Ichthyol Res (2010) 57:325–342 DOI 10.

1007/s10228-010-0177-z

REVIEW

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 Ó The Ichthyological Society of Japan 2010

Abstract The development of behaviours that are relevant to larval dispersal of marine, demersal fishes is poorly understood. This review focuses on recent work that attempts to quantify the development of swimming, orientation, 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 3–15 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 8–10 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 ontogenetically 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
J. M. Leis (&) Ichthyology, Australian Museum, 6 College St, Sydney, NSW 2010, Australia e-mail: jeff.leis@austmus.gov.au

account when considering dispersal, and in particular in dispersal models. Although quantitative information on the ontogeny 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 Á Dispersal Á Orientation Á Swimming Á 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 history 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

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Thus far. More recently. The traditional view was that the behavioural abilities of marine fish larvae are so feeble as to be irrelevant to dispersal. Some published works report size as standard length (SL). Earlier reviews dealt with some aspects of the ontogeny of larval behaviour. Masuda (2009) provides an excellent recent review of the ontogeny of behaviour in larvae of pelagic fishes. and for simplicity. that is. results based on reared larvae should be checked using wild larvae (e. whereas others report total length (TL). In the present paper. 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. but acknowledge that some terminologies might refer to them by other labels. and little has been quantitative (Arvedlund and Kavanagh 2009). so in this paper. Arvedlund and Kavanagh 2009). Regression statistics reported in Table 2 are from the publications cited in Table 1. and use them in behavioural comparisons of part of the pelagic larval phase (e. and comparisons involving younger larvae are very rare. speed measured in a laboratory container without any intentional intervention by the investigator. Generally. 2007). especially those of rocky and coral reefs. These laboratory studies were based on a measure called ‘‘routine speed’’. except where labelled as body lengths per second (BL s-1). Boehlert and Mundy 1988. including those produced by predators. but the research reviewed here shows this view to be wrong. 1991. 2009). passive nets or seines.326 J. demersal fishes that includes all posthatch stages prior to settlement that are subject to pelagic dispersal. not just when larvae are ready to settle. Miller et al. M. This review concentrates on the ontogeny of behaviours and sensory abilities that are relevant to the dispersal of demersal fish species: swimming. often feeding. is critical to understanding how larvae survive and disperse in the sea (Kingsford et al. Most authors have ignored possible differences between day and night in swimming behaviour. Sensory abilities have been less studied. but for this review adopt an ecological perspective of ontogeny of behaviour in marine. and reared larvae may frequently have a wider range of growth rates than wild larvae. 1988. have received attention (Leis 2006).g. with many different systems of terminology and no consensus on the most appropriate. nearly all studies of swimming ontogeny have utilised reared larvae. the majority of research has been on structural rather than functional development of sense organs. Noakes and Godin 1988). Therefore. hearing and olfaction. I refer to the young fish considered here as larvae. nearly all research on the behavioural ontogeny of demersal fishes has been done with reared larvae. vertical distribution. To avoid awkward phrasing. they have implicitly assumed that the larvae actively swim constantly in the ocean. Routine speed returns swimming speeds that are much lower than those found by other methods (see Fisher and 123 . the plotted values are mean swimming performance for each 1 mm increment in size. but few marine demersal species were included (Blaxter 1986. Therefore. Clark et al. particularly swimming and orientation. and laboratory tank size. It emphasises recent research results. The emphasis in the present paper is on larvae of marine demersal fishes. yet a knowledge of the capacity of larvae to detect and respond to sensory cues. Ideally. 2002. in wild larvae. attempts to put these into context. behaviours relevant to dispersal. This is seldom possible due to the difficulty of obtaining wild larvae over a range of developmental stages. vision. Leis (Miller et al. In this paper. Yet. it is important to be clear about what is being measured and to avoid mixing different measures. speed is reported as cm s-1. Leis et al. and this will introduce a small amount of additional variation into the figures. With the exception of studies of vertical distribution based on samples taken with plankton nets or midwater trawls. Fisher and Leis 2009).g. size will be used as a proxy for developmental stage in preference to age. 2005. All studies have found a wide variation in swimming performance at any size. Smith and Fuiman 2004. time since feeding. but it may be possible to obtain wild settlement-stage larvae with light traps. The nomenclature of early life-history stages of fishes is complex. Faria et al. Further. and points out directions for future research. when attempting to apply the results of their studies that typically measured swimming speed over only short periods. and much research has taken place in the last 20 years. Swimming Various methods of measuring swimming ability provide vastly different measures. 1988. or at least that the proportion of time spent swimming does not change temporally. Laboratory studies (reviewed in Leis 2006) show that many factors can influence either the proportion of time spent swimming or the swimming speed itself. size may or may not be a better proxy than age: this simply has not been tested. and wrong for a large portion of the pelagic larval stage. No attempt has been made here to convert TL to SL. Pearre 2003). I do not attempt to distinguish between larvae and juveniles. orientation. size has been found to be a better predictor of swimming ability than age (Leis 2006). 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. However. including food density.

The present paper focuses on research that addresses ontogeny of performance rather than ontogeny of morphology. But. ‘‘rush and manoeuvrability’’. or were inactive and hung in the water without swimming. (2007. Taki et al. for example. 1997. (2000) 327 Leis et al. (2006a). the comparison of temperate species in the temperate environment versus tropical species in the tropical environment. an attempt is made to compare swimming performance among taxa and among the environments occupied by the study species (e. (2007. this may not matter.g.g. (2005). (2007. (2008) Fisher et al. or to predict swimming performance from larval morphology. studies of routine speed will not be included here except for the important work of Fisher and Bellwood (2003). In reality. Late in the larval phase of an anemonefish. Faria et al. but between the combination of environments and the species that occur in them. In this context. Kohno and Sota 1998) described the development of fins and 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. 2009a) Clark et al. 1987. day and night swimming behaviours are unlikely to be equivalent. (2006a) Guan et al. 1983. 2007) Leis et al. and that the proportion of time spent swimming may vary ontogenetically. In this section. (2008) Ryland (1963) Perciformes Perciformes Scorpaeniformes Pleuronectiformes a Serranidae Sparidae Cottidae Pleuronectidae Tropical Warm-temperate Cool-temperate Cool-temperate 3 2 1 1 2 2 1 Values are the number of species studied Adults of the study species live in rivers and upper estuaries. These ontogenetic and day–night differences in speed and proportion of time spent swimming in the laboratory indicate that in the ocean. That is. Doi et al. 2009a) Clark et al. temperate). (2005) Leis et al. 1998. it is difficult to apply these descriptive measures to questions of dispersal. At night. Leis et al. 2009b) Leis et al. These behaviours will be difficult to study in the ocean. However. 2009b) Fisher et al. it is not possible to determine if any differences revealed in these comparisons are due to taxonomic differences or to environmental differences. 2009a) Leis et al. They found that larvae of five species (families Apogonidae and Pomacentridae) swam constantly during the day. (2005). Narisawa et al. because when considering the influence of behaviour on larval dispersal and how this may differ among locations or environments. because not only the species but also the families and in some cases the orders of fishes differ among environments. (2000) Clark et al. but few studies have correlated the two. (2007. active larvae swam nearly twice as fast at night as during the day (inactive individuals were not included in this calculation). (2006b. the only meaningful comparison is not just between different environments. or to some combination of the two. Kohno and co-workers (Kohno et al. the comparisons are confounded taxonomically. but larvae are found in coastal and estuarine environments of SE Australia Leis 2009). (2009) Leis et al. but more research is undoubtedly required. (2007. Leis et al. Fisher and Hogan (2007) were able to predict the critical 123 .Ontogeny of larval fish behaviour Table 1 Demersal marine fish taxa for which the ontogeny of swimming speed has been studied in larvae Order Gonorynchiformes Gadiformes Perciformes Perciformes Perciformes Perciformes Perciformes Perciformes Perciformes Perciformes Perciformes Family Chanidae Gadidae Apogonidae Carangidae Ephippidae Leiognathidae Lutjanidae Percichthyidaea Polynemidae Pomacentridae Sciaenidae Habitat Tropical Cool-temperate Tropical Tropical Tropical Tropical Tropical Warm-temperate Tropical Tropical Warm-temperate Critical speed 1 1 1 2 1 1 1 1 1 2 2 1 1 1 1 1 1 1 1 2 1 1 1 1 In situ speed Endurance Reference Leis et al. It would be very useful to predict swimming performance from morphology. increasing to about 60–80% at the end of the pelagic period. individual larvae were either active and swam constantly as during the day. and for that reason. ‘‘complete swimming ability’’). with a mean of 34% across the full larval period. without quantitative information on speed or endurance. but at night younger larvae swam only about 15% of the time. tropical vs. (2007) Guan et al. ‘‘less active swimming’’. it is only relevant to examine the taxa that naturally occur in the location or environment in question.

