ontogeny of behavior in larvae of marine demersal fishes

7/31/2019 Ontogeny of Behavior in Larvae of Marine Demersal Fishes

1/19

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


2/19

(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

326 J. M. Leis

123


3/19

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

Ontogeny of larval fish behaviour 327

123


4/19

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

123


5/19

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).


123


6/19

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,


are species means for 1 mm size





temperate taxa. Straight broken

lines correspond to relative

speeds in body lengths per

second (BL s-1

)

330 J. M. Leis

123


7/19

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


123


8/19

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


are species means for 1 mm size





temperate taxa

332 J. M. Leis

123


9/19

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


123


10/19

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

334 J. M. Leis

123


11/19

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


123


12/19

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

336 J. M. Leis

123


13/19

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


123


14/19

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

123


15/19

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


123


16/19

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.

References

Arvedlund M, Kavanagh K (2009) The senses and environmental cues

used by marine larvae of fish and decapod crustaceans to find

tropical coastal ecosystems. In: Nagelkerken I (ed) Ecological

connectivity among tropical coastal ecosystems. Springer,

Dordrecht, pp 135184

Barnett AM, Jahn AE, Sertic PD, Watson W (1984) Distribution of

ichthyoplankton off San Onofre, California, and methods for

sampling very shallow coastal waters. US Fish Bull 82:97111

Batschelet E (1981) Circular statistics in biology. Academic, London

Blaxter JHS (1973) Monitoring the vertical movements and light

response of herring and plaice larvae. J Mar Biol Assoc UK

53:635647

Blaxter JHS (1986) Development of sense organs and behavior of

teleost larvae with special reference to feeding and predator

avoidance. Trans Am Fish Soc 115:98114

Blaxter JHS (1991) Sensory systems and behaviour of larval fish. In:

Mauchline J, Nemoto T (eds) Marine biology: its accomplish-

ment and future prospect. Elsevier, Amsterdam, pp 1538

Boehlert GW, Mundy BC (1988) Roles of behavioral and physical

factors in larval and juvenile fish recruitment to estuarine nursery

areas. Am Fish Soc Symp 3:5167

Boehlert GW, Gadomski DM, Mundy BC (1985) Vertical distribution

of ichthyoplankton off the Oregon coast in spring and summer

months. Fish Bull 83:611621

Breitburg DL (1991) Settlement patterns and presettlement behavior

of the naked goby, Gobiosoma bosci, a temperate oyster reef

fish. Mar Biol 109:213221

Brett JR (1964) The respiratory metabolism and swimming perfor-

mance of young sockeye salmon. J Fish Res Board Can

21:11831226

Clark DL, Leis JM, Hay AC, Trnski T (2005) Swimming ontogeny of

larvae of four temperate marine fishes. Mar Ecol Prog Ser

292:287300

Dixson DL, Munday PL, Jones GP (2009) Ocean acidification

disrupts the innate ability of fish to detect predator olfactory

cues. Ecol Lett 13:6875

Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS,

Srinivasan M, Syms C, Thorrold SR (2008) Coral reef fish

smell leaves to find island homes. Proc R Soc B 275:28312839

Doi M, Kohno H, Taki Y, Ohno A (1998) Development of swimming

and feeding functions in larvae and juveniles of the red snapper,

Lutjanus argentimaculatus. J Tokyo Univ Fish 85:8195

Faria AM, Ojanguren AF, Fuiman LA, Gonclaves E (2009) Ontogeny

of critical swimming speed of wild-caught and laboratory-reared

red drum Sciaenops ocellatus larvae. Mar Ecol Prog Ser

384:221230

Fisher R (2005) Swimming speeds of larval coral reef fishes: impacts

on self-recruitment and dispersal. Mar Ecol Prog Ser

285:223232

Fisher R, Bellwood DR (2001) Effects of feeding on the sustained

swimming abilities of late-stage larval Amphiprion melanopus.

Coral Reefs 20:151154

Fisher R, Bellwood DR (2002) The influence of swimming speed on

sustained swimming performance of late-stage reef fish larvae.

