Size-Specific Vulnerability to Predation and SensorySystem Development of White Seabass,

Atractoscion nobilis, Larvae

Daniel Margulies

ABSTRACT: The size-specific vulnerability ofwhite seabass, Atractoscron nobilis, larvae (2.5-15.0mm SL) to two types of fish predators-adultnorthern anchovy, Engraulis mordax, and juvenilewhite seabass-was examined in laboratory preda-tion trials. Concurrent analyses were made of thedevelopmental ontogeny of larval visual and mech-anoreceptive systems. The proportion of larvae re-sponding to or escaping attacks by either predatorincreased with larval size. There were no signifi-cant differences in proportions of larvae respondingto or escaping attacks of either predator untillarvae were 6.0-7.5 mm SL (early postflexionstage). At this size, larvae were better able to evadethe slower, more discontinuous attacks of juvenilewhite seabass compared with the faster attacks ofadult anchovy. Major developmental events occurduring this larval stage, including rapid improve-ment in visual acuity, visual accommodation to dis-tant objects, growth and stratification of the optictectum, and large increases in the numbers of freeneuromasts on the head and trunk. It is likely thatat larval sizes >7 mm SL, the slower attacks ofjuvenile white seabass allow more time for larvae toprocess and integrate visual and mechanoreceptivesensory input from several modalities. White sea·bass larvae (and sciaenids in general) become moredemersal in distribution during the late larvalstages in nearshore southern California waters.This ontogenetic shift deeper into the water col·umn may be related to predator-avoidance capabil-ities of the larvae, since most demersal planktivoresexhibit some type of hovering, ambush, or discon-tinuous mode of predation similar to that of juve-nile white seabass and attack at much slowerspeeds than pelagic, shoaling fish predators. Asthey shift downward, older white seabass larvaemay maximize their predator-detection capabilitieswhen encountering demersal fish predators.

For most marine and estuarine fishes, preda-tion-induced mortality during early life stagesmay be crucial in determining year-class

Daniel Margulies, Southwest Fisheries Center La JollaLaboratory, National Marine Fisheries Service, NOAA,P.O. Box 271, La Jolla, CA 92038; present address: Inter-American Tropical Tuna Commission, c/o Scripps Institutionof Oceanography, La Jolla, CA 92093.

Manuscript Accepted April 1989.Fishery Bulletin, U.S. 87: 537-552.

strength. Predation has long been recognized asan important potential regulatory mechanism inprerecruit life stages (Houde 1978, 1987; Hunter1981, 1984), but many of the specific factors thatinfluence predation rates on early life stages arenot well understood (Bailey and Houde 1989).

One of the crucial aspects of predator/preydynamics involves the developmental or physio-logical basis for capture and escape responses.Fish larvae possess several sensory systems pre-sumed to be important in predator detection;these include visual, mechanoreceptive, andauditory systems. During early ontogeny, thesesensory systems undergo rapid development,and the improvement in these systems isthought to be crucial in controlling vulnerabilityto predation (Hunter 1984; Blaxter 1986). How-ever, experimental investigations combining thestudy of larval sensory system development andvulnerability to predation are limited. Larvae ofseveral species, including the northern anchovy,Engaulis 'nwrdax, (O'Connell 1981; Webb 1981;Folkvord and Hunter 1986), Atlantic herring,Clupea harengus harengus, (Blaxter et al. 1983;Blaxter and Batty 1985; Fuiman 1989), Capeanchovy, Engraulis capensis, (Brownell 1985),bloater, Coregonus hoyi, (Rice et al. 1987), andwhite perch, Morone americana, (Margulies inpress) have been studied to examine either sen-sory system development or predator-avoidancebehaviors. Similar studies have been conductedon larvae of flatfish (Neave 1984, 1986) and sev-eral gadoids (Fridgeirsson 1978; Bailey 1984).These types of investigations, however, have notbeen combined during one study using a singlecohort of experimental fishes.

The purpose of this study was to examine,experimentally, the size-specific vulnerability ofwhite seabass, Atractoscion rwbilis, larvae todifferent types of fish predators, and to deter-mine if there was a developmental or neuro-logical basis for any observed changes in larvalvulnerability or behaviors. The developmentalstudies of larval white seabass centered on theontogeny of two sensory systems, vision and

537

mechanoreception, which are presumed to beimportant components of predator detection andlarval escape responses (Blaxter 1986). Theontogeny of avoidance/escape responses andother larval behaviors of white seabass werethen analyzed in relation to the structural andfunctional development of their sensorysystems.