Putting larval-fish swimming speeds into an ecological context is not always easy. P \ 0. 1) serve as reminder that any such relationship is almost certain to be temperature and taxon dependent. even if a different relationship between morphology and speed might be found in species from colder environments. Settlement-stage larvae have very well developed fins. M. in part depending on the direction that is swum. leading to the concept of ‘‘influential speed’’. musculature and other swimming structures that are absent or incompletely developed in smaller larvae.0001. but it is not the speed at which larval fishes swim in the ocean (Fisher and Leis 2009). P. a scorpaeniform. Leis speed (Ucrit.g. 2008) found a significant relationship between total length (mm) and speed [Ucrit = 0. But. once again. Fisher et al. Sources of data are shown in Table 1. see below) of wild. and Fisher and Hogan (2007) rightly caution that predictions based on their model are unlikely to apply to smaller. and different approaches have been attempted. Critical speed is relatively easy to 123 .03. Hollow symbols are warmtemperate taxa.328 J. larger symbols with thick borders are cool-temperate taxa. personal communication]. (2008) wrote ‘‘dah’’ (days after hatch) instead of TL. An attempt to predict Ucrit from size alone for larvae of four cold-temperate marine species (a gadiform. Guan et al. Solid dark symbols are tropical taxa. Critical speed Critical speed (Ucrit) is a laboratory raceway measure of potential swimming ability: speed is increased incrementally in short (2–5 min) steps until the larva can no longer swim against the current (Brett 1964. Clearly.79 TL . but this is an error. can often enable larvae to reach a coastal settlement habitat when passive larvae would not (e. Porch 1998). 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. a salmoniform. For example. and a pleuronectiform. 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. Leis and Stobutzki Fig. settlement-stage larvae from a few morphological measures. which is frequently parallel to depth contours in continental shelf waters. this approach has potential. Straight broken lines correspond to relative speeds in body lengths per second (BL s-1) 1999) can leave the mistaken impression that larvae that are slower than the effective speed will have little influence on dispersal. sustained swimming at almost any speed has the potential to influence dispersal outcomes. Note that Guan et al. 1 Ontogeny of critical speed (Ucrit) in larvae of marine demersal fishes. which is much lower than ‘‘effective speed’’. Snelgrove. Several larvalfish modelling exercises (reviewed in Leis 2006) have concluded that speeds of 2–3 cm s-1 are able to influence dispersal outcomes. swimming at speeds that are slower than local currents but normal to the current direction.90. Critical speed is a very useful standard comparative measure of the prolonged swimming speed of fishes. what is ‘‘ecologically meaningful’’ is context dependent. The slow speeds of these coldwater species compared to tropical species (see Fig. Solid medium. In reality. including body size (they had measures of both morphology and speed for 100 mostly tropical species).2. Plotted values are family means of up to three species for 1 mm size increments. less developed larval stages. R2 = 0. 2000). The concept of ‘‘effective speed’’ (meaning a swimming speed on average at least as fast as the average current in a particular location. however. That is.

