Recently, it has become apparent that the swimmingabilities of marine fish larvae, at least those of perci-form species, are considerable (Leis 2006). As theyapproach the settlement stage, larvae of many species
can swim at speeds similar to those of the ambient cur-rents in which they conduct the pelagic portion of theirlife history (Fisher 2005). This capacity provides larvaewith the ability to strongly influence their dispersal tra-jectories. Therefore, knowledge of the swimming abil-ities of larvae is of more than academic interest as
Ontogeny of swimming speed in larvae of pelagic-spawning, tropical, marine fishes
Jeffrey M. Leis1, 3,*, Amanda C. Hay1, Matthew M. Lockett1, Jeng-Ping Chen2,Lee-Shing Fang2, 4
1Ichthyology, Australian Museum, 6 College Street, Sydney, New South Wales 2010, Australia2National Museum of Marine Biology and Aquarium, 2 Houwan Road, Checheng, Pingtung 944, Taiwan
3School of Biological Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052,Australia
4Present address: Department of Sport, Health and Leisure, Cheng Shiu University, 840 Chengcing Road, Niaosong hsiang,Kaohsiung County 83347, Taiwan
ABSTRACT: During the pelagic larval phase of teleost fishes, the larvae are subject to dispersal bycurrents. Dispersal trajectories can be substantially modified if the larvae have sufficient swimmingabilities, so it is important to document how swimming ability develops during the pelagic larvalphase. We used reared larvae (4 to 29 mm standard length) from commercial aquaculture farms inTaiwan to measure the development of swimming ability (critical speed, Ucrit) in larvae of 9 species(from 7 families) of Indo-Pacific coral reef and coastal fishes that hatch from pelagic eggs: Trachino-tus blochii (Carangidae – jacks), Chanos chanos (Chanidae – milkfish), Platax teira (Ephippidae –batfishes), Leiognathus equulus (Leiognathidae – ponyfishes), Lutjanus malabaricus (Lutjanidae –snappers), Eleutheronema tetradactylum (Polynemidae – threadfins), and Epinephelus coioides,E. fuscoguttatus and E. malabaricus (Serranidae – groupers). Mean critical swimming speedsincreased from <5 cm s–1 in the smallest larvae to a maximum of 47 cm s–1 in settlement stage larvae,with the increase in speed by the time of settlement ranging from 6- to 100-fold. Increase in swim-ming speed was more strongly correlated with size of larvae (R2 = 0.38 to 0.93, p < 0.005) than withage (correlation with age was absent in 3 species and explained 10 to 43% less variation than did sizein the others). The relationship between speed and size was linear. In 6 species (T. blochii, C. chanos,L. malabaricus and the 3 Epinephelus species) speed increased at a rate of 2.1 to 2.6 cm s–1 for each1 mm increase in size. Three species (P. teira, L. equulus and E. tetradactylum) had a significantlyslower rate of increase of 1.3 to 1.7 cm s–1 for each 1 mm increase in size. On average, the best per-formers in each 1 mm size increment were 1.5 to 7.3 cm s–1 faster than mean performers, dependingon species. Throughout development the vast majority of mean length-specific speeds were 10 to 20body lengths (BL) s–1, and length-specific speed increased significantly with size in 6 species. Maxi-mum length-specific speeds for each species reached 18 to 31 BL s–1. Although the ontogeny of swim-ming speed varies among species of tropical marine fishes, over similar size ranges, larvae that hatchfrom pelagic eggs have swimming abilities similar to those reported for larvae that hatch fromdemersal eggs.
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 349: 255–267, 2007
numerical biophysical models require good measuresof swimming ability if they are to realistically predictdispersal outcomes (Cowen et al. 2006, Leis 2007).
Most recent estimates of swimming ability of marinefish larvae have been made with a laboratory methodcalled critical speed (Ucrit) (Brett 1964) that uses a race-way and incremental increases in speed until the lar-vae can no longer maintain position (Stobutzki & Bell-wood 1994, Fisher et al. 2000, 2005, Fisher 2005, Leis &Fisher 2006). The Ucrit is a convenient standard methodof measuring potential swimming ability and is, there-fore, ideal for comparing the performance of differentspecies or developmental stages of fish. Measurementsof Ucrit are now available for the larvae of a wide vari-ety of mostly tropical, perciform fish species. However,the vast majority of these data are only from the latesettlement-stage larvae of these species (Fisher 2005,Fisher et al. 2005, Leis & Fisher 2006), whereas bio-physical dispersal models require information onswimming ability throughout the pelagic larval phase(Leis 2007). At present, Ucrit data across a wide range ofdevelopmental stages are available for only 8 speciesof 6 families of marine fishes (Fisher et al. 2000, Clarket al. 2005, Leis et al. 2006a): 2 coral-reef pomacen-trids, one coral-reef apogonid, one reef-associatedcarangid, 2 warm-temperate sparids, a warm-temper-ate sciaenid and a warm-temperate estuarine perci-cithyid. In addition, Fisher (2005) presented ‘nor-malised’ larval swimming speed data on 2 otherpomacentrids and an apogonid, and although thesehad performance similar to their confamilials, the
actual speed-at-age data were not included). Thepomacentrids and apogonids are small fishes thatspawn non-pelagic eggs, whereas the other 5 speciesconsist of moderate to large fishes that spawn pelagiceggs. In all these species, larvae settle at a relativelysmall size (8 to 13 mm standard length, except thepelagic carangid, which does not settle) and have rela-tively direct development with few larval specializa-tions (Neira et al. 1998, Leis & Carson-Ewart 2004). Asvaluable as these data are, the vast diversity of marineteleost fishes is not well represented by these 8 spe-cies, and many of the families of most interest toecologists and managers are not included.
We sought to expand the taxonomic coverage ofontogenetic Ucrit data by studying a number of marinespecies common in the aquaculture industry in Taiwan(Yu 2002). Working from the National Museum ofMarine Biology and Aquarium (NMMBA, Pingtung,Taiwan), we were able to obtain quantitative data onthe ontogenetic increase in swimming ability of 9 spe-cies in 7 families (Table 1, Fig. 1). These include spe-cies from a variety of habitats and of considerable com-mercial and ecological interest. None of the genera westudied here, and only one of the families, had previ-ously been studied in this manner. This more than dou-bles the species for which the ontogeny of Ucrit swim-ming performance in the larvae is known and extendssuch measurements to species that settle at sizes up toca. 25 mm standard length (SL). The species studiedhere (Table 1, Fig. 1) include one gonorynchiform spe-cies (Chanos chanos) and 8 perciform fishes. The
256
Family and species Adult habitat Settlement Ucrit N Cohortssize size (with (d)
Table 1. Study species and characteristics. Adult habitat and settlement size information from Bagarinao (1991), Doi et al. (1991),Kohno et al. (1993), Leu et al. (2005), Australian Museum fish database and authors’ unpublished data. N is number of specimensfor which Ucrit was measured (and the number in parentheses for which age was known). Cohorts refers to the number of separate
groups of larvae studied; d = no. of days during which Ucrit was measured. nd = no data available
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes
chanid and polynemid species have rela-tively direct development with few larvalmorphological specializations, whereasthe ephippidid, leiognathid, lutjanid andserranid species have highly specializedlarvae with morphologies that differ sub-stantially from the settled juveniles. Sim-ilarly, the size at which the larvae leavethe pelagic environment varies fromabout 12–13 mm (Chanidae) to about20–25 mm (Polymenidae, Lutjanidae,Serranidae).