Very little is known of the early life history ofthe white seabass, even though it is the largestsciaenid occurring in coastal waters of Californiaand Baja California and has historically been afavored sport and commercial species (Feder etal. 1974; Vojkovich and Reed 1983). White sea-bass spawn in spring and early summer in near-shore coastal waters of southern California, andproduce pelagic eggs. Abundance and distribu-tion of young-of-the-year in southern Californiawaters have been reported by Allen and Frank-lin (988). Larval morphological developmenthas been described by Moser et al. (1983), butlarval ecology, predator-avoidance behaviors,and sensory system development have not beendescribed.

METHODS

Larval Rearing

White seabass larvae used in the experimentswere hatched from eggs obtained from brood-stock adults maintained at the Hubbs MarineResearch Center at Sea World in San Diego.Eggs were transported to the aquarium at theSouthwest Fisheries Center La Jolla Laboratoryand stocked in 76 L aquaria at stocking densitiesof 6 L- 1. During the culture experimentswater temperature ranged from 17° to 19°C, anda constant photoperiod of 13 h light: 11 h darkwas maintained.

First-feeding white seabass larvae were fedrotifers, Brachionus pLicatilis, cultured on thegreen alga Tetraselmis. Older larvae were se-quentially fed diets ofAnemia nauplii, a mixtureof Anemia nauplii and wild copepods, and adultAnemia. The developmental size range of whiteseabass tested ranged from hatching (2.6 mmSL, 0 day after hatch) to juvenile metamorphosis(15.0 mm SL, 42 days after hatch) (Fig. 1).

FISHERY BULLETIN: VOL. 87, NO.3. 1989

southern California and are potential naturalpredators of white seabass larvae. These twopredator groups represent different types ofraptorial predatory behavior (Table 1). Adultnorthern anchovy are pelagic, cruising predatorsthat attack prey at relatively high speeds andoften from oblique angles. Juvenile white sea-bass attack at much slower speeds and have asomewhat discontinuous mode of attack that in-volves an approach, glide, and then engulfing ofprey. Northern anchovy also initiate attacksfrom much greater distances.

Predators were held in laboratory holdingtanks and fed adult Anemia, minced euphausiidsand occasionally white seabass larvae. To mini-mize predator learning behavior, after comple-tion of predation trials on a given date, predatorswere transferred to separate holding tanks; thisensured that no predator was used more thantwice during the 6 wk experimental period.

Experimental Methods

The predation experiments were conductedfollowing the methods of Folkvord and Hunter(1986), with several modifications. Predationtrials were carried out in rectangular fiberglasstanks, 1.4 m3 in volume, with a clear glass win-

16

A,14 , Juvenile,,

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2,

Hatch

FIGURE l.-Sizes, ages, and developmental stages oflarval white seabass prey used in predation trials.

LARVAL AGE (days after hatch)Experimental Predators

Adult northern anchovy and juvenile whiteseabass were used as predators. Both of thesepredator groups occur in nearshore waters of

538

o 10 20 30 40 50

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

TABLE 1.-Modes of predation exhibited by adult Engraulis mordax and juvenile Atractoscion nobi/is.

Predator

Engrau/is mordax(Adults)

Atractoscion nobi/is(Juveniles)

AttackSize (mm) distance (dm)

Range Mean Range Mean

85-107 96.4 20-70 36.6

62--86 72.2 5-30 14.7

Attack speedrange (m/s)

0.50-1.50

0.05-0.20

Mode of attack

Fast speed; approach andattack continuous; often fromoblique angle

Slow to moderate speed; at-tacks often discontinuous,with approach, glide, theningestion; angle of attackhorizontal or oblique

dow on one side for observation. Flourescentlamps produced 2,000--3,000 mc at the surface ofeach tank. A black plastic tent enclosed the win-dow, providing a darkened compartment forobservations. Metric rules placed on the tankwindow allowed estimation of predator attackdistances. The tanks were supplied with flow-through ambient seawater 07°-19°C), exceptduring an experiment when the water wasstatic. Since adult northern anchovy often occurin large schools and juvenile white seabass aresolitary or found in loose aggregations, it wasdecided that northern anchovy predators ingroups of five individuals and white seabass ingroups of three should be used. This simulatedthe predators' natural condition yet preventedpredator "swamping" of larval prey.