whereas the species larger than 2.e. one blenniid and one acanthurid. at about the size at which the larvae settle. Fisher 2005). larvae of tropical taxa are fast throughout development. and consistently swim at about 5 (BL s-1) over the size ranges tested (Fig. serranid and lutjanid larvae increase rapidly in speed with size (2–3 cm s-1 per 1 mm increase in size). but at sizes larger than 5 mm. but five are warm-temperate in distribution. average current speeds of 10–15 cm s-1 are common in many coastal environments (Fisher 2005). However. with critical speeds faster than 10 cm s-1 and with most species swimming at 15–20 BL s-1 for much of their larval phase (pomacentids reach almost 30 BL s-1). Leiognathidae. only the last of which has pelagic eggs. information on Ucrit at hatching is available for a few coralreef fishes (six pomacentrids. 1.Ontogeny of larval fish behaviour 329 measure. On a per-size basis. Comparisons of critical speed to ambient currents are problematical because larvae seldom swim at their critical speed in the ocean. Therefore. The ontogeny of critical speed has strong phylogenetic and environmental influences. By assuming that the among-species increase in speed with size applied throughout the larval phase. so perhaps this should be expected as part of the transition between pelagic and demersal environments. 1. larvae of pomacentrids are among the fastest swimmers. current speeds vary widely among locations and times. of course. Notable exceptions are the tropical families Lutjanidae and Serranidae.5–4. The plotted points are family values (means of 2–3 species in six families. It can be seen from Fig. speed in body lengths per second. sciaenids remain at 10 BL s-1. Among these ten species. hence there is more information on the ontogeny of Ucrit than for other measures of swimming performance. BL s-1) to remain approximately constant (Fig. The ontogeny of critical speed has been reported for 22 marine species in 15 families (Table 1). A post-settlement decrease in critical speed was documented in pomacentrids (Stobutzki and Bellwood 1994). (2007) regarding physiological changes associated with settlement]. and four are from cool-temperate environments (Table 1). Great Barrier Reef) for more than 50% of their larval phase.25 mm at hatching swam at speeds of 2–4 cm s-1. 1). Sparidae. which means that larvae of many tropical and warm temperate species are capable of effectively opposing currents from sizes of 5 to 10 mm. Based on these limited data. Aside from the serranids and lutjanids mentioned above. two apogonids. a departure from a positive relationship between size and speed is possible at larger sizes. after the exceptionally large fin spines have reached maximum relative size and are becoming relatively smaller. Polynemidae) and perhaps three more (Serranidae. Fisher’s prediction was not very different from the empirical data in Fig. and attempts to predict swimming speeds of pelagic larvae from those of recently settled individuals should be done with great caution [for example. and. Smaller larvae of these families are much slower than similar-sized larvae of other families. 1).24 cm s-1 for each 1 mm increase in hatching size. 1). whereas sparids and percichthyids larger than 7–8 mm can swim at 15–20 BL s-1. (2008) plot (their fig. From about 7 to 9 mm. the most common pattern is for the relative speed (i. see Nilsson et al. and as settlement approaches. 123 . speed increased at a rate of 1. although it appears that at least two families (Lutjanidae. In addition. Gadidae. Larvae of taxa that are distributed in cool-temperate waters (Pleuronectidae. they are among the fastest larvae tested. 1).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. 1). 1 that critical speed increases with size. 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).e. In addition to the data summarised above that cover a substantial portion (but not all) of the pelagic larval phase. in contrast. Guan et al. Cool-temperate species. Larvae of taxa distributed in warm-temperate waters (Sciaenidae. and further. Aside from the decrease in speed at larger sizes noted above. and influencing their dispersal when considerably smaller. Ontogenetic data on critical speed are summarised in Fig. Percichthyidae) are more variable in the development of critical speed. did not reach an average critical speed of 10 cm s-1 over the measured size range (Fig. Most of the species are tropical (n = 13). Pomacentridae) have a decrease— or at least a levelling off—in critical speed at the largest sizes. i. 5) but do not formally analyze Ucrit data from two other species of cool temperate fishes—an osmerid and a pleuronectid—which have size versus speed relationships similar to the other cool-temperate taxa in Fig.25 mm at hatching (two pomacentrids and the acanthurid) had speeds that were virtually zero. Larvae of such taxa are initially relatively slow (5–10 cm s-1). and single species values for nine families). although percichthyids and carangids are faster than pomacentrids at certain sizes (Fig. 1. 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. where small larvae have exceptionally large spines in the dorsal and pelvic fins (Leis and Carson-Ewart 2004). and their critical speed does not exceed 5 cm s-1 until about 7–9 mm (Fig. Larvae smaller than 2. These just hatched larvae (1. Cottidae) have some of the slowest reported critical speeds. 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.

because of their slower speed. no in situ studies of larvae of cool-temperate species are available. because viscosity is higher at lower temperatures. For temperatures above 20°C. It is not generally possible to measure both critical and in situ speed in the same individual.28 (Table 2). but the ratio of the two varied with species (Table 2). some species decreased in speed at larger sizes: Epinephelus coioides. but it is now considered that these values should be closer to 300 and 1. M.19 to 2. the exception being the lutjanid Lutjanus malabaricus. For nine of the ten species above. Solid dark symbols are tropical taxa. fish larvae swimming at the critical speed (Fig. and is therefore temperature dependent. and values for the tropical species ranged widely from about 2 to 18 BL s-1. because it is thought that it is too energetically costly to swim any significant distance in a viscous environment. Sources of data are shown in Table 1. Hollow symbols are warmtemperate taxa. In situ speeds are lower than critical speeds. but the slope of that relationship varied widely among species. larvae of cool-temperate species will not reach Re 300 until 10–11 mm. larvae in warmer water will be capable of swimming in a largely inertial hydrodynamic environment. but generally being higher. As with the critical speed. with values generally between 3 and 15 BL s-1. for most of the pelagic larval phase. 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 overall mean of the ten species-specific ratios of in situ 123 . Therefore. and because of the difficulties involved in working with very small larvae (\5–6 mm).000. At any size. In situ speed Much less information is available on the ontogeny of swimming of larvae in the ocean. In situ speed was nearly always slower than critical speed (Fisher and Leis 2009). encompassing the speeds of the warm-temperate species. 1) will reach Re 300 by 5–8 mm. so comparisons between the two measures are based on mean values within 1 mm size increments. 2). Eleutheronema tetradactylum and Caranx ignobilis. or in situ speed (Leis and Carson-Ewart 1997). in situ speed data are available for a narrower range of larval sizes than for Ucrit. The relationship between size and speed is more complex and variable for in situ speed than it is for critical speed (Fig. Unfortunately. there is a positive linear relationship between size and in situ speed. In half of the ten species above. Plotted values are species means for 1 mm size increments. there was a significant positive correlation between size-specific measures of critical and in situ speed. 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). and the increased viscosity of cold water. The value of Re is inversely dependent on the viscosity of sea water. Straight broken lines correspond to relative speeds in body lengths per second (BL s-1) J.330 Fig. In contrast. from 0. Leis Much interest has been expressed about when fish larvae move from swimming in a viscous hydrodynamic environment to an inertial one. 2 Ontogeny of in situ speed in larvae of marine. warm-temperate species were slower by 4–10 cm s-1 than tropical species. depending on the species. respectively (see Leis 2006). demersal fishes. The three warm-temperate species had relative speeds of 3–8 BL s-1. for which there was not a significant relationship between size and in situ speed.