The goals of this study were to mea-sure the development of swimming abil-ity (defined as Ucrit) across a range of spe-cies, families and early life history stagesof tropical fishes, and to compare thepatterns of swimming developmentamong these and other taxa for whichsimilar data were available. We sought tocharacterize the ontogeny of swimmingin these species (for example, to deter-mine if the increase in speed with sizewas essentially linear, as has been deter-mined in other species) and to make thisinformation available to investigatorswho increasingly are including larvalbehaviour in dispersal models.
MATERIALS AND METHODS
Larvae were obtained from commer-cial aquaculture farms in the vicinity ofKaohsiung, southern Taiwan, in May2004 and in May and June 2005. Rearingconditions varied with species, but mostwere reared in outdoor concrete or earthponds. Exceptions were Epinephelusspp., which were reared in indoor con-crete tanks, and Chanos chanos andsome Eleutheronema tetradactylum,which were reared in outdoor concretetanks under shade cloth. The aquacultur-ists we dealt with did not maintainbreeding stock, but obtained eggs forrearing from elsewhere. The larvae weobtained from the aquaculturists wereplaced in oxygenated plastic bags andtransported about 1 h by road to the lab-oratory at NMMBA. In the laboratory thelarvae were acclimated in 40 l aquariafilled from the NMMBA seawater sys-tem. Each aquarium was fitted with anaerator and kept at ca. 25°C. Twice daily,
257
Fig. 1. Larvae of the study species over the range of sizes and developmentalstages used to determine swimming speed. For each species, ethanol-preservedindividuals near the extremes of sizes (mm, SL) studied are shown; left column:small larva; right column: large larva. The images are not to scale. (A) Trachino-tus blochii (Carangidae) left, 4 mm; right, 6 mm; (B) Chanos chanos (Chanidae):left, 8 mm; right, 11 mm; (C) Platax teira (Ephippididae): left, 5 mm; right,11 mm; (D) Leiognathus equulus (Leiognathidae): left, 4.5 mm; right, 14 mm; (E)Lutjanus malabaricus (Lutjanidae): left, 5.5 mm; right, 18.5 mm; (F) Eleu-theronema tetradactylum (Polynemidae): left, 7 mm; right, 20 mm; (G) Epineph-elus coioides (Serranidae): left 4, mm; right, 20 mm (E. fuscoguttatus and
E. malabaricus are very similar to E. coioides and are not illustrated)
Mar Ecol Prog Ser 349: 255–267, 2007
the larvae were fed with live, newly hatched brineshrimp Artemia nauplii and 50% of the total volumeof water was exchanged with fresh seawater. Theaquaria were cleaned daily by suctioning debris off thebottom.
Growth rates were estimated for the larvae in theculture ponds and also during the time larvae wereheld at NMMBA. In some cases, reliable age estimatesfor larvae were not available, and in others, age esti-mates were imprecise. Therefore, growth rate esti-mates for larvae from the culture ponds were less reli-able than those from the laboratory. Growth in theculture pond was estimated by assuming that the lar-vae were 2 mm long at hatching and had lineargrowth, and using the size of larvae on the day weobtained them and the age provided by the aquacul-turist. Growth during the time the larvae were held atNMMBA was estimated from the slope of the age ver-sus size regression over that time. Growth estimateswere obtained for 6 of the 9 species from the cultureponds; those excluded were Trachinotus blochii, Plataxteira and Epinephelus fuscoguttatus. Growth estimatesat NMMBA were obtained for 5 of those 6 species;Chanos chanos was excluded.
Reported sizes of larvae are SL in mm. Ages are re-ported as days after hatch (dah) based on the age re-ported by the aquaculturist when the larvae were ob-tained. The nomenclature of early life history stages offishes is complex, with many different systems of termi-nology and no consensus on the most appropriate. De-pending on the nomenclature used, the individuals westudied (Fig. 1) would be considered larvae or juve-niles, or a mixture of both. We do not attempt to distin-guish between larvae and juveniles. To avoid awkwardphrasing and for simplicity we refer to the young fishunder study here as larvae, but acknowledge that someterminologies might refer to them by other labels. In thespecies studied, notochord flexion was complete atabout 4 to 6 mm, depending on species. Therefore, inChanos chanos, Eleutheronema tetradactylum andEpinephelus fuscoguttatus, all individuals studied werepostflexion. In Leiognathus equulus, Lutjanus mala-baricus, Platax teira and Trachinotus blochii, the small-est individuals were flexion stage larvae. In Epine-phelus coioides and E. malabaricus, the smallest larvaewere preflexion stage. The size of the smallest speci-mens tested was dictated either by the smallest avail-able from the aquaculturists during May and June inTaiwan, or the smallest that we could work with in theswimming chamber. The largest specimens of mostspecies were approximately settlement size. Exceptionswere P. teira and T. blochii for which the largest avail-able larvae were 11 and 6 mm, respectively. In the lat-ter, settlement does not take place as the adults arepelagic.
Multilane swimming chambers were used to mea-sure swimming abilities (Stobutzki & Bellwood 1994).The chambers were made of clear Perspex with 6laneways, each 30 mm wide, 50 mm high and 180 mmlong. A black line across the lid of the chamber pro-vided the larvae with a point of reference while swim-ming. Aside from the fine mesh (0.5 mm) ends, thechamber design was identical to that of Stobutzki &Bellwood (1994, 1997) and they were the same cham-bers used by Clark et al. (2005) and Leis et al.(2006a,b).
The chambers were plumbed into the seawater sys-tem at NMMBA, which provided a continual flow of‘fresh’ seawater. Even distribution of flow wasachieved by a T-piece diffuser placed in the headerportion of the chamber. Turbulence in the chamberwas minimised by a 40 mm long section of flowstraighteners at the start of each laneway. This alsominimised possible boundary layers. Previous mea-surements have shown that water velocity in the 5 mmclosest to the wall was not significantly different to thatin the centre of the chamber (Stobutzki & Bellwood1997, Stobutzki 1998, Fisher et al. 2000). Water flowspeed was controlled by turning a calibrated valve.Flow rates were calibrated by recording the time takenfor water flowing over the chamber’s outlet weir to filla container of known volume, divided by the cross-sec-tional area of the chamber. The average of 5 calibra-tions was used as the flow speed for a given valveangle. The chambers were calibrated several timesover the course of the study. Flow speeds in excess of50 cm s–1 could be achieved with this system, but dueto vagaries of the seawater system and differences inhow the swim chambers were plumbed in the 2 yr, themaximum flow was less on some occasions, and somelarvae were able to swim faster than the chambermaximum on some occasions (see later discussion ofhow data from such ‘outswimmers’ were treated).