Feeding motivation of predators was stan-dardized by presenting constant numbers ofadult Artemia to predators prior to predationtrials with larvae. (Arlern-ia are a good standardprey because they do not avoid predatory at-tacks by fishes.) Preliminary experiments hadindicated that feeding behavior of adult northernanchovy was more variable than that of juvenilewhite seabass; thus, five groups of five Artem-iaeach were presented to each anchovy predatorgroup and three groups of five Artemia eachwere presented to white seabass. After theArte?nia additions, white seabass larvae wereintroduced into the predation tanks in groups offive (each larval group added = trial). Trial dura-tion was 10 minutes or until all prey were eaten.Larvae and Arte'mia were added to the tanks inclear beakers that were gently submerged at thewater surface. After the initial Arte'm;ia trials,each predator group was tested with 6--8 larvaltrials, followed by a final Artemia trial to test forpredator satiation.

On the same day as predation experiments,subsets of 10--12 larvae were removed from cul-

ture tanks and fixed in 5% formalin for calcula-tion of mean larval sizes; additional subsets oflarvae were removed for examination of sensorysystem ontogeny (discussed below). The totalnumber of predator-prey interactions observedfor each larval size class and predator type ispresented in Table 2.

TABLE 2.-The total number of predator-prey interactions ob-served for each larval size and age class and predator type.

X larval size Larval age Observations per predator type

(mm) (d) Northem anchovy White seabass

3.1 4 36 394.5 12 35 326.1 17 33 387.4 23 30 379.1 27 40 38

12.5 34 38 4014.8 42 42 50

Classification of behaviors followed Folkvordand Hunter (1986). Four measures of predator-prey interactions were calculated: mean andmaximum attack distances; percentage of larvalavoidance responses; percentage of larvalescapes; and predation rate (percentage oflarvae captured during each 10 min trial). Ap-proximate predator attack speeds also wereestimated. A predator attack was a directedmovement toward a prey with the mouth open.Predator attack distance was the distance indecimeters (dm) from a prey to the point oforigin of attack. An avoidance response was achange in speed or direction of a larva occurringbefore a predator could complete an attack. Anescape occUITed when a predator failed to cap-ture a larva during a single attack. Repeatedattacks were scored as separate events.

Two potential biases to the predator-prey

539

interactions were addressed. Variation in preda-tor performance was examined by calculatingthe percentage of predator en'or occurring infive groups of both types of predator feeding onadult Artem-ia. Since Artem;ia show no avoid-ance responses, a predator error was recordedwhen a predator simply missed the prey. Per-centage of predator en'or was calculated for eachpredator group and among groups. In addition,potential stress or mortality of larvae due tohandling was examined. For each larval sizeclass, four replicates (trials) of five larvae eachwere transferred into 76 L tanks containing nopredators. Mortality observed in control tankswas used to adjust for handling-induced mortal-ity or increased vulnerability of larvae in preda-tion trials.

Analysis of Larval Sensory SystemDevelopment

Subsets of larvae from each size class wereremoved from culture tanks for analyses oflarval visual and mechanoreceptive systems.Groups of 6--8 larvae from each size class werefixed in 5% phosphate-buffered formalin for his-tological analysis of organogenesis. Larvae weredehydrated, cleared, embedded in paraplast,and serially sectioned at 5 IJ.m transversely andsagittally. Sections were stained with Harris'haemotoxylin, counterstained with eosin, andviewed under light microscopy at 80--1250 mag-nification. Ontogenetic development of the lens,retina, and optic tectum were examined andswimbladder inflation was noted. Size-specificvisual acuity was calculated from retinal sectionsusing the formula: sin a = elf, where a is theminimum separable angle, e is the distance be-tween the centers of adjacent cones, andfis thefocal length of the lens (Neave 1984). Cones weremeasured as numbers per 100 IJ.m length ofretina (d), thus the reciprocal 10 d gives coneseparation in mm. The expression wao multipliedby 1.11 to adjust for approximate 10% shrinkageduring processing, and the focal length of thelens was calculated by multiplying its radius (r)by 2.55 (Matthiessen's ratio; Matthiessen 1880),giving: sin a = 0.0435/dr.

Separate groups of 6--8 larvae from each sizeclass were examined for development of freeneuromast organs. These larvae were anaesthe-tized with MS-222 and immersed in a bath of thevital stain Janus Green (0.05% Janus Greenmade up with 50% seawater) (Blaxter et al.1983). Larvae were immersed for 20--30 minutes

540

FISHERY BULLETIN: VOL. 87. NO.3. 1989

and then removed for examination of numberand location of free neuromasts under lightmicroscopy.

Histological sections also were examined todetermine the timing of swimbladder inflation inlarvae.