6 to 1.4 0.65).13 NS 0.003 Tropical non-reef Tropical reef Tropical non-reef Warm-temperate Tropical reef Tropical reef Warm-temperate Warm-temperate The P value is for the null hypothesis that the slope of the regression line is not different from zero. temperatures. with a narrow range of values: 0. yet the larval stage lasts for days to months.002 0.87 0. 2008). If true. the ratios are relatively low. 2009).80 Slope 95% CI -0. The medians are significantly different (Wilcoxon rank-sum test. ‘‘temperature influences the trajectory of larval critical swimming speed development.31 (n = 3).91.18 2.081 NS 0. Ucrit) in the ocean than do temperate species. In warm-temperate species.34 U ? 5.065. A recent study of the influence of schooling on orientation in settlement-stage larval fishes showed that larvae in groups swam about 10% faster than individual larvae (J.19 U ? 3.05). relatively little attention has been paid to the influence of temperature on the development of swimming abilities in larvae.00 0.92 U .41–0.45 1.66 U . or taxa.31 0. larvae are swimming as fast as average currents in many coastal areas. Further research in this area is needed (see.3 to 7.4 0.9 -0.7 -0.1 to 0.1 0.29.80 0. Clearly.098 NS 0. and 95% CI = 0.24 U ? 9. Irisson. 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. Swimming endurance is measured by forcing unfed larvae to swim to exhaustion in a laboratory raceway at a constant speed (Stobutzki and Bellwood 1997). 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.91.52 0.8 1.080 NS 0.-O.43 Habitat Tropical reef Tropical reef 331 0. and a much higher median (0. n = 7).8.Ontogeny of larval fish behaviour 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 Carangidae Ephippidae Leiognathidae Lutjanidae Polynemidae Sciaenidae Serranidae Serranidae Sparidae Sparidae Species Caranx ignobilis Platax teira Leiognathus equulus Lutjanus malabaricus Eleutheronema tetradactylum Argyrosomus japonicus Epinephelus coioides Epinephelus fuscoguttatus Acanthopagrus australis Pagrus auratus IS 0. This suggests that the relationship between critical speed and in situ speed may differ between environments.2.009 0.29 0.e. for example.91 0. This mean value is similar to the 0.28 U .63 0. most larvae for which there are data on in situ swimming abilities were swimming at Reynolds numbers larger than 300.8. The tropical species have a wider range of values (0.67 0.4 to 5.03 0.26 U ? 0.31 and 0.38 0.03 0.26 0.39–0.2 to 1. So.72). but it is important to keep in mind that all such species are from warm-temperate or tropical environments. In most published 123 .068 NS 0.57 (SE = 0. and they swim at speeds considered by dispersal modellers to be ‘‘influential’’ for dispersal outcomes (i.e.016 0. and that tropical species may swim closer to their potential speed (i. NS not significant Sources of data and statistical analyses are given in Table 1 speed to critical speed (based on 1 mm size increments) was 0. Mean in situ speed reaches 10 cm s-1 at 8–18 mm. 2). but that the relationship is species-specific’’ (Guan et al.1 0. As noted in the original publications (Table 1). P \ 0. At 10 cm s-1. so it is important to know when during ontogeny larvae are capable of swimming over periods and distances that are ecologically meaningful. The ratios of in situ speed to critical speed seem to differ among taxa from different environments. The time or distance over which larvae can swim is called endurance.0 -0.7 to 8.2 to 1. and a value of about 50% of the critical speed seems a reasonable central value for in situ speed. Munday et al. larvae in the ocean do not swim as fast as they are able.10. median 0. Until now. and is typically reported as kilometres swum rather than as hours swum.45 U ? 1.17 0. but the values for individual species ranged from 0. personal communication). Endurance Critical speed and in situ speed are typically measured over minutes.65 0. 0.29 to 0. and thus out of a hydrodynamic environment dominated by viscous forces.43. then comparisons of critical speed between different environments may not be informative about possible differences in swimming speeds in the ocean.1 to 0.1 -0. Larvae swim in the ocean at 5–15 BL s-1 throughout most of their pelagic period (Fig.69 U .5 ratio determined from studying settlement-stage larvae (Leis and Fisher 2006).3 P Overall mean IS/U 0.2 to 1. depending on species. more than 3 cm s-1) for most of their pelagic period (Leis 2006).012 0. However.39 0.55 U ? 2.0 to 0. An additional dimension of crossenvironment (or temperature) comparisons is the observation that in gadids and cottids.

there are few comparisons of reared and wild larvae for endurance. Clearly. Leis studies. Fisher and Leis 2009). this could lead to higher endurance estimates for reared larvae than wild larvae. the speed was the same for all developmental stages. and influence dispersal outcomes by increasing the area that larvae pass over or through. but there is at least one example where reared larvae of a pomacentrid had greater endurance than wild larvae (Leis and Clark 2005). and there are no in situ measures of endurance with which to ‘‘calibrate’’ laboratory measures of endurance. 3 Ontogeny of endurance swimming in larvae of marine demersal fishes. Sources of data are shown in Table 1. 3). thus increasing the possibility of finding a suitable habitat by chance. The ontogeny of endurance swimming has been studied in only nine species of eight families (Table 1. 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.332 Fig. provide some indication of when larvae are able to swim meaningful distances in the ocean. measuring endurance swimming in this way is problematical for several reasons. Second. Hollow symbols are warmtemperate taxa J. If so. Unfortunately. and all involve settlement-stage larvae. Between 7 and 10 mm. Fig. and endurance (distance swum) is inversely proportional to swimming speed (Fisher and Bellwood 2002). except that tropical species attain greater endurance prior to settlement. Although this provides a standard value that can be compared across taxa or developmental stages. laboratory endurance measures are not directly applicable to the ocean. but it was often variable among individuals of a species (Fig. like critical speed. Orientation Without orientation. Much more data are available on the endurance of settlement-stage larvae (see Leis 2006. it is very unlikely that larvae in the ocean actually swim to exhaustion. It is also likely that reared larvae will often have greater reserves than wild larvae due to optimal feeding conditions in rearing containers.g. however. and can grow and develop while swimming (Fisher and Bellwood 2001. In all cases. Plotted values are species means for 1 mm size increments. Endurance values do. Third. but in some (e. All studies of ontogeny of endurance were done with reared larvae. 2000). endurance started to increase. larvae that are able to feed have more-or-less open-ended endurance. primarily because many settle at larger size. 3). with values of 5–15 km. any fixed raceway speed is arbitrary. Fisher et al. speed was scaled to body size. Leis and Clark 2005). endurance values in excess of 20 km were common. and may reach 50 km or more. Finally. There is no obvious difference in endurance between warm-temperate and tropical species. endurance in larvae smaller than 7 mm was small (\4 km). By the time larvae reached the size of settlement (assuming it is more than 10 mm). at sizes larger than 7–10 mm. swimming by larvae will act primarily to increase diffusion. the endurance swimming abilities of larvae can be remarkably large. First. The two types of orientation should not be 123 . Solid dark symbols are tropical taxa. There are no endurance data for cooltemperate species. It is likely that endurance measured in this standard way is strongly influenced by larval condition or body reserves. M.