Larvae were acclimated to any differences in waterquality between holding tank and swim chamber bygradual addition of seawater from the swimmingchamber system. Larvae were placed in a chamberlane and allowed to acclimate for 5 min at 1 cm s–1. Anylarva showing signs of stress during the acclimationperiod was removed and replaced with another indi-vidual. Water temperature in the swimming chamberranged from 27 to 31°C, the ambient temperature inthe ocean off southern Taiwan at that time of year.
We measured Ucrit, which quantifies maximumswimming speed over periods of minutes. Starting at1.5 cm s–1 flow, speed was increased at a target incre-ment of 2 to 3 cm s–1 every 5 min until the larvae wereunable to swim against the flow. Due to vagaries in theseawater system and differences in the plumbing lead-ing to the swim chambers used during 2004 and 2005,
258
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes
the actual range in speed increment steps was 1.6 to3.7 cm s–1 when all 6 laneways of the swimming cham-ber were in use. To achieve a flow speed fast enough toreach Ucrit for the larger stages of 3 species, 3 lanewaysof the swim chamber were closed and the system recal-ibrated. In this case, the speed increment steps were5.3 to 5.4 cm s–1. The time elapsed at the point wheneach larva drifted into the downstream mesh (t in theequation below) was recorded. Critical speed (Ucrit) oflarvae was calculated following Brett (1964):
Ucrit = U + (t/ti × Ui)
where U = penultimate speed, Ui = speed increment(normally ca. 2 cm s–1), t = time swum in the final speedincrement, and ti = the time interval for each velocityincrement (5 min). The total time for a critical speedmeasurement was proportional to the Ucrit achievedand varied from 0.5 min for the smallest slowest indi-viduals (i.e. unable to achieve 1.5 cm s–1) to 75 min forthe larger fastest individuals. Given the swimmingendurance these larvae are capable of (hours to days;J. M. Leis unpubl. data) and that for other warmwaterspecies (Fisher et al. 2000, Clark et al. 2005, Leis et al.2006a), it is unlikely that the larvae would havebecome fatigued over such time intervals. Compar-isons have shown that varying the time increment (ti)and speed increment (Ui), which results in variations inthe time over which the full Ucrit test takes place, haslittle effect on the resultant Ucrit value (Fisher et al.2005).
Fatigued larvae were removed from the chamber,euthanized and fixed in Bouin’s solution for 1 h, thentransferred into 70% alcohol and stored. All preservedlarvae were later examined under a dissecting micro-scope to determine SL and stage of development.These specimens are archived in the Fish Collection ofthe Australian Museum, Sydney (under registrationstations AMS I.43864 and I.43865).
A total of 13 individual larvae of 2 species (Lutjanusmalabaricus and Epinephelus malabaricus) couldmaintain position at the highest speed that the cham-ber could produce in some situations. The true Ucrit ofthese outswimmers was underestimated by anunknown amount. For this reason, their data were notincluded in the regression analysis but were noted(see Fig. 2).
To determine the best predictor of performance, val-ues of critical swimming speed and endurance wereregressed against SL using linear, power and exponen-tial models. The linear model provided the best fit for 5species. In the other 4 species, the R2 of the linearmodel was within 0.03 to 0.07 of the R2 of the best fit(power) model, and the 2 regression lines were verysimilar (i.e. the power curve was nearly linear). There-fore, we report here only the linear relationships,
although the power and exponential relationships areprovided in Appendix 1. Age versus Ucrit relationshipswere also calculated, but these provided a muchpoorer fit than did the size versus Ucrit relationships.Because age and SL are related, we performed anotheranalysis whereby we regressed SL against age for indi-viduals for which we had both variables. The residualsfrom this analysis (the variation in size that was not dueto age, i.e. variation in growth) and SL were used asindependent variables in a multiple linear regressionagainst Ucrit. This analysis could be done for 7 speciesand allowed an assessment of the relative importanceof size and growth rate on swimming performance. Ineach case, only SL had a significant influence on Ucrit.The results of these analyses are not included, but theyfurther confirm the superiority of size as a predictor ofswimming performance.
In addition to average performance, we also reportthe speed of the best performers at different sizes. Thiswas done because the best performers may not onlyhave the most influence on dispersal outcomes, butthey may be the individuals most likely to survive theextremely high mortality of the larval stage (Grorund-Colvert & Sponaugle 2006).
To study larvae from a wide variety of sizes andstages of development, we either obtained multiplecohorts from aquaculturists or kept larvae in theNMMBA laboratory while they grew. Thus, for all spe-cies the Ucrit data were collected from more than oneday (although the same larvae were never measuredmore than once), and for most species from more thanone cohort of larvae (Table 1). We attempted to ensurethat the size ranges of larvae tested on different daysoverlapped as much as possible, but overlap was notalways achieved. Although there were never enoughmeasurements from different cohorts or days to for-mally test to see if inclusion of data from differentcohorts or days introduced additional variance, therewas some evidence that it did so (e.g. omission of mea-surements from one day might result in an increase inoverall R2). However, as there was no basis for deter-mining which cohorts or days provided the most repre-sentative data, they are all included in our analysis.
RESULTS
We obtained rough growth estimates of 2 types.Growth rates for larvae in the culture ponds were 0.08to 0.72 mm d–1 for 6 species with a mean of 0.30 mmd–1. Growth for larvae at NMMBA was 0.30 to 0.62 mmd–1 for 5 species with a mean of 0.40 mm d–1.
The Ucrit values ranged from 0 to 64 cm s–1. Asexpected, Ucrit increased with increasing size of the lar-vae in each species (Table 2, Fig. 2), although in most
259
Mar Ecol Prog Ser 349: 255–267, 2007
cases the variation in speed at any size was large. Thespeed versus size relationships were linear or approxi-mately so; the slopes were significantly different fromzero and, with one exception (Trachinotus blochii, inwhich only larvae of 4 to 6 mm were available),explained at least 49% of the variation in speed. Therate of increase in speed ranged from 1.31 to 2.64 cms–1 for each 1 mm increase in size. The increase inspeed from the smallest larvae studied to settlementstage larvae ranged from 6- to 100-fold, depending onspecies.
In general, size was a much better predictor of Ucrit
than was age (Table 2). No age estimate was availablefor the Epinephelus fuscoguttatus larvae, and for mostspecies, an age estimate was not available for all indi-viduals tested. Of the 8 species for which some agedata were available, 5 had a significant relationshipbetween age and Ucrit, but in 7 of the 8 species, therelationship explained considerably less of the varia-tion in Ucrit than did size (10 to 82% less overall and 10to 43% in species with a significant age:Ucrit relation-ship; Table 2). In the exceptional species, E. malabari-
cus, 90% of the variation was explained by both rela-tionships. Growth rates in aquaculture environmentsare unlikely to be representative of those in the wild,so these speed versus age relationships should be usedwith caution.