Data Analysis

For each predation trial, predation rate (per-cent killed in 10 minutes) was calculated from theequation: A = 1"n + 1'1 - mn, where A = totalmortality rate, rn = control mortality rate, n =experimental predation rate, and mn = the in-teraction effect which estimates the proportionof larvae consumed but which would have diedanyway from handling stress or other causes(Ricker 1975). Percentage of larvae respondingand escaping were considered total survivalrates (8) and were calculated by first estimatingtotal conditional mortality (A) (proportion "notresponding" or "not escaping") and then calculat-ing the difference as 8 = 1 - A (Ricker 1975).

Lens diameter, visual acuity, and thickness ofthe optic tectum were calculated for each larvalsize class and developmental stage. Develop-mental ontogeny of the retina, optic tectum, andswimbladder were described. The mean numberof neuromast organs also was calculated, andcomposite maps were developed of the patternsof neuromast organ formation.

Statistical analyses of data were performedusing SAS (SAS 1982) statistical programs.

RESULTS

Predator/Prey Interactions

Potential Biases

Preliminary determinations of predator errorby both predator types indicated that predatorperformance would not bias results. Mean preda-tor error per trial for northern anchovy adultsfeeding on Arte1"nia was 3.3% (range 2.1--5.1%)while error rate for juvenile white seabass was2.7% (range 0.8--6.1%). There were no signifi-cant differences in mean error rate among preda-tor groups, within trials, or between species(ANOVA, P > 0.10).

Larval mortality in control tanks (no preda-tors) was low, ranging from 0.0 to 12.5% meanvalues for any larval size group. Experimentalpredation and escape rates were adjusted by thecontrol rates.

Larval Responses

The probability of a white seabass larva re-sponding to or escaping a predatory attack gen-erally increased with larval size, although majordifferences in these responses were apparent de-pending upon type of fish predator. The meanpercentage of larvae escaping attacks by north-ern anchovy ranged from 3% in yolk-sac larvae (3mm SL) to 43% in metamorphosing fishes (15mm SL) (Fig. 2A), while the percentage re-sponding to anchovy attacks ranged from 14%(yolk-sac stage) to 56% (at metamorphosis) (Fig.2B). Mean predation rate (percentage of larvaeeaten in 10 minutes) by anchovy predators de-creased from 95% on yolk-sac larvae to 56% onearly juveniles (Fig. 2A). The predator/preyinteractions were best described by exponentialregressions (Fig. 2).

White seabass larvae were better able torespond to or escape attacks of juvenile whiteseabass than those of northern anchovy. Meanpercentage of larvae escaping white seabass at-tacks ranged from 8% for yolk-sac larvae to 74%for metamorphosing fishes (Fig. 3A), while thepercentage responding to attacks increased from18% (yolk-sac stage) to 84% (at metamorphosis)

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

(Fig. 3B). Responses and escapes from juvenilewhite seabass improved significantly in largerlarvae, particularly between the larval sizes of7.5 versus 9.0 mm SL (t-test, P < 0.01). Re-sponse and escape success nearly doubled duringthis developmental stage. Mean predation rateby juvenile white seabass predators decreasedfrom 80% on yolk-sac larvae to 65% on 6 mmlarvae, increased to 87% on 7.5 mm larvae, andthen steadily decreased to 30% on early juveniles(Fig. 3A). These predation functions also werefit to exponential regressions (Fig. 3).

The success of avoidance movements by re-sponding larvae (numbers escaping/numbers re-sponding) generally increased with larval size(Table 3). Approximately 21% of respondinglarvae in the 3.1 mm size category successfullyescaped northern anchovy attacks; this percent-age increased to 50% in 4.5 mm larvae and 75%at metamorphosis. Avoidance success from juve-nile white seabass attacks ranged from 39% for3.1 mm larvae to 75% for 7.0 mm individuals andimproved to nearly 90% in early juveniles.

Statistical comparison of the responses andescapes from northern anchovy versus whiteseabass predators indicated that a significantlyhigher percentage of larvae >6.0 mm SL

Predator: Engrau/ls mordax

I-+-+',J"1 ,1 +1 ""1

/~

-t-r--f

.... 100'f1I...... A~CJ 80~eCJ 60zi[e 40~ww 20~

FIGURE 2.-Vulnerability of white seabass larvae to Ill:adult northern anchovy predators as a function of lar- :5 0val length. A. Solid circles are percentage of larvae Bescaping an attack, error bars are 2 x SE, regression

CJequation is Arcsine Y = 5.078 eO.I44SL (on = 44, or = z 800.73), where Y = proportion oflarvae escaping and SL is ....zf.= larval standard length (mm); open circles are per- O~ 60centage of larvae eaten in 10 min trials, error bars are A.CJ2 x SE, regression equation is Arcsine Y = 81.326 ;ee-O. 036SL (n = 44, or = 0.96), where Y = propor-