The percentage of larvae with (within trajectory) directional swimming was 67–90% in nine of the species.0–20. Fig. Irisson et al. the orientation of many larvae. location dependent Yes No Yes. the only way of doing this was by diver observations of larvae in the ocean (Leis et al. 2009b. Larvae as small as 5 mm have been studied in situ. this ratio was correlated with r (ratio of net speed to nominal in situ speed = 1.003. others not directional Higher among-individual precision with size Small larvae to N. For example. The four tropical reef species in Fig.0–20.5 13. 2006a) For E. Table 3).5–21. but the swimming directions of the two size groups were significantly different Vertical distribution of the same species was also studied confused: (1) within-individual trajectories (that is. SE = 0. the orientation of individual larvae).032.5 7.0 Yes.477.0–14. Until recently. 4). This means that individual larvae of most species do not swim randomly in the ocean. R2 = 0. 2008. 4).0 9.0 7.0–12. fuscoguttatus. 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.Ontogeny of larval fish behaviour Table 3 Studies of ontogeny of orientation of marine fish larvae Family: species Size range (mm SL) Proportion (%) of individuals significantly orientated 67 82 29 90 75 72 74 71 74 84 Among-individual orientation Ontogenetic changes in orientation Adult habitat 333 Carangidae: Caranx ignobilis Ephippidae: Platax tiera Leiognathidae: Leiognathus equulus Lutjanidae: Lutjanus malabaricus Polynemidae: Eleutheronema tetradactylum Sciaenidae: Argyrosomus japonicus Serranidae: Epinephelus coioides Serranidae: Epinephelus fuscoguttatus Sparidae: Pagrus auratus Sparidae: Acanthopagrus australis 8. only large larvae Yes No No No Bimodal directionality in small larvae. possibly due to low sample size. based on the mean bearing of individuals).593 (SE = 0.11 9 r .5–13. (2009a).0–10. 123 . significant orientation was not found in either medium or large larvae. for the four species studied by Leis et al. the within-trajectory precision is frequently low. 1996). and as expected.e. t test on arcsinetransformed data) than the mean r of the two tropical species that live on muddy or sandy bottom as adults (mean = 0.0–23.5–18. 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. medium to S.0. 4 have a mean r of 0. When values of r are plotted against size of larvae. b) Warm-temperate species were studied off southeastern Australia (Leis et al. n = 84).6 12. there is no obvious ontogenetic trend in the precision of orientation (Fig. net speed was 62–83% of the nominal in situ speed. only small larvae No Yes. and (2) among many individual trajectories (that is. but a new technique using a drifting in situ chamber (or DISC. large to N Medium larvae to shore (NW). see Batschelet 1981). 2009a. large parallel to shore (SE) Only large larvae had significant among-individual orientation Small larvae to shore (NW). only small larvae Yes. Paris et al. but this has been tested in only a few species. which is significantly greater (P = 0. Significant within-trajectory orientation is found in the large majority of individual larvae of most species that have been studied (Table 3). large parallel to shore (NE) Tropical reefassociated Tropical reef Tropical soft bottom Tropical reef Tropical soft bottom Warm-temperate estuary and reef Tropical inshore reef Tropical reef Warm-temperate estuary and reef Warm-temperate estuary and reef Tropical species were studied off southern Taiwan (Leis et al. The precision of orientation (i. can be expressed by a statistic called r (the length of the mean vector. which ranges from 0 (fully random) to 1 (entirely linear).625). Although individual trajectories are usually significantly different from random swimming. n = 42).0 7.0–9.024. 2009) offers great potential to complement and extend diver observations.0 6. none in large larvae Smallest larvae to NE (to shore).0 5. the straightness of a trajectory). 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 in situ swimming speed.5 7. Orientation has been studied only by in situ techniques. some size groups No overall Yes.08. 2006b.

However. and the authors of the study (Leis et al.g. it seems that each species must be considered individually.e. differences in orientation precision among species. All four of the studies used reared larvae.g. Leis and Carson-Ewart 2003). This shows a lack of any ontogenetic trend in within-individual orientation. either the cues used for orientation change. Ontogenetic changes in among-trajectory orientation were also found in seven of the ten species (Table 3). So. Solid dark symbols are tropical reef taxa. and in one species only the largest larvae had directional (among trajectory) swimming. Leis and only 29% in Leiognathus equulus. One might expect ontogenetic improvement in orientation. sensory abilities change. but they do not seem to improve thereafter. Solid medium symbols with thick black borders are tropical nonreef taxa. e. the motivation to respond to cues changes. 4 Ontogeny of precision of directional swimming (length of the mean vector) in larvae of marine demersal fishes. an assumption that the orientation will be spatially consistent may not be justified. that orientated swimming would be more common or more precise in larger larvae. It is unclear 123 . and none were able to compare results to anything other than wild settlement-stage larvae of related species. The last species lives as an adult in soft-bottom habitats. so we know nothing about the orientation abilities of larvae smaller than about 5 mm. 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. M. 4) or in the proportion of individual larvae that had within-trajectory orientation. 5). Fig. With only ten species studied. i. which can be problematical given the generally low overall precision of the among-trajectory orientations of larvae of many species. the variety of ontogenetic changes in among-individual orientation is somewhat surprising. and it is premature to generalise about the ontogeny of among-individual orientation. the frequency distribution of the mean orientations of individual larvae was significantly different from random. then as larvae grow. In seven of the ten species. The available studies of orientation ontogeny (Table 3) have some limitations. 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. which is a small proportion of the pelagic larval duration. If orientation changes with development. and do not improve with growth or age thereafter. e. or perhaps all three changes occur. All of these studies were based on observing larvae for at most 10 min at a time. In some cases. There are. In none of these ten species was there an ontogenetic trend in within-trajectory orientation precision either in the r statistic (Fig. The ontogeny of orientation has been studied in more than one location for very few species. So. Sources of data are shown in Table 3 J. Ontogenetic changes in orientation imply several things about the sensory cues used for orientation. among-trajectory orientation was found.334 Fig. In two species. Hollow symbols are warm-temperate taxa. Plotted values are species means for 1 mm size increments. and because location-dependent orientation has been found in settlement-stage larvae of some species (e. the number of larvae studied in some of the size classes was low. the smallest larvae studied showed significant orientation while larger larvae did not. 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). Very small larvae cannot be studied in situ with diver observation methods. it seems that orientation abilities are formed at a relatively early stage in ontogeny (by 5 mm). however.g. It is reasonable to assume that orientation abilities are poor at hatching and improve between hatching and 5 mm. the smallest individuals studied are considerably larger. and for some species. the opposite (apparent ontogenetic deterioration in orientation ability) was just as common.

and within-individual orientation precision does not improve with growth. there is room for further study of the ontogeny of orientation in larvae in marine fishes. this size did not correspond to any change in sensory organs (Masuda 2009). Above: small larvae (7–10 mm SL) swam on average in a north-west direction toward shore (n = 18). so schooling at this stage may have more to do with preparation for post-settlement existence than it does with the pelagic stage. larvae of this size do not have complete fins. In larvae of pelagic fishes. and the thin radius that penetrates the outer circle is the overall mean direction (after Leis et al. Sabate et al. directly test if the behaviours of reared and wild larvae differ. The bars represent the frequency distribution of the mean swimming directions of individual larvae. and expand taxonomic coverage. personal communication). but may not be very precise. and although their fins are fully formed. Nor is it safe to assume that larvae of demersal fishes are any different. Clearly. 2010). Yet a species in which only within-trajectory orientation is present can have an increased probability of finding settlement habitat if the larvae maintain their within-trajectory orientation over time (Huebert and Sponaugle 2009). which begins to shoal at about 6 mm (Breitburg 1991). and orientation varies among species. Schooling There are reasons to expect that larvae in groups or schools may have better orientation than individual larvae (Larkin and Walton 1969. and it is not possible to generalise. Two exceptions are the mugilid Aldrichetta forsteri. 2006a). Irisson. and the gobiid Gobiosoma bosci. but most of them also school following settlement (Leis and CarsonEwart 1998). Carangids school from 12 to 16 mm. However. Simons 2004). This is Fig. 123 . 5 Ontogenetic change in among-individual orientation in larvae of a sparid. schooling begins after fin formation is complete. Ontogenetic changes in amongindividual orientation are common. 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. which forms aggregations when as small as 4–6 mm (Kingsford and Tricklebank 1991). there seem to be a variety of patterns in the development of schooling among pelagic fishes. Bottom: large larvae (10–12 mm SL) swam on average in a north-east direction parallel to shore (n = 19). Some species are known to school shortly before settlement. 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. Especially needed are studies that examine the consistency of orientation patterns over time and at different locations. in both species. and larvae of such a species will have dispersal outcomes very different from passive drift with the currents.Ontogeny of larval fish behaviour 335 Based on the available studies. Most individual larvae swim directionally. The two frequency distributions are significantly different whether the results from such short-term studies can be scaled up to longer periods. little is known about the ontogeny of schooling in larvae of demersal fishes. thus supporting this expectation. or if schooling by larvae of demersal species is even common. Acanthopagrus australis. More work is needed on the ontogeny of schooling in fish larvae. So. 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. in coastal waters 1 km from shore.-O. A species with an overall among-trajectory orientation is able to have the greatest influence on dispersal. Among-individual orientation is common.