To determine whether the slopes of the regressionsof Ucrit on size differed among species, an analysis ofcovariance (ANCOVA) was performed with Ucrit as thedependent variable, species as a fixed factor and sizeas the co-variate. ANCOVA revealed a significantinteraction between species and size (factor × co-vari-ate; F(8,372) = 6.440, p < 0.0001) indicating that theslopes of the various regressions of Ucrit on size werenot homogenous; i.e. the influence of size on Ucrit dif-fered among species. Examination of the regressionslopes and their 95% confidence limits (Table 2) sug-gested that the species could be loosely placed into 2groups: those with slopes less than 2 (Platax teira,Leiognathus equulus, and Eleutheronema tetradacty-lum) and those with slopes greater than 2 (Trachinotusblochii, Chanos chanos, Lutjanus malabaricus, Epi-nephelus coioides, E. fuscoguttatus and E. malabari-
260
Relationship R2 p Slope ± 95% CI Speed (BL s–1)Mean (SE) Range
Table 2. Relationships between critical speed (Ucrit in cm s–1) and size, Ucrit (cm s–1) and age (days after hatch [dah]) and Ucrit (body lengths[BL] s–1) and size. CI = confidence interval, ns = not significant (p > 0.05), nd = no data available
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes 261
02468
10121416 (A) Trachinotus blochii
0
5
10
15
20
25 (B) Chanos chanos
0
5
10
15
20
25 (C) Platax teira
0
5
10
15
20
25
30
35 (D) Leiognathus equulus
0
10
20
30
40
50
60 (E) Lutjanus malabaricus
0
5
10
15
20
25
30
35 (F) Eleutheronema tetradactylum
0
10
20
30
40
50 (G) Epinephelus coioides
0
10
20
30
40
50
60 (H) Epinephelus fuscoguttatus
y = 2.135x – 6.193R2= 0.91
y = 2.546x – 10.766R2= 0.92
y = 2.197x – 9.700R2= 0.79
y = 1.366x – 1.018R2= 0.61
y = 1.691x – 2.396R2= 0.49
y = 2.058x – 9.838R2= 0.49
y = 2.269x – 11.128
y = 1.305x – 0.290
y = 2.515x – 0.775
R2= 0.82
R2= 0.50
R2= 0.38
0
10
20
30
40
50
60
70
Ucr
it (c
m s
–1)
Ucr
it (c
m s
–1)
Ucr
it (c
m s
–1)
Ucr
it (c
m s
–1)
Ucr
it (c
m s
–1)
Size (mm, SL)0
2
4
4
3.5 4 5 64.5 5.5 6.5
5 6 7 8 9 10 11
8 12 16 20 24 28
4 6 8 10 12 14 16 18 20 12
5
3
5 6 7 8 9 10 11 12 13 14
5 7 9 11 13 15 17
10 15 20 25
14 16 18 20 22 24 26 28
5 10 15 20 25 30
Size (mm, SL)(I) Epinephelus malabaricus Fig. 2. Relationship between size (mm, SL) and swimming
speed (Ucrit, cm s–1 ) in larvae of 9 species of tropical marinefishes. The thick line is the regression line (details in Table 2)and the thin lines represent speeds of 20 body lengths (BL) s–1
(top), 10 BL s–1 (middle) and 1 BL s–1 (bottom). (A) Trachinotusblochii; (B) Chanos chanos; (C) Platax teira; (D) Leiognathusequulus; (E) Lutjanus malabaricus (in addition, 6 larvae [25 to31 mm SL] outswam the chamber at 35 cm s–1 and 1 [21 mmSL] at 46 cm s–1); (F) Eleutheronema tetradactylum; (G) Epi-nephelus coioides; (H) Epinephelus fuscoguttatus; (I) Epi-nephelus malabaricus (in addition, 6 larvae [18 to 22.5 mm
SL] outswam the chamber at 36 cm s–1)
Mar Ecol Prog Ser 349: 255–267, 2007
cus). When these groups were analysed separately,neither group had a significant interaction betweenspecies and size (for slope > 2: F(5,182) = 0.86, p = 0.51;for slope < 2: F(2,190) = 1.27, p = 0.28) indicating thatregression slopes did not differ among species withinthe groups. An ANCOVA on these 2 groups with slope(>2 or <2) as the factor confirmed that regressionslopes differed significantly between the 2 groups(F(1,372) = 30.96, p < 0.001).
Mean speeds expressed in terms of body lengths(BL) (length-specific Ucrit) ranged from 9.8 to 23.5 BLs–1 (Table 2) depending on species. In all species,except Chanos chanos, at least 1 individual had amaximum length-specific Ucrit greater than 20 BL s–1
(range of maximum length-specific Ucrit among specieswas 17.8 to 31.1 BL s–1). Six of the 9 species had signif-icant linear relationships between length-specificspeed and SL (p < 0.05, R2 = 0.07–0.90 depending onspecies; Table 2), confirming an increase in length-specific Ucrit with increase in size. In every species, theamount of variation in length-specific Ucrit explainedby the linear relationships was less than for Ucrit,although the difference ranged from 4 to 60%.
For each species, within each 1 mm increment of sizefor which Ucrit values for at least 2 individuals wereobtained, the speed of the fastest individual was com-pared with the mean speed to quantify the differencebetween best performers and average performers.Depending on species, the best performers averaged1.5 to 7.3 cm s–1 faster than did mean performers(Table 3), but with some individuals swimming asmuch as 15 cm s–1 faster than the species mean. A sig-nificant relationship between size and the differencebetween best and mean performance was evident onlyin Leiognathus equulus larvae, where the differencebetween best and mean speed increased at a rate of0.65 cm s–1 per mm increase in size (speed difference =0.65[SL]+ 0.77, p = 0.014, R2 = 0.468). It is likely that
within a species, the magnitude of the differencerecorded between mean and best performance is posi-tively correlated with the number of individuals mea-sured. Thus, the ‘best performance’ we report is likelyto be an underestimate of the true best performancewithin the population of larvae.
DISCUSSION
The chief advantage of using Ucrit to investigate theontogeny of swimming performance in fish larvae isthe ability to compare swimming speed among devel-opmental stages and among species. In the larvae ofthe 9 species we examined, Ucrit increased rapidly withincrease in size and the rate of increase varied amongspecies. Further, the absolute magnitude of theincrease from the smallest larvae to settlement sizevaried greatly among species. Variation in Ucrit at anysize was high, as has been found also in previous stud-ies of both reared and wild larvae (Fisher et al. 2000,2005, Clark et al. 2005, Leis et al. 2006a).
Morphology undoubtedly influences swimmingspeed (Fisher et al. 2005). The larvae tested here had 4basic morphologies (Fig. 1): (1) clupeid-like, i.e. veryelongate with a long, straight gut along the ventraledge (Chanos chanos); (2) generalized perciform, i.e.moderate depth, laterally compressed, with a compactgut (Trachinotus blochii, Leiognathus equulus, Eleu-theronema tetradactylum); (3) generalized perciformmorphology, but with very elongate spines in dorsaland pelvic fins (Epinephelus spp., Lutjanus malabari-cus); and (4) rotund, i.e. head and trunk deep andbroad with a small, compressed tail (Platax teira).