~e40

tion of larvae eaten in 10 minutes and SL = larval~~standard length (mm). B. Percentage of lan'ae Te- e 20sponding to an attack, error bars are 2 x SE, regres- ...

sion equation is Arcsine Y = 15.293 eO.OSlSL In = 44, r= 0.89), where Y = proportion of larvae respondingand SL = larval standard length (mm). 0 2 4 6 8 10 12 14

LARVAL STANDARD LENGTH (mm)

541

FISHERY BULLETIN: VOL. 87. NO.3. 1989

20

80

2 4 6 8 10 12 14

LARVAL STANDARD LENGTH (mm)

B

A

60

40

j,i.....~ 100()cet:oC

CJza:ce()tJ)IUIUce>a:::5

o

CJZ 80Eiiz ....~ ~ 60mcelUI-:!C 40ceo~I-ce 20...

FIGURE 3.-Vulnerability of white seabass larvae tojuvenile white seabass predators as a function of lar-val length. A. Solid circles are percentage of larvaeescaping an attack, error bars are 2 x SE. regressionequation is Arcsine r = 10.976 eO.120SL (n = 44, r =0.89). where Y = proportion of larvae escaping and SL= larval standard length (mm); open circles are per-centage of larvae eaten in 10 min trials, error bars are2 x SE. regression equation is Arcsine Y = 81.210e-O.04SSL (n = 44,r = 0.92), where r = propor-tion of larvae eaten in 10 minutes and SL = larvalstandard length (mm). B. Percentage of larvae re-sponding to an attack, error bars are 2 /. SE. regres-sion equation is Arcsine Y = 16.822 eO.096SL (n = 44,/;!.= 0.94), where Y = proportion of larvae respondingand SL = larval standard length (mm).

Predator type

Northern anchovy White seabass

TABLE 3.-Avoidance success of responding larvae(numbers escaping/numbers responding).

escaped white seabass attacks, while a signifi-cantly higher percentage of larvae >7.5 mm SLresponded to white seabass attacks (ANCOVAwith Least Squares Means, P < 0.05). This in-creased responsiveness to white seabass preda-tors (compared to northern anchovy) translatedinto significantly reduced consumption rates bywhite seabass predators on larvae >8.5 mm SL(ANCOVA with Least Squares Means, P <0.05).

542

Larval Visual Ontogeny

The Retina and Visual Acuity

Histological examination of the white seabassvisual system revealed numerous developmentalchanges from hatch to juvenile metamorphosis.In yolk-sac larvae, the lens was present, but thel'etina was unpigmented and undifferentiated.At time of yolk absorption (ca. 3.2 mm SL), theretina became differentiated into distinct layers,the photoreceptive layer contained visual cellsand the epithelial (basal) layer became pig-mented. Presumably, at this stage the eye wasfunctional.

In young larvae (3.~7.0 mm SL), the retinaappeared to be composed of only cone cells andno retinomotor 4 mmSL, the posteroventral area of the retina (-15-20° below the horizontal plane) was character-ized by densely packed cone cells, constitutingan a-rea· tempora.lis. A lens retractor muscle firstappeared histologically at a standard length of4.5 mm (Fig. 4). Seen in sagittal section, the lensretractor articulated posteriad with the ventral

SE

7.19.17.07.56.65.14.5

iescapeSE success

4.9 38.811.5 57.913.2 70.0

6.7 80.07.3 81.15.3 90.06.0 88.0

3.2 21.44.3 47.06.8 63.07.4 51.79.2 58.8

12.4 64.314.8 75.0

Larval SL i escape(mm) success

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

floor of the retina and anteriad to the lens bymeans of an extremely thin ligament. In olderlarvae and juveniles, the lens retractor becamebipartite, presumably aiding in movements ofthe lens posteriad and/or ventrad.

The outer nuclear layer

0B -

.---. LENS DIAMETER+ -700 ........ CONE DENSITY 60 E0 - ::I.