as schooling may strongly influence other orientation and swimming abilities. calculations based on retinal structure (Job and Bellwood 1996. and its use by juveniles and adult salmon is well established (e. Hearing abilities of fish larvae are well developed by settlement (reviewed in Arvedlund and Kavanagh 2009).g. By settlement.e. 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.g. but shows that sense organ performance increases with growth. and even before. There is no direct evidence from marine larval fishes of the latter. we can anticipate that olfaction could be used in orientation for most or all of the pelagic larval period. Many species that spawn nonpelagic eggs (i. 2002. Arvedlund and Kavanagh (2009) conclude that larvae of coral reef fishes ‘‘develop their olfactory organs rapidly (including olfactory receptor neurons)’’. Sensory abilities Orientation. However. whether vertically or horizontally. 2005). Leis especially important.g. larvae may have the ability to hear throughout their pelagic period.e. This result indicates that larvae from nonpelagic eggs have functional olfactory organs for their entire pelagic period. implying an olfactory sense while still in the demersal egg (Arvedlund and Kavanagh 2009). Vision is relevant to orientation via direct observation. concentrating on pomacentrids. M. Reviews of sensory abilities that are relevant to the orientation of fish and invertebrate larvae provide a good overview (Kingsford et al. (2008)]. where predator threats are assumed to be lower (Johannes 1978). In this review. because most studies of sensory organ structure are not clearly informative about function (for a more complete consideration of structural sense organ development. and even less has addressed the ontogeny of such abilities. 8–10 mm) were able to hear. 2009). but in most cases. see Arvedlund and Kavanagh 2009). Therefore. on the order of mm to cm (Job and Bellwood 1996. the generality of the statements in this section remains to be tested. Quinn 1980). Research on the ontogeny of these senses has included only a limited range of species and families. but circumstantial evidence exists for the use of a solar compass by pomacentrid larvae (e. vision can be used for orientation for most or all of the pelagic larval period. the development of sensory abilities is intimately related to the ability of larval fish to orientate. Vision may be relevant to orientation over much larger scales if a solar compass or some other celestial cue is used. the olfactory organs of pomacentrids and a lethrinid appear to be functional in newly hatched larvae (Arvedlund and Kavanagh 2009). Whether anemonefishes are representative of other species with nonpelagic eggs— let alone those with pelagic eggs—remains unknown. fish larvae have well-developed olfactory abilities [see reviews by Kingsford et al. and therefore of limited use to orientation by direct observation. 2006. and well before the nasal pit is roofed over. Therefore. but is limited by underwater visibility to a few tens of metres. what frequencies of sound or what 123 . All three senses considered here are functional relatively early in the pelagic larval phase. Montgomery et al. These newly hatched larvae avoided water with the scent of adult fishes. Shand 1997. Therefore. Pomacentridae) demonstrated a response to sound with increased sensitivity as the eggs developed (Simpson et al. larvae that hatch from pelagic eggs do not have functional eyes for one to a few days. (2002) and Arvedlund and Kavanagh (2009) and a recent paper by Dixson et al. and are therefore potentially useful in orientation over most of the larval phase. The only work on the ontogeny of hearing abilities in larvae of marine fishes shows that larvae as small as could be studied (i. Research on the ontogeny of sense organ function in marine demersal fishes is limited. would help them move from their hatching location on the reef and into open water. Arvedlund and Kavanagh 2009). Little work has been done on the visual abilities of larvae in the context of orientation. However. which. This section focuses on work demonstrating actual sensory function. ephippium. a study of embryos of anemonefishes (Amphiprion rubrocinctus and A. but structurally. due to uncertainties about the actual cues that larvae utilise (e. demersal or brooded) hatch with functional eyes. but there is little information on the ontogeny of olfaction in marine fish larvae. 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.336 J. requires the ability to detect and respond to cues. at least for species with demersal eggs. 2000).) imprint on the smell of the anemone taxa upon which the larvae subsequently settle. the distance over which each sense organ is effective for orientation and how this changes with growth is generally unknown. forming separate nares (Kavanagh and Alford 2003). olfaction and hearing. Leis and Carson-Ewart 2003). Embryonic anemonefishes (Pomacentridae: Amphiprion spp. Lara 2001) and anecdotal field observations of behaviour suggest that settlement-stage larvae can see underwater as well as human divers can (Leis and CarsonEwart 2001). the emphasis is on vision. rather than studies of structural development of sense organs. implying that. in the sea. However. Therefore. and that hearing ability increased with size of larvae until settlement (Wright 2006). Research on feeding behaviour in the laboratory suggests the distance over which larvae can see and respond to foodsize objects is limited.