The smallest (6 to 7 mm, SL) Chanos chanos larvae(clupeid-like morphology) were slower than similar-sized generalized perciform larvae. However, C. chanoslarvae increased in speed rapidly with increase in size, so
that by 13 mm (settlement size) theirUcrit was similar to those of both thegeneralized perciforms and the perci-forms with elongate fin spines.
The rotund species (Platax teira) and2 of the generalized perciform species(Leiognathus equulus, Eleutheronematetradactylum) had similar initial per-formance and rate of increase in Ucrit.Over the narrow range of sizes forwhich we had data, Trachinotusblochii, the third generalized perci-form species, had the best swimmingperformance, with the fastest Ucrit val-ues at 4 mm SL and a rate of increasein Ucrit with increase in size that wasamong the highest we measured in this
262
Species N (size Mean diff. Greatest diff.increments) (cm s–1) (SE) (cm s–1)
Table 3. Comparison of best (fastest) vs. average swimmers (Ucrit). N is thenumber of 1 mm size increments for which more than 1 individual wasmeasured. The mean and greatest differences in Ucrit are across all 1 mm size in-crements. Epinephelus malabaricus is omitted due to insufficient number of size
increments with more than 1 individual
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes
study. The swimming performance of T. blochii is simi-lar to that of another carangid, Caranx ignobilis (Fig. 3).
The 3 Epinephelus species were initially slow swim-mers, with very low Ucrit values until reaching about7 to 8 mm SL, but speed improved rapidly after thatand they were among the fastest swimming larvae atsettlement size. The initially poor swimming perfor-mance of the Epinephelus larvae was probably relatedto the very long, robust, bony spines of their dorsal andpelvic fins (more than half the length of the body).These large defensive spines are probably an impedi-ment to swimming, and small larvae of these speciesmay have a behaviour in relation to predators and preythat relies on stealth and deception rather than speedor manoeuvrability (Moser 1981). In these 3 Epineph-elus species, the fin spines reach a maximum relativelength (50 to 70% of SL) at about 5 to 6 mm, approxi-mately the same size that notochord flexion and con-comitant caudal fin formation are underway (Doi et al.1991, Kohno et al. 1993, Leu et al. 2005). At slightlylarger sizes, when the relative size of the fin spines isdecreasing and the caudal fin is fully formed, mean-ingful swimming ability begins to be displayed. Fromthis, it seems likely that the smallest Epinephelus lar-vae (<8 mm) will have limited ability to directly influ-ence dispersal outcomes. Given the similarity in theontogeny of Ucrit among these 3 species and the factthat their morphology is similar to that of other epi-nephelin serranid larvae (Baldwin et al. 2004), this
conclusion can be expected to apply to larvae of otherepinephelin serranid species (i.e. sea basses andgroupers). Pooling data for the 3 Epinephelus speciesresults in a strong relationship (Ucrit = 2.815[SL] – 7.960,R2 = 0.91, p < 0.0001) that may be useful for other epi-nephelin species.
Larvae of the lutjanid Lutjanus malabaricus alsohave elongate spines in dorsal and pelvic fins (20 to35% of SL), although not as long as in the Epinephelusspp. However, the smallest L. malabaricus larvae wetested were 2 mm larger than the smallest Epinepheluslarvae. Although it is not clear if both have limitedswimming abilities when very small, at the smallestsize they have in common in this study (5 mm SL), theUcrit values of the 2 genera were similar (Fig. 2). Larvaeof the genera Lutjanus and Epinephelus had similarincreases in Ucrit with size over the common size range.
Our results indicate that from relatively early indevelopment (the smallest sizes tested in all but the 3Epinephelus species, and from about 7 to 8 mm inthose species), the larvae of the species we studiedwere able to swim at speeds that placed them outsideof the strictly viscous hydrodynamic environment (i.e.Reynolds number > 300) and fast enough to influencedispersal outcomes (Leis 2006). At tropical tempera-tures, larvae that swim at 10 to 20 BL s–1 will haveReynolds numbers >300 from 4 to 5 mm SL (Leis 2006),and this includes most of the species considered here.The speeds of the larvae we studied were overwhelm-
ingly in the range of 10 to 20 BL s–1 andall species were capable of 10 cm s–1
before settlement. A current speed of10 cm s–1 is typical in many coastal envi-ronments (Fisher 2005), which meansthat the larvae of these species are capa-ble of swimming faster than average cur-rent speeds (i.e. are ‘effective swim-mers’; sensu Leis & Stobutzki 1999) wellbefore settlement in many locations.Heuristic modelling indicates thatspeeds as low as 1 to 5 cm s–1 can influ-ence dispersal outcomes (Leis 2006).Based on extrapolation of the speed ver-sus size relationships from our Ucrit mea-surements, average speeds of 1 cm s–1
can be attained by the species studied at1.8 to 6.7 mm SL, and larvae 1.5 to 2.5mm larger can attain speeds of 5 cm s–1.Extrapolation of these relationships tolarvae smaller than 5 to 6 mm is some-what dubious as in most of these speciessuch small larvae would not have com-pleted notochord flexion, and differentspeed versus size relationships mayapply before the caudal fin is formed. It is
P. amboinensisA. melanopusS. nematopteraA. japonicusP. auratusA. australisM. novemaculeataC. ignobilis
20 BL s–1
10 BL s–1
Fig. 3. Ontogeny of Ucrit in larvae of tropical and warm-temperate fish species.Plotted values are mean Ucrit at 1 mm increments of length (SL). Data for:Pomacentrus amboinensis (Pomacentridae), Amphiprion melanopus (Poma-centridae) and Sphaeramia nematoptera (Apogonidae) from Fisher et al.(2000); Argyrosomus japonicus (Sciaenidae), Pagrus auratus (Sparidae), Acan-thopagrus australis (Sparidae) and Macquaria novemaculeata (Percichthyidae)from Clark et al. (2005); Caranx ignobilis (Carangidae) from Leis et al. (2006a).Species represented by symbols of the same shape are in the same family. Thepomacentrids and apogonid hatch from non-pelagic eggs, whereas the sci-aenid, sparids and the percicithyid hatch from pelagic eggs. The size versusspeed relationships of the 9 study species from the present paper are provided
in this same format in Appendix 2
Mar Ecol Prog Ser 349: 255–267, 2007
clear, however, that small larvae can achieve speedsthat are meaningful in the context of dispersal.
The fastest larvae were able to swim considerablyfaster than mean performance at any size. This meansthese exceptional larvae (i.e. best performers) achievea given swimming speed at smaller sizes, and at anysize will have a greater potential to influence dispersaloutcomes. Therefore, this variance in size should betaken into account when developing biophysical mod-els of larval fish dispersal. Such models would be anideal means of examining the dispersal implications ofexceptional swimming performance. Further, severallines of evidence indicate that it may be the excep-tional rather than average individuals that survive thevery high mortality rates during the pelagic larvalperiod (Leis 2007). Although growth has been mostoften studied in this respect, exceptional swimmingability may also lead to increased survival, and it ispossible that exceptional rather than average perfor-mance is the appropriate metric for biophysical disper-sal models.