A 0500 50 0\ 0,,% ,.- ...··l\. 0 0 /t'- - ......IS

400 f- .... , 40 c·····f.... 0 l' ->.... ,/ I-300 ...;t........... 30 CiS• __ ' •.•••,.,••0 Z" ........ 1&1

~" 00_..+ Q200 + 20 1&1,l z, 0100 .,.~ 10

(,)

0 2 4 6 8 10 12 14 300

u~

III...oc!>l-S(,)ce.Jce:::)en>

E:::L-IX

1&1I-1&1::EceQenz1&1.J

100 r-A

80

60

40

20

LARVAL STANDARD LENGTH (mm)

+

FISHERY BULLETIN: VOL. 87, NO.3, 1989

FIGURE 6.-Visual development of larval white seabass as afunction of larval length. A. Visual acuity, error bars are 2 J<SE, regression equation is Y = 138 - 18.2 SL + 0.726 SL2 tn= 66, ,,2 = 0.96>, where Y = visual aruity (min of arc) and SL= larval standard length (mm). L.R. is the first appearanceof the lens retractor muscle; Nuclei is the first appearance ofmitotic bodies in the outer nuclear layer; and R.M. is retino-motor response. B. Squares are changes in lens diameter,error bars are 2 )( SE, regression equation is Y = -58.7 +37.8 SL (n = 78,r = 0.97), where Y = lens diameter (IJom)and SL = larval standard length (mm); circles lU'e changes incone cell density, en'or bars are 2 x SE, regression equationis r = 52.6 - 2.3 SL (n = 66. ,,2 = 0.89), where Y = cone celldensity (no./100 IJom) and SL = larval standlU'd length (mm).Open circles are measurements taken in the area. temporalis.Values for a 30 mm SL juvenile are given for comparison tolarvae.

FIGURE 7.-Retinomotor response of a 12.5mm SL. light-adapted white seabass larva.showing migration of the epithelial maskingpigment. ONL is the outer nuclear layer.x400.

544

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

FIGURE 8.-Cross-section through the optictectum of a 9.2 mm SL white seabass larva. Thetectum is bilayered at this stage, with an innerstratum perit'entriculare (SPV) and an outerstratum zonale (SZ). The SZ is thickening andexhibits increasing numbers of neurons migratingfrom the inner layer. The torus longitud'inalis (T)is quite prominent by this stage. x !OO.

III: 100ILl A>c 80-IIII: T.L.ILlz_ 60 + -t--"",-tzo ,t----t----0',.. r...~·-·~-......'"11I:1(1:- 40c ,-I +III: 20ILl...::::l0 0

300 BE e-- ... TOTAL..:! 0---0 OUTER LAYERrn 250

-+----f----1rnILlz 200 ..---lIIIi:U .r'":c... 150 , --~:Ii I ~ _-::::l "'. -~---- -...

100,... fr--

u1'/ t/ILl...

50 ~.¢--4

f

+

t

'--''---'--J..---L.....L.......L.......L......J...-.J..-.L.......J'---'--J..---L.......L-..r~

o 2 4 6 8 10 12 14 30LARVAL STANDARD LENGTH (mm)

length (Fig. 9B). Growth and differentiation ofthe SZ appeared to involve cell migrations fromthe inner SPY with a progressive increase in theSZ:SPV ratio (Fig. 9A). This ratio increasedrapidly at first feeding (-3-4 mm SL), stayedconstant at lengths of 4.0-7.5 mm SL, and thenincreased again from 7.5 mm to early juvenilestages.

Another important event in the ontogeny ofthe optic tectum involved the development of thetarus longitu.dinaJis (TL). This structure firstappeared histologically at a larval length of6.8--7.0 mm SL (Fig. 9A). Seen in transversesection, the TL developed as a teardrop-shapedstructure with a wide area of contact dorsad withthe optic tectum and ventrad with the epithala-mus (Fig. 8). The TL continued to grow withontogeny, and in older larvae and early juvenilesthe TL exhibited an increasing number ofneuronal projections to the cerebellum.

FIGURE 9.-Development of the optic tectum of larval whiteseabass as a function of larval length. A. Change in the ratioof the outer layer/inner layer, T.L. is the first appearance ofthe toms longitudinalis. B. Solid circles represent totalthickness of tectum. error bars are 2 x SE, regression equa-tion is :r = -48.6 + 38.8 SL - 1.35 SL2 (11 = 64,r = 0.97),where Y = total width of tectum (ILm) and SL = larvalstandard length (mm); open circles represent thickness ofouter layer, error bars are 2 x SE, regression equation is r= -33.8 + 20.3 SL - 0.56 SL2 (n = 60,,2 = 0.97), where Y= width of outer layer (ILm) and SL = larval standard length(mm). Values for a 30 nml SL juvenile are given for compari-son to larvae.

545

Ontogeny of Mechanoreceptors

Neuromast Development

Staining with Janus Green provided somewhatvariable results, in that not all white seabasslarvae took up the stain equally well. Someneuromast organs stained better than others,but the use of 6-8 fish per larval size classseemed to provide good composite patterns ofneuromast formation.