Hernandez et al. whereas wind-induced turbulence affects the vertical distribution of larvae. Holocentridae. 1999. but over only short time periods (minutes) and in the upper portion of the water column (20 m). Serranidae) with a significant ontogenetic change in vertical distribution moved deeper with development (Fig. In contrast. three other abundant families (Lethrinidae. Forward and Tankersley 2001. which in turn influences horizontal movement of larval fish via depth-stratified flow. Paris and Cowen 2004). ` Lagardere et al. larvae may not actually move vertically. (2010) point out. some recent examples of research on ontogenetic change in vertical distribution using different methods will be emphasised. and using a MOCNESS net within the upper 100 m. 1985). and that in such a case. Labridae. they will be exposed differentially and in a time-dependent manner to a range of physical and biological factors that vary with depth. however. copyright Limnology and Oceanography. In contrast. presumably because the ability of larvae to maintain a preferred vertical distribution was compromised as wind stress increased. only on mass transfers of populations that integrate the movement of many individuals (Pearre 2003). Irisson et al. 6. Interestingly. Rather. (2009) point out the complex effect of wind on larval distribution and dispersal: wind-driven currents can affect the horizontal distribution of fish larvae. Many of these are relevant to dispersal. to advance. and these means have provided much valuable information. how cue strength varies spatially and temporally. postflexion larvae were abundant at depth as well as the surface. (2010) noted that studies using towed nets cannot provide information on the Fig.g. This study clearly shows some of the advantages and limitations of studying vertical distribution in the most traditional way. Leis 2006). Postflexion larvae of these families were on average 25 m deeper than preflexion larvae. If larvae do undertake ontogenetic vertical migrations. Barnett et al. as revealed from a towed-net study in the tropical open ocean (from Irisson et al. Urophycis regia (Gadidae. and a huge literature exists. The traditional means of studying vertical distribution is by towed plankton nets or midwater trawls. They further note that what is interpreted from net tow data as ontogenetic migration might be the result of the differential distribution of mortality.g. Irisson et al. The field of the sensory abilities of larval fishes is important. In a recent example. off an island in the tropical oceanic Pacific. 2009). Vertical distribution and migrations constitute the most studied aspect of larval fish behaviour. although pomacentrids had a statistically nonsignificant upward movement. Observations of larvae by divers provide information on vertical movement of individual larvae in the ocean. Therefore. 6 Ontogenetic descent in a community of larval fishes. whereas vertical distribution behaviour can influence dispersal only indirectly. no effect of wind stress was found when the data for preflexion and postflexion larvae were combined. Acanthuridae. Hernandez et al.Ontogeny of larval fish behaviour 337 scent). Pomacentridae) lacked ontogenetic changes. Another recent study of vertical distribution using nets found ontogenetic changes in the effects of wind on the vertical distribution of larval hake. Boehlert et al. postflexion hake larvae had a higher dispersion when strong winds increased turbulence in the upper water column. 1984). and this resulted in increased variance. that in most families. 2010. Irisson et al. It has long been known that larval fish distribution is seldom uniform vertically. Vertical distribution The behaviours involved with horizontal swimming considered above can directly influence dispersal outcomes. if difficult. fig.g. a broad review of vertical distribution behaviour is not attempted here. Many net-based studies have revealed ontogenetic changes in vertical distribution (e. Each shape represents the probability density function of the vertical centre of mass of the larval patch sampled over the range 0–100 m. (2010) found that wild larvae of all five families (Apogonidae. Lutjanidae. but some have not (e. and in spite of significant recent advances. The distribution of larvae has a deeper centre of mass as larvae develop from the preflexion to the postflexion stage movement of individual larvae. In this case. 6). how sense organ performance varies ontogenetically. through interaction with currents that are vertically stratified with respect to velocity (e. many postflexion larvae were present in the surface layer in spite of the apparent downward ontogenetic migration (which they described as a spread). used with permission). preflexion larval hake actively avoided turbulent surface waters created by strong winds. and that in contrast to preflexion larvae. and ontogenetic changes in vertical distribution are well documented in a range of species (Neilson and Perry 1990. both of which are 123 .

For example. In any case. In the latter studies. and larvae of one species of Epinephelus (Serranidae) had an ascent. Argyrosomus japonicus.-O. there is conflicting evidence about the consistency of vertical distribution patterns among related species. see Table 3 for the taxa) studied. b). The use of such a pressure apparatus showed that in larvae of two of the four families studied (Balistidae. 2006a. A recent study of the influence of schooling on orientation in settlement-stage larval fish showed that larvae in groups had more precise vertical distribution behaviour (i. fish larvae are capable of regulating their vertical distribution from about the time they hatch. barokinesis behaviour in the laboratory was a good predictor of the depth at which the wild larvae were captured in the ocean (Huebert 2008). and values were 0. Data are from the diver observation study of Leis et al. 2006a). mean amplitude ranged from 3 to 9 m. and that these occur at both an individual and a population level. the towed-net study of Irisson et al. larvae of one sparid species had an ascent while another had a descent (Leis et al. for example in a dispersal model. whereas a second Epinephelus species had no ontogenetic changes in vertical distribution (Leis et al. the depth-frequency distribution was more narrow) than did individual larvae (J. An ontogenetic increase in amplitude was observed in only two species (a sciaenid and a serranid). So. although an individual larva was only observed at one size or age (Fig. Vertical distribution studies using towed nets concern larvae that are generally smaller than those studied by diver observation. albeit on a different scale. have an ontogenetic descent between sizes of 6 and 20 mm of about 50–80 m in open ocean conditions (Huebert 2008). predicted depth was not correlated with size of larvae). Based on the capture depth.e.338 J. Plotted values are the mean depths of individual larvae as observed by divers for about 10 min. Thus. in a warm-temperate coastal area (depth 15–20 m). Diver observation has documented both ontogenetic ascents and ontogenetic descents over the upper 20 m by observing reared larvae of different sizes and ages. whereas the diver-observation studies. no ontogenetic change was found in the predicted depth (i. personal communication).e. descents were 3–7 m (values refer to the modal depth). Ontogenetic ascents (n = 4) were as common as ontogenetic descents (n = 3) among the nine species (of seven families. It is clear that ontogenetic changes in vertical distribution are common. monacanthids did. further study of a wider variety of species is necessary before firm conclusions can be reached. it is possible that the ontogeny of schooling may interact with the ontogeny of vertical distribution behaviour. In these nine species.5–0. Irisson. (2010) concluded that vertical distribution patterns and their ontogeny were consistent among species or genera within a family. Ontogenetic vertical migrations were about equal in magnitude: ascents were 3–10 m. so vertical distribution behaviour can have an influence on dispersal throughout the larval phase. found within-family and within-genus differences in ontogenetic patterns of vertical distribution. 2009a). Larvae of size 3–16 mm were used. 7 Ontogenetic descent by larvae of a sciaenid. within families. 7). Larger larvae occur deeper than do smaller larvae. 2009a. changes in vertical position can be initiated and quantified by changes in pressure. Vertical distribution behaviour and ontogenetic changes in it can also be studied in the laboratory by various means. the limited data available indicate that behavioural ontogeny may differ among different habitats. Pomacanthidae). 2009). two of which exhibited no ontogenetic change in vertical distribution (Leis et al. 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 observation. Conclusion A key conclusion from this review is that ontogeny of behaviour differs among different species. and their swimming speeds increase at a slower rate 123 . Or. 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. For example. Although it is clear that vertical distribution and ontogenetic changes vary among species. however. and based on data presented in the paper. Leis Fig. For example. used with permission] limitations of the method. larvae of species from cool-temperate waters swim slower at any size.9 m for each 1 mm increase in size of the larvae. (2006a) [Figure from Leis (2006). usually 10 min). and this may partially explain the differences. and may even differ between congeners. M. Generally speaking. caution should be applied in any attempt to substitute the behaviour of a different species. In addition.