Although Ucrit is sometimes referred to as a measureof sustainable speed (e.g. Stobutzki & Bellwood 1994),Ucrit is, in fact, measured over only short periods (i.e.minutes) and is technically a measure of prolongedswimming speed (as distinct from both burst speed andsustainable speed; Plaut 2001). The Ucrit is best thoughtof as a measure of potential performance. It is unlikelythat larvae in the sea actually swim at their Ucrit speedfor sustained periods, so Ucrit is not a realistic measureof performance in the sea (Leis 2006). However, thereare indications that Ucrit can be used to predict larvalswimming performance in the sea. Fisher & Wilson(2004) concluded that a speed of about one-half of Ucrit
was sustainable over periods of 24 h, and empiricalevidence shows that larvae in the sea actually swim(i.e. in situ speed; Leis & Carson-Ewart 1997) at about30 to 50% of Ucrit (Leis & Fisher 2006, Leis et al.2006a,b, 2007). This is important because measure-ment of Ucrit in the laboratory is much easier and moreefficient than measuring in situ swimming in the sea.Further, it is possible to work with much smaller larvaein the laboratory than in the sea; therefore, to theextent that the relationships between Ucrit and in situspeed can be extrapolated to smaller larvae, laboratorytesting allows the possibility of obtaining realistic esti-mates of swimming speed in the sea for much smallerlarvae.
Because swimming performance of reared larvaemay not be representative of performance of wild lar-vae, it is important to compare performance of wildand reared larvae where possible (Leis 2006). Unfortu-nately, our ability to make such comparisons was con-strained by limited data on swimming performance inwild larvae. The only comparisons that could be made
between our reared larvae and wild larvae of the sameor closely related species are for settlement stage lar-vae of the lutjanids and serranids; no Ucrit data areavailable for wild larvae of the other families or forother developmental stages. Wild settlement stage lar-vae of 4 species of Lutjanus (L. analis, L. carponotatus,L. cyanopterus and L. quinquelineatus) with settle-ment sizes similar to those of L. malabaricus (21 to26 mm SL) had mean Ucrit values of 40 to 52 cm s–1
(SE = 0.9 to 5.4) (Fisher et al. 2005). Over the size rangeof 21 to 26 mm SL, reared L. malabaricus larvae hadaverage Ucrit values predicted by the regression equa-tion (Table 2) of 38 to 51 cm s–1 (and measured SE = 1.4to 2.9); this performance is equivalent to the wild lar-vae of the other 4 Lutjanus species. Epinephelus andPlectropomus are closely related genera of the sameserranid tribe and their settlement stage larvae aremorphologically similar (Leis 1986). Settlement stageP. leopardus larvae (17 mm SL) had an average Ucrit of31.5 cm s–1 (SE = 3.2) (Fisher et al. 2005), whereas17 mm SL larvae of the 3 Epinephelus spp. had aver-age Ucrit values of 27 to 33 cm s–1 (SE = 1.3 to 3.3). Thus,Ucrit values in the 2 serranid genera are equivalent.Therefore, to the extent that we could compare Ucrit
performance of wild and reared larvae, the valueswere essentially identical in terms of both mean andvariation.
There was no indication that growth rates of thereared larvae were substantially different from thoseof wild larvae. This is an issue because it is desirablethat reared larvae are as similar as possible to wild lar-vae to help ensure that their behaviours are equiva-lent. With the exception of Chanos chanos, essentiallynothing is known about growth rates of wild larvae ofany of the species we studied. Growth estimates forwild and reared C. chanos larvae appear similar; wildlarvae of C. chanos between 5 and 14 mm SL were esti-mated to grow at 0.5 mm d–1 (Bagarinao 1991), and inthe Taiwanese aquaculture farms, larvae of C. chanosgrew at 0.37 mm d–1. Growth rates of reared larvae ofthe other species in our study (0.08 to 0.72 mm d–1)were within the range of mean values reported for wildmarine fish larvae (Benoit et al. 2000, Meekan et al.2003), indicating that they do not differ from wild lar-vae in this respect.
Obtaining larvae from the aquaculture industry hasseveral advantages, most notably that we neither hadto maintain the extensive infrastructure necessary forrearing marine fish larvae nor develop the species-spe-cific methods required to obtain optimal survival andgrowth in captivity. Working in Taiwan, where a widevariety of species is under culture, was also advanta-geous (Yu 2002). Disadvantages include the sometimesvague information we received on larval ages and thelack of control over availability of species or develop-
264
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes
mental stages. For example, Taiwanese aquaculturistswere reluctant to provide Epinephelus larvae in themiddle stages of development (ca. 6 to 10 mm), statingthat larvae were particularly fragile at these stages andthat the disturbance required to capture larvae for uswould be detrimental to larvae remaining in the cul-ture pond. This influenced the size range available tous of some of the study species.
Although the patterns of ontogeny of swimming var-ied among species studied here, the variation waswithin relatively narrow bounds. The 9 species consid-ered here generally swam at between 10 and 20 BL s–1
throughout their larval development and regardless ofsize. This is in agreement with results on other tropicaland warm-temperate marine fish species (Fig. 3). The 8other species for which data on ontogeny of Ucrit existalso swam in most cases at between 10 and 20 BL s–1
throughout their larval development. At one extreme,larger larvae of the 2 pomacentrid species swam some-what faster than this, reaching speeds of about 30 BLs–1 (Fig. 3), whereas at the other extreme, larvae of asciaenid swam at just under 10 BL s–1 at all but thelargest sizes (Fisher et al. 2000, Clark et al. 2005). Sim-ilar to the species we studied, these other species hadan approximately linear increase in swimming speedwith the increase in size, with one apparent exception:a pomacentrid Pomacentrus amboinensis seemed tohave an allometric 2-phased increase in swimmingability, with little increase in speed until larvaereached about 8 mm SL, after which speed increasedmarkedly (Fisher et al. 2000).
In contrast, the within-species increase in Ucrit
between the smallest larvae and those at settlementstage differed markedly among species, principallydue to among-species differences in the rate ofincrease of Ucrit with increase in size and differences insize at settlement. In the species for which the smalleststudied larvae were 4 to 5 mm SL, the increase inspeed by settlement stage was 6-fold for Leiognathusequulus and 100-fold for Epinephelus coioides. Forspecies in which the smallest larvae were 5 to 6 mm SL,the increase in speed was 5- to 6-fold for Chanoschanos and Eleutheronema tetradactulm, but 10-foldfor Lutjanus malabaricus. This is a further indication ofthe substantial differences among species in theontogeny of swimming abilities.