At hatching, larvae had 5 or 6 pairs of neuro-masts on the head and 5 or 6 pairs extendingalong the trunk (Fig. lOA, B). All of theseorgans appeared to be free neuromasts (not en-closed by canals). Each free neuromast consistedof a basal, naked neuromast organ attachedapically to a cylindrical, gelatinous cupula. The

FISHERY BULLETIN: VOL. 87. NO.3. 1989

only other stained structures were the nasalpits.

The total number and patterned formations offree neuromasts increased with ontogenetic de-velopment (Figs. 10, 11). At first feeding, larvaehad 6-8 neuromasts on the head and 6 or 7 on thetrunk. During development, new head neuro-masts appeared first in the supraorbital and in-fraorbital areas, while on the trunk they re-cruited midlaterally (Fig. 11). The period of mostrapid addition of free neuromasts was in thelarval size range of 4-9 mm SL. During the earlypostflexion stage (-7-10 mm SL), free neuro-masts began to form in distinct supraorbital. in-fraorbital, and preopercular (hyomandibular)rows on the head and in a single midlateral rowon the trunk (Figs. 10, 11). By 12.5 mm SL,

60 A / .../

rn A/TOTAL... 50 ...-rn ,/c ......,..... ,/:E0 40

/l' ~~~~+a::=wz 30 .+ +............... -t... ~II.0 ,~{ .....·t······· , ,/'r;;;;Ka:: 20wID +t'-f ......t",A---9"'/:E= .J ,r + +Z 10 + +.,.~"9' .1.0.. P.O. Partial L.L. H••d

Partial Partial L.L. Canal. Dlallnct

02 4 6 8 10 12 14 16

60

rn... 50rnc:E0 40a::=wz 30II.0a:: 20wID:E=Z 10

0 5 10 15 20 25 30 35 40

LARVAL AGE (days)

FIGURE lO.-Numbers of free neuromasts developing on larval whiteseabass as a function of larval length (AI and age (8). Error bars are 2x BE. 1.0.'s are infraorbital and supraorbital rows on the head; P.O. isthe preopercular or hyomandibular row on the head; and L. L. is thelateral line. Values are based on staining and should be consideredapproximate only.

546

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

FIGURE 1I.-Composite maps showing the location of free neuromast organs during development of white seabass larvae. Larvaloutlines were modified from those of Moser et al. (1983).

some of the recruiting neuromasts were beingenclosed by canals on the head and trunk; someexisting free neuromasts were being incor-porated in canals as well. At juvenile meta-morphosis, the three major branches of the headcanals, as well as the lateral line on the trunk,were fairly distinct (Figs. lOA, 11), forming theprecursor to the juvenile and adult lateral linesystem.

Swimbladder Development

In yolk-sac larvae, the swimbladder appearedas a collapsed sac dorsad to the yolk sac, while infIrst-feeding larvae it was still partially flattenedand situated dorsad to the anterior digestivetract. Timing of complete swimbladder inflationwas variable; most larvae exhibited full inflationat lengths of 4.f>-5.5 mm SL. In larvae >4 mm, apneumatic duct was present in the anterodorsalarea of the swimbladder. It was not clearwhether swimbladder inflation occurred by wayof air-gulping at the surface or by gas secretioninternally.

DISCUSSION

Neurosensory Basis For AvoidanceResponses

The overall probability of white seabass larvaeescaping predatory attacks seems highly depen-dent on the size of the larvae, the type and qual-ity of sensory input being integrated by thelarvae, and the type of predator encountered(Fig. 12). Yolk-sac larvae have nonfunctionaleyes, a small number of free neuromast organson the head and trunk, and a noninflated swim-bladder. At fIrst feeding (-3.2 mm SL), the eyebecomes functional, but visual acuity is poor; thepure-cone retina limits peripheral vision and mo-tion detection, and no accommodation is possible(since there is no lens retractor muscle). There isstrong correlative evidence that increases innumbers of free neuromasts and improvementsin the visual system are responsible for theimproved avoidance responses observed in pre-dation trials. In larvae

FISHERY BULLETIN: VOL. 87, NO.3, 1989

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54

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01 45 10 15 20 25 30 35I I

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FIGURE 12.-Developmental events and sensory system development during the early life history of the white seabass. Format isbased on Hunter and Coyne (1982). Developmental data are from my study, except some behavioral data from Orhun (unpubl.data) and osteological data from Moser et al, (1983). Y-S = yolk-sac stage, 1.0. = infraorbital, S.D. = supraorbital, H.M. =hyomandibular, L.L. = lateral line, T.L. = tOTltslongitudinaUs, ONL = outer nuclear layer of retina.

acuity is poor and no acoustic inputs are likelythrough the swimbladder. During notochordflexion (-5--7 mm SL), visual accommodation isdeveloped with the lens retractor muscle, theswimbladder is inflated (potentially providingacoustic stimuli), and there begins a major re-cruitment of free neuromasts on the head andtrunk. Up to this point in development, it wouldappear that vision plays a limited role in preda-tor detection.