especially on larvae of species in cool-temperate waters. Therefore. 2007). the former can be expected to initially have better speed and endurance than larvae from pelagic eggs. reserves. Such differences may also influence survival. or encounter different conditions along the way. Individuals that swim in different directions will reach different destinations. 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. A major gap in our understanding of the ontogeny of larval-fish behaviour concerns what happens at night. Further. However. for example. A good example is provided by the larvae of the sparid Acanthopagrus australis. of a similar magnitude to the speeds of the currents in which the larvae swim. Information on diel changes in the vertical distribution of larvae is available from towed net samples. Further. if any. However. 2007). or may predispose individuals to certain behaviours in a way that varies among them (for example. such variation has important implications for dispersal. In all measures of performance—speed. swimming speeds of larvae in the ocean can be. thus delaying the beginning of influential swimming speeds. and certainly from the time the caudal fin forms. both of which have implications for dispersal outcomes. at any given size they would be likely to have less influence on dispersal than larvae from warm water. swimming direction). Leis and McCormick 2002). The best evidence comes from studies of swimming. 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). Therefore. while all the time swimming faster with growth (Leis et al. and with both wild and reared larvae. 5) that coincides with ascent from midwater to the neuston. A caveat is that this ‘‘spawning mode head start’’ should apply only within habitats. larvae from demersal (and brooded) eggs generally hatch at larger sizes and are more developed at hatching than larvae from pelagic eggs (Moser 1996. The reasons for this are not entirely clear. Leis and Carson-Ewart 2004). and that which does occur will apply over a smaller proportion of the pelagic period. over much of the pelagic period. there is no difference in critical speed or endurance between larvae from the two spawning modes. the former will take longer to reach any given size.e. because the growth rates of cold-water species are likely to be slower than those of warm-water species (O’Connor et al. 2006a). Whether this putative ‘‘head start’’ lasts through the full pelagic larval stage depends on growth rates. A final consideration is that demersal and brooded eggs are incubated in the adult habitat. endurance. Regardless of the reasons. almost nothing is known about diel effects. Therefore. A recurrent theme is whether larvae of species with demersal (and brooded) eggs have behavioural capabilities that differ from species with pelagic eggs. growth rate and other measures. This is the case throughout ontogeny. depending on location. orientation and vertical distribution simultaneously is one clear advantage of the diver observation method of studying larval-fish behaviour (Leis et al. as larvae from cold water apparently swim slower than do larvae from warm water. Swimming will have a greater influence on dispersal if it is orientated. The same reasoning would also apply to the development of orientation abilities. but aside from that. This species has a ontogenetic change in swimming direction (from toward the shore to parallel to the shore. This effect would not be expected for larvae that hatch from pelagic eggs. larvae will have the swimming ability to influence dispersal outcomes. and of course the velocity (i. Fig.Ontogeny of larval fish behaviour 339 per increase in size than in larvae from warmer waters. variation among individuals is often relatively high. An apparent paradox emerges from the work on swimming in larval fishes—at least for species from warmer water. Being able to study swimming speed.e. yet they are 123 . orientation and depth selection. Innovative thinking is required to develop means to study these behaviours at night. However. and thus to have more influence on dispersal outcomes sooner. 1996). and keeping larvae in a viscous hydrodynamic environment for a longer period. one should not necessarily expect. These larvae have the highest rates of oxygen uptake ever recorded in exothermic vertebrates (Nilsson et al. It is well established that individuals vary in condition (i. larvae of a species with demersal eggs in cool-temperate waters to have better initial swimming ability than larvae of a species with pelagic eggs in tropical waters. it is very likely that inherited factors may either enable ‘‘better’’ performance. Over much of the pelagic larval period. one can expect larvae of cold-water species to have even less influence on dispersal than warm-water larvae (Leis 2007). The behaviours and their development reviewed here cannot be considered separately when trying to understand and predict larval dispersal. for example. which would have an obvious impact on dispersal outcomes. so on a post-hatch age basis. because they are exposed to cues from the adult habitat for only a short time after fertilisation. Individuals that swim faster or straighter will reach their ultimate destination sooner. on larval behaviour or its ontogeny in the ocean. These three behaviours and their changes will have an important and probably synergistic impact on the dispersal of this species. speed and direction) of larvae will have a major impact on their distribution. More work is needed. but this variation is likely to have both genetic and environmental elements. and on a per-size basis. if at all.

DP0345876). as did Michelle Yerman. Bellwood DR. Academic. models of larval-fish dispersal need to include the behaviours considered here and their ontogeny (Leis 2007). Job SD (2000) Development of swimming abilities in reef fish larvae. Bellwood DR (2003) Undisturbed swimming behaviour and nocturnal activity of coral reef fish larvae. who also helped with data analysis. J Tokyo Univ Fish 85:81–95 Faria AM. and least about sensory abilities. Drs Seishi Kimura. meaning that behaviour has the potential to influence dispersal over most of the pelagic larval duration. Mar Ecol Prog Ser 202:163–173 Forward RB. Sertic PD. Perhaps this efficiency should not be surprising. Suzanne Bullock provided editorial assistance. Mundy BC (1988) Roles of behavioral and physical factors in larval and juvenile fish recruitment to estuarine nursery areas. Pratchett MS. References Arvedlund M. pp 15–38 Boehlert GW. 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Acknowledgments Preparation of this review was supported by the MTSRF. A19804335. the study of the ontogeny of behaviour in marine larval fishes is itself at an early stage of development. J Mar Biol Assoc UK 53:635–647 Blaxter JHS (1986) Development of sense organs and behavior of teleost larvae with special reference to feeding and predator avoidance. Enfield. Such high metabolic requirements combined with very high endurance seem at first glance to be paradoxical. the passive portion of the pelagic larval duration will be short. Fish Bull 83:611–621 Breitburg DL (1991) Settlement patterns and presettlement behavior of the naked goby. Fuiman LA. Thorrold SR (2008) Coral reef fish smell leaves to find island homes.340 J. This can only be explained if the larvae of demersal reef fishes are very efficient swimmers. Srinivasan M. Coral Reefs 20:151–154 Fisher R. US Fish Bull 82:97–111 Batschelet E (1981) Circular statistics in biology. even for swimming. Ojanguren AF. 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Most of my research cited in this paper was supported by the Australian Research Commission (grants A19530997. Joe Nelson provided relevant literature. Leis JM. Munday PL. Irisson and the editors of Limnology and Oceanography provided permission to reproduce Fig. and methods for sampling very shallow coastal waters. Mar Ecol Prog Ser 384:221–230 Fisher R (2005) Swimming speeds of larval coral reef fishes: impacts on self-recruitment and dispersal. In: Domenici P. Kapoor BG (eds) Fish locomotion: an etho-ecological approach. Elsevier. Jones GP. pp 135–184 Barnett AM. Kavanagh K (2009) The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems. (2010). Springer. Dispersal models require quantitative input on the behavioural abilities of fish larvae throughout their pelagic phase (Leis 2007). pp 333–373 Fisher R. Hay AC. For this reason. Planes S. Syms C. J Exp Biol 210:2436–2443 Fisher R. 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