Although the majority of tropical, demersal teleostfish families spawn pelagic eggs (Leis 1991), manyfamilies that do not spawn pelagic eggs (e.g. Apogo-nidae, Blenniidae, Gobiidae, Pomacentridae) are veryspeciose (Nelson 2006). Therefore, both spawningmodes are well represented. In both spawning groups,morphological developmental events relevant to swim-ming, such as notochord flexion and concomitant for-mation of the caudal fin, tend to occur at about the
same size (Leis & Carson-Ewart 2004); the main devel-opmental difference between groups is simply size athatching. Larvae hatching from non-pelagic eggs tendto be larger, and therefore, more developed than thosefrom pelagic eggs (Thresher 1984, Moser 1996, Leis &Carson-Ewart 2004), and as a result, they may be bet-ter swimmers initially. There were, however, no consis-tent differences in the ontogeny of swimming abilitybetween these 2 groups (Fig. 3). Three of the speciesrepresented in Fig. 3 hatch from non-pelagic eggs: the2 pomacentrids, Pomacentrus amboinensis and Am-phiprion melanopus, and the apogonid, Sphaeramianematoptera. Two of these species had linear increasesin speed with increase in size, whereas the third didnot (Fisher et al. 2000); the apogonid was among theslowest species studied and had the slowest rate ofincrease in speed, whereas the later stages of the 2pomacentrids were among the fastest larvae on a persize basis and had high rates of increase in swimmingspeed. Due to the differences in size and developmentat hatching, it might be expected that any difference inswimming ability between the 2 spawning groupswould be most obvious at smaller sizes, but this wasnot the case (Fig. 3). Small and mid-size larvae fromnon-pelagic eggs swam at speeds similar to similar-size larvae from pelagic eggs. Despite this lack of size-related difference in swimming performance betweenthe 2 groups, there may be age-related (i.e. days afterhatch) differences in swimming performance betweenthe 2 groups. This question is difficult to address withreared larvae because growth rates and variationsthereof are unlikely to be the same as those in wildlarvae.
The available data indicate that a one-size-fits-allmodel of fish swimming ontogeny is not a realisticexpectation. Although a linear model of increase inspeed over the size range studied was appropriate forour 9 test species, the previously studied species withthe highest relative speed (a pomacentrid, Fig. 3) had adifferent size:speed relationship. Even for the specieswith linear relationships between swimming speedand size, the 2 critical factors in the relationships dif-fered; both the rate of increase of speed with increasein size and the actual speeds attained differed amongspecies (as did length-specific speed). Closely relatedspecies did, however, have similar speed:size relation-ships. Finally, there are reasons to expect that larvae ofcool-water and cold-water species will not have swim-ming abilities or size:speed relationships similar tothose of tropical species (Leis 2007), but so few Ucrit
data are available for cooler-water taxa that this ex-pectation cannot be tested at present.
In conclusion, we provide for the first time informa-tion on the ontogeny of swimming performance in thelarvae of medium to large species (and families) of
265
Mar Ecol Prog Ser 349: 255–267, 2007
tropical marine fishes that hatch from pelagic eggs;most are of major commercial importance. Early intheir development, larvae of these species are able toswim strongly and attain speeds that place them out-side of the inefficient viscous hydrodynamic environ-ment. Such speeds are able to influence their dispersaloutcomes. Speeds of 10 to 20 BL s–1 were typical, andsome were as high as 64 cm s–1. Size was a better pre-dictor of swimming performance than was age. Swim-ming speeds increased at species-specific linear ratesof 1.3 to 2.6 cm s–1 for each 1 mm increase in size. Thefastest individuals were considerably faster than aver-age, and this may be important for biophysical disper-sal models. This swimming performance can now betaken into account in numerical, biophysical dispersalmodels and other applications that require informationon the development of swimming ability in fish larvae.
Acknowledgements. We thank Dr. K.-T. Shao, AcademicaSinica, who made our work in Taiwan possible. We also thankthe staff of NMMBA for their excellent cooperation, particu-larly Dr. I.-S. Chen and C.-Y. Chung. Our work could not haveproceeded without the assistance of C. Wen and K.-P. Kan. L.-H. Chao generously introduced us to many Taiwaneseaquaculturists and spent many hours helping us obtain larvae.D. Clark, M. Brown and R. Piola assisted ably. R. Johnson con-firmed identification of one species using DNA. G. Howarthand S. Bullock provided editorial assistance. This research wassupported by an ARC Discovery Grant (DP0345876) and aDST International Science Linkages Grant (IAP-IST-CG03-0043) to J.M.L., and by the Australian Museum.
LITERATURE CITED
Bagarinao TU (1991) Biology of milkfish (Chanos chanosForsskål). Southeast Asian Fisheries Development Center,Iloilo
Baldwin CC, Leis JM, Rennis DS (2004) Epinephelinae, tribesNiphonini and Epinephelini (groupers, rock-cods, coraltrouts). In: Leis JM, Carson-Ewart BM (eds) The larvae ofIndo-Pacific coastal fishes: a guide to identification (FaunaMalesiana Handbook 2). Brill, Leiden, p 377–382
Benoit HP, Pepin P, and Brown JA (2000) Patterns of meta-morphic age and length in marine fishes, from individualsto taxa. Can J Fish Aquat Sci 57:856–869
Brett JR (1964) The respiratory metabolism and swimmingperformance of young sockeye salmon. J Fish Res BoardCan 21:1183–1226
Clark DL, Leis JM, Hay AC, Trnski T (2005) Swimmingontogeny of larvae of four temperate marine fishes. MarEcol Prog Ser 292:287–300
Cowen RK, Paris CB, Sirnivasan A (2006) Scaling of connec-tivity in marine populations. Science 311:522–527
Doi M, Munir MN, Nik Razali NL, Zulkifli T (1991) Artificialpropagation of the grouper, Epinephelus suillus [=E.coioides], at the marine finfish hatchery at TanjongDemong, Terengganu, Malaysia. Kertas PengembanganPerikanan Bil 167:1–41
Fisher R (2005) Swimming speeds of larval coral reef fishes:impacts on self-recruitment and dispersal. Mar Ecol ProgSer 285:223–232
Fisher R, Bellwood DR, Job SD (2000) Development of swim-
ming abilities in reef fish larvae. Mar Ecol Prog Ser202:163–173
Fisher R, Leis JM, Clark DL, Wilson SK (2005) Critical swim-ming speeds of late-stage coral reef fish larvae: variationwithin species, among species and between locations. MarBiol 147:1201–1212