Mar Biol 140:801807

Fisher R, Bellwood DR (2003) Undisturbed swimming behaviour and

nocturnal activity of coral reef fish larvae. Mar Ecol Prog Ser263:177188

Fisher R, Hogan D (2007) Morphological predictors of swimming

speed: a case study of pre-settlement juvenile coral reef fishes.

J Exp Biol 210:24362443

Fisher R, Leis JM (2009) Swimming performance in larval fishes:

from escaping predators to the potential for long distance

migration. In: Domenici P, Kapoor BG (eds) Fish locomotion: an

etho-ecological approach. Science, Enfield, pp 333373

Fisher R, Bellwood DR, Job SD (2000) Development of swimming

abilities in reef fish larvae. Mar Ecol Prog Ser 202:163173

Forward RB, Tankersley RA (2001) Selective tidal-stream transport

of marine animals. Oceanogr Mar Biol Ann Rev 39:305353

340 J. M. Leis

123


17/19

Guan L, Snelgrove PVR, Gamperl AK (2008) Ontogenetic changes in

the critical swimming speed ofGadus morhua (Atlantic cod) and

Myoxocephalus scorpius (shorthorn sculpin) larvae and the role

of temperature. J Exp Mar Biol Ecol 360:3138

Hernandez FJ, Hare JA, Fey DP (2009) Evaluating diel, ontogenetic

and environmental effects on larval fish vertical distribution

using generalized additive models for location, scale and shape.

Fish Oceanogr 18:224236

Houde ED (1989) Comparative growth, mortality, and energetics of

marine fish larvae: temperature and implied latitudinal effects.

US Fish Bull 87:471495

Huebert KB (2008) Barokinesis and depth regulation by pelagic coral

reef fish larvae. Mar Ecol Prog Ser 367:261269

Huebert KB, Sponaugle S (2009) Observed and simulated swimming

trajectories of late-stage coral reef fish larvae off the Florida

Keys. Aquat Biol 7:207216

Hurst TP, Cooper DW, Scheingross JS, Seale EM, Laurel BJ, Spencer

ML (2009) Effects of ontogeny, temperature, and light on

vertical movements of larval Pacific cod (Gadus macrocepha-

lus). Fish Oceanogr 18:301311

Irisson J-O, Guigand C, Paris CB (2009) Detection and quantification

of marine larvae orientation in the pelagic environment. Limnol

Oceanogr Methods 7:664672

Irisson J-O, Paris C, Guigand C, Planes S (2010) Vertical distribution

and ontogenetic migration in coral reef fish larvae. Limnol

Oceanogr 55:909919

Job S, Bellwood DR (2000) Light sensitivity in larval fishes:

implications for vertical zonation in the pelagic zone. Limnol

Oceanogr 45:362371

Job SD, Bellwood DR (1996) Visual acuity and feeding in larval

Premnas biaculeatus. J Fish Biol 48:952963

Johannes RE (1978) Reproductive strategies of coastal marine fishes

in the tropics. Environ Biol Fish 3:6584

Kavanagh KD, Alford RA (2003) Sensory and skeletal development and

growth in relationto theduration of theembryonicand larvalstages

in damselfishes (Pomacentridae). Biol J Linn Soc 80:187206

Kingsford MJ, Tricklebank KA (1991) Ontogeny and behavior of

Aldrichetta forsteri (Teleostei: Mugilidae). Copeia 1991:916

Kingsford MJ, Leis JM, Shanks A, Lindeman K, Morgan S, Pineda J

(2002) Sensory environments, larval abilities and local self-

recruitment. Bull Mar Sci 70:309340

Kohno H, Sota K (1998) Ontogenetic intervals based on the

development of swimming and feeding-related characters in

larvae and juveniles of the lumpfish, Inimicus japonicus.

Suisanzoshoku (Aquacult Sci) 46:333342

Kohno H, Taki Y, Ogasawara Y, Shirojo Y, Taketomi M, Inoue M

(1983) Development of swimming and feeding functions in

larval Pagrus major. Jpn J Ichthyol 30:4760

Lagardere F, Amara R, Joassard L (1999) Vertical distribution and

feeding activity o

ontogeny of behavior in larvae of marine demersal fishes

Documents