-hatch age basis, the former can be
expected to initially have better speed and endurance than
larvae from pelagic eggs, and thus to have more influence
on dispersal outcomes sooner. Whether this putative head
start lasts through the full pelagic larval stage depends on
growth rates. A caveat is that this spawning mode head
start should apply only within habitats. Therefore, one
should not necessarily expect, for example, larvae of aspecies with demersal eggs in cool-temperate waters to
have better initial swimming ability than larvae of a species
with pelagic eggs in tropical waters. A final consideration
is that demersal and brooded eggs are incubated in the adult
habitat, so the embryos are potentially exposed to cues
from that habitat that may aid in orientation during the
larval stage and in finding settlement habitat at its end
(Arvedlund and Kavanagh 2009). This effect would not be
expected for larvae that hatch from pelagic eggs, because
they are exposed to cues from the adult habitat for only a
short time after fertilisation, if at all.
In all measures of performancespeed, endurance,
orientation and depth selection, variation among individu-
als is often relatively high. This is the case throughout
ontogeny, and with both wild and reared larvae. The rea-
sons for this are not entirely clear, but this variation is
likely to have both genetic and environmental elements. It
is well established that individuals vary in condition (i.e.
reserves, growth rate and other measures; Leis and
McCormick 2002). Further, it is very likely that inherited
factors may either enable better performance, or may
predispose individuals to certain behaviours in a way that
varies among them (for example, swimming direction).
Regardless of the reasons, such variation has important
implications for dispersal. Individuals that swim faster or
straighter will reach their ultimate destination sooner,
which would have an obvious impact on dispersal out-
comes. Individuals that swim in different directions will
reach different destinations, or encounter different condi-
tions along the way, both of which have implications for
dispersal outcomes. Such differences may also influence
survival. However, it is also important to keep in mind that
even small average deviations from a random swimming
direction or vertical distribution can have a major effect on
the spatial distribution of larvae during their pelagic phase
and the location where they settle at the end of it.
Over much of the pelagic larval period, swimming
speeds of larvae in the ocean can be, depending on loca-
tion, of a similar magnitude to the speeds of the currents in
which the larvae swim. Therefore, over much of the pelagic
period, and certainly from the time the caudal fin forms,larvae will have the swimming ability to influence dispersal
outcomes. However, as larvae from cold water apparently
swim slower than do larvae from warm water, at any given
size they would be likely to have less influence on dispersal
than larvae from warm water. Further, because the growth
rates of cold-water species are likely to be slower than
those of warm-water species (OConnor et al. 2007), the
former will take longer to reach any given size, thus
delaying the beginning of influential swimming speeds, and
keeping larvae in a viscous hydrodynamic environment for
a longer period. The same reasoning would also apply to
the development of orientation abilities. Therefore, one canexpect larvae of cold-water species to have even less
influence on dispersal than warm-water larvae (Leis 2007),
and that which does occur will apply over a smaller pro-
portion of the pelagic period.
A major gap in our understanding of the ontogeny of
larval-fish behaviour concerns what happens at night.
Information on diel changes in the vertical distribution of
larvae is available from towed net samples, but aside from
that, almost nothing is known about diel effects, if any, on
larval behaviour or its ontogeny in the ocean. Innovative
thinking is required to develop means to study these
behaviours at night.
The behaviours and their development reviewed here
cannot be considered separately when trying to understand
and predict larval dispersal. Swimming will have a greater
influence on dispersal if it is orientated, for example, and of
course the velocity (i.e. speed and direction) of larvae will
have a major impact on their distribution. A good example
is provided by the larvae of the sparid Acanthopagrus
australis. This species has a ontogenetic change in swim-
ming direction (from toward the shore to parallel to the
shore; Fig. 5) that coincides with ascent from midwater to
the neuston, while all the time swimming faster with growth
(Leis et al. 2006a). These three behaviours and their chan-
ges will have an important and probably synergistic impact
on the dispersal of this species. Being able to study swim-
ming speed, orientation and vertical distribution simulta-
neously is one clear advantage of the diver observation
method of studying larval-fish behaviour (Leis et al. 1996).
An apparent paradox emerges from the work on swimming
in larval fishesat least for species fromwarmer water. These
larvae have the highest rates of oxygen uptake ever recorded
in exothermic vertebrates (Nilsson et al. 2007), yet they are
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capable of swimmingwithout food or restfor many days
and distances of many kilometres. In some cases this is over
100 km, or 5 9 106 body lengths (Fisher and Leis 2009).
Such high metabolic requirements combined with very high
enduranceseem at first glance to be paradoxical. This can only
be explained if the larvae of demersal reef fishes are very
efficient swimmers. This is consistent with the estimates of
Reynolds numbers for in situ speeds which indicate that reef-fish larvae swim in an inertial hydrodynamic environment.
Perhapsthisefficiency should not be surprising, because small
bats and small birds are capable of even greater endurance
with little or no food or rest (McGuire and Guglielmo 2009).
More work on the physiology of swimming in larval fishes
would be illuminating.
Study of the ontogeny of behaviour in fish larvae indi-
cates that most behaviours develop early during the pelagic
larval phase. Therefore, the passive portion of the pelagic
larval duration will be short, meaning that behaviour has
the potential to influence dispersal over most of the pelagic
larval duration, although both the quantity and the qualityof this influence will vary ontogenetically. For this reason,
models of larval-fish dispersal need to include the behav-
iours considered here and their ontogeny (Leis 2007).
Dispersal models require quantitative input on the
behavioural abilities of fish larvae throughout their pelagic
phase (Leis 2007). However, the study of the ontogeny of
behaviour in marine larval fishes is itself at an early stage
of development, so the information available to modellers
is very limited. We know most about swimming abilities
and vertical distribution, and least about sensory abilities,
in particular the range over which they can guide orienta-
tion. On the other hand, even for swimming, the number of
taxa for which there are relevant behavioural data is very
limited compared to the phyletic diversity of marine fishes.
More work is required on the full range of larval behav-
ioural abilities, and researchers should investigate a wider
range of taxa, especially species that live in cooler waters.
Acknowledgments Preparation of this review was supported by the
MTSRF, the Hermon Slade Foundation and the Australian Museum.
Most of my research cited in this paper was supported by the
Australian Research Commission (grants A19530997, A19804335,
DP0345876). Joe Nelson provided relevant literature. J.-O. Irisson
and the editors ofLimnology and Oceanography provided permission
to reproduce Fig. 6 from Irisson et al. (2010). Suzanne Bullock pro-vided editorial assistance, as did Michelle Yerman, who also helped
with data analysis. Drs Seishi Kimura, Gento Shinohara and Kunio
Sasaki invited me to submit this review to Ichthyological Research.
Reviewers provided constructive criticism. My great thanks to all.
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