Fisher R, Wilson SK (2004) Maximum sustainable swimmingspeeds of late-stage larvae of nine species of reef fishes.J Exp Mar Biol Ecol 312:171–186
Grorund-Colvert K, Sponaugle S (2006) Influence of conditionon behavior and survival potential of newly settled coralreef fish, the bluehead wrasse, Thalassoma bifasciatum.Mar Ecol Prog Ser 327:279–288
Kohno H, Daini S, Supriatna A (1993) Morphological develop-ment of larval and juvenile grouper, Epinephelusfuscoguttatus. Jpn J Ichthyol 40:307–316
Leis JM (1986) Larval development of four species of theIndoPacific coral trout genus Plectropomus (Pisces: Ser-ranidae: Epinephelinae) with an analysis of the relation-ships of the genus. Bull Mar Sci 38:525–552
Leis JM (1991) The pelagic phase of coral reef fishes: larvalbiology of coral reef fishes. In: Sale PF (ed) The ecologyof fishes on coral reefs. Academic Press, San Diego, CA,p 183–230
Leis JM (2006) Are larvae of demersal fishes plankton ornekton? Adv Mar Biol 51:59–141
Leis JM (2007) Behaviour of fish larvae as an essential inputfor modelling larval dispersal: behaviour, biogeography,hydrodynamics ontogeny, physiology and phylogenymeet hydrography. Mar Ecol Prog Ser 322:225–238
Leis JM, Carson-Ewart BM (1997) Swimming speeds of thelate larvae of some coral reef fishes. Mar Ecol Prog Ser159:165–174
Leis JM, Carson-Ewart BM (2004) The larvae of Indo-Pacificcoastal fishes: a guide to identification (Fauna MalesianaHandbook 2). Brill, Leiden
Leis JM, Fisher R (2006) Swimming speed of settlement-stagereef-fish larvae measured in the laboratory and in thefield: a comparison of critical speed and in situ speed. Proc10th Int Coral Reef Symp, Okinawa: 438–445
Leis JM, Stobutzki IC (1999) Swimming performance of latepelagic larvae of coral-reef fishes: in situ and laboratory-based measurements. In: Séret B, Sire JY (eds) Proc 5thIndo-Pacific Fish Conf, Nouméa, 1997. Société Françaised’Ichtyologie et Institut de Recherche pour le Développ-ment, Paris, p 575–583
Leis JM, Hay AC, Clark DA, Chen IS, Shao KT (2006a) Behav-ioral ontogeny in larvae and early juveniles of the gianttrevally, Caranx ignobilis (Pisces: Carangidae). Fish Bull104:401–414
Leis JM, Hay AC, Trnski T (2006b) In situ behaviouralontogeny in larvae of three temperate, marine fishes. MarBiol 148:655–669
Leis JM, Wright KJ, Johnson RN (2007) Behaviour that influ-ences dispersal and connectivity in the small, young lar-vae of a reef fish. Mar Biol 153:103–117
Leu MY, Liou CH, Fang LS (2005) Embryonic and larvaldevelopment of the malabar grouper, Epinephelus mal-abaricus (Pisces: Serranidae). J Mar Biol Assoc UK85:1249–1254
Meekan MG, Carleton JH, McKinnon AD, Flynn K, Furnas M(2003) What determines the growth of tropical reef fishlarvae in the plankton: food or temperature? Mar EcolProg Ser 256:193–204
Moser HG (1981) Morphological and functional aspects ofmarine fish larvae. In: Lasker R (ed) Marine fish larvae:morphology, ecology and relation to fisheries. University
266
Leis et al.: Swimming speed in larvae of pelagic-spawning fishes
of Washington Press, Seattle, p 90–130Moser HG (1996) The early stages of fishes in the California
Current region. Calif Coop Ocean Fish Invest Atlas33:1–1505
Neira FJ, Miskiewicz AG, Trnski T (1998) Larvae of temper-ate Australian fishes: laboratory guide for larval fish iden-tification. University of Western Australia Press, Nedlands
Nelson JS (2006) Fishes of the world, 4th edn. J Wiley, Hobo-ken, NJ
Plaut I (2001) Critical swimming speed: its ecological rele-vance. Comp Biochem Physiol A Comp Physiol 131:41–50
Stobutzki IC (1998) Interspecific variation in sustained swim-ming ability of late pelagic stage reef fish from two fami-
lies (Pomacentridae and Chaetodontidae). Coral Reefs17:111–119
Stobutzki IC, Bellwood DR (1994) An analysis of the sustainedswimming abilities of pre- and post-settlement coral reeffishes. J Exp Mar Biol Ecol 175:275–286
Stobutzki IC, Bellwood DR (1997) Sustained swimming abili-ties of the late pelagic stages of coral reef fishes. Mar EcolProg Ser 149:35–41
Thresher RE (1984) Reproduction in reef fishes. TFH Publica-tions, Neptune City, NJ
Yu NH (2002) New challenges: breeding species in Taiwan,VIII. Fish Breeding Association of the Republic of China,Kaohsiung, Taiwan
267
Family Species Linear model R2 Power model R2 Exponential model R2
Carangidae Trachinotus blochii y = 2.515x – 0.775 0.376 y = 2.107x1.057 0.369 y = 3.837e0.218x 0.359
Chanidae Chanos chanos y = 2.058x – 9.838 0.487 y = 0.031x2.469 0.453 y = 0.699e0.252x 0.443
Ephippidae Platax tiera y = 1.305x + 0.290 0.497 y = 1.615x0.892 0.494 y = 3.639e0.128x 0.493
Leiognathidae Leiognathus equulus y = 1.691x + 2.396 0.494 y = 0.413x1.495 0.519 y = 2.219e0.167x 0.471
Lutjanidae Lutjanus malabaricus y = 2.269x – 11.128 0.824 y = 0.071x2.034 0.600 y = 1.171e0.168x 0.608
Polynemidae Elutheronema y = 1.366x – 1.018 0.611 y = 0.567x1.306 0.681 y = 3.944e0.104x 0.608tetradactylum
Serranidae Epinephelus coioides y = 2.546x – 10.766 0.924 y = 0.0046x3.250 0.931 y = 0.137e0.356x 0.825
Serranidae Epinephelus y = 2.197x – 9.700 0.790 y = 0.416x1.467 0.783 y = 7.150e0.076x 0.738fuscoguttatus
Serranidae Epinephelus y = 2.135x – 6.193 0.905 y = 0.050x2.108 0.918 y = 0.299e0.202x 0.934malabaricus
Appendix 1. Comparison of size vs. Ucrit regression statistics for linear, power and exponential models for each tropicalmarine fish species tested. y = critical swimming speed, x = standard length (SL)
0
10
20
30
40
50
60
10–11
9–8–97–86–75–64–53–410
11–12
12–13
13–14
14–15
15–16
16–17
17–18
18–19
19–20
20–21
21–22
22–23
23–24
24–25
25–26
26–27
27–28
28–29
Ucr
it (c
m s
–1)
Size (mm, SL)
C. chanos
Ep. coioides
Ep. fuscoguttatus
Ep. malabaricus
El. tetradactylum
Lu. malabaricus
Le. equulus
P. teira
T. blochii 10 BL s-1
20 BL s-1
Appendix 2. Ontogeny of Ucrit in larvae of 9 species of tropical marine fishes that hatch from pelagic eggs from the present study:Chanos chanos, Epinephelus coioides, Epinephelus fuscoguttatus, Epinephelus malabaricus, Eleuthronema tetradactylum,Lutjanus malabaricus, Leiognathus equulus, Platax teira and Trachinotus blochii. Plotted values are mean Ucrit (cm s–1) at 1 mmincrements of standard length (SL). Species represented by symbols of the same shape are in the same family. Dashed lines con-nect values across intervening size increments for which data are lacking. Note that for Ep. malabaricus, Ucrit data were available
for only 4 size increments: 3–4, 5–6, 24–25 and 25–26 mm SL
Editorial responsibility: Charles Birkeland (ContributingEditor), Honolulu, Hawaii, USA
Submitted: February 19, 2007; Accepted: June 8, 2007Proofs received from author(s): October 24, 2007