During the early postflexion stage (-7 mm),the visual system begins to undergo numerouschanges (Fig. 12). Acuity continues to improve,early rod precursors develop in the retina, theoptic tectum increases markedly in size andstratification, and the torus longitu,din..alis be-gins to develop in the midbrain. At 10.5--12.5 mmSL, double cones and early rod cells are presentin the retina. These changes are essential to

visual improvement and integration. Visualacuity calculated for most adult marine fishes is2--10 minutes of arc (Tamura 1957); values foradult white seabass are unknown but probablyfall in this range. Thus, approximately 75--80% ofthe improvement in acuity seen from hatch toadult stage in white seabass has occurred by thelate larval stage. However, for vision to playamajor role in predator detection, improvementin acuity must be accompanied by developmentof rod cells, by accommodation to distant objects(lens retractor muscle), and by growth and de-velopment of the optic tectum. The developmentof rod vision helps to improve peripheral vision(O'Connell 1981) and motion detection (Blaxter1986), both crucial aspects of predator detection.Rods also aid in improved visual performance indimmer light (O'Connell 1981), which wouldimprove foraging skills and predator-detection

548

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

as white seabass become more demersal. Growthand stratification of the optic tectum allow formore complex interconnections with other braincenters in teleosts and are essential for the de-velopment of progressively more sophisticatedbehavioral responses (Munro 1984). The taru,slongitu.dinalis functions in midbrain integrationof proprioceptive information (Groman 1982) andis involved in the control of visual motor patterns(Munro 1984).

The free neuromasts in fish larvae probablyfunction in detection of differences in velocitybetween the fish and surrounding water. Theincorporation of neuromasts into canals (as oc-curs in older white seabass larvae and earlyjuveniles) probably aids in schooling or detectionof accelerations in water movements caused byother animals, such as predators (Blaxter et al.1983). The increases in numbers and in pat-terned formations of neuromasts with white sea-bass larval size probably improve detection ofpredator movements and aid in swimming move-ments and proprioception.

During the early postflexion stage (7.5--10.0mm SL), these improvements in mechanorecep-tive and visual capabilities appear to be directlyrelated to improved detection and escape re-sponses. However, depending upon the type ofpredator encountered. a significant differenceexists in the degree of improvement in avoidancecapabilities (Fig. 12). Early postflexion larvaeexhibit a modest improvement in evading north-ern anchovy attacks, but display a dramatic im-provement in detecting and escaping the slower,more discontinuous attacks ofjuvenile white sea-bass. Since some startle responses are elicitedeven in yolk-sac larvae, it appears that neuralmotor pathways such as Mauthner-type neurons(Eaton and DiDomenico 1986) are present andfunctioning during all developmental stages.Just prior to and during the early postflexionstage, larvae undergo notable additions ofneuro-mast organs and major improvements in the vis-ual system. Since the outcome of a predator-preyinteraction is heavily dependent upon reactionvelocity and timing (Webb 1976), the slower,close-range attacks of juvenile white seabassprobably allow more time for detection of sen-sory stimuli from several modalities as well assensory-motor integration needed for responseand escape movements.

Improvements in visual and mechanoreceptivesystems have been implicated in the evasion be-haviors of northern anchovy larvae (Webb 1981;Folkvord and Hunter 1986), while acoustic stim-

uli detected through the gas-filled otic bullaeseem important in the development of startleresponses of Atlantic herring larvae (Fuiman1989). The inflation of the otic bullae with gasand the occurrence of a well-developed acous-tico-Iateralis system, however, seems to be morecharacteristic of clupeoid larvae (Fuiman 1989).Although acoustic stimuli or Rohon-Beard(mechanoreceptive) input could also be related toimproved evasion I'esponses of white seabasslarvae, the observed improvements in theneuromast and visual systems seem to bedirectly related to the improved avoidancecapabilities.

Larval Vulnerability to AttacksLarval size and developmental stage are the

most important factors related to larval vulner-ability in laboratory trials. The type of predatorencountered also influences predation rates.However, although white seabass larvae werebetter able to respond to juvenile white seabassattacks than those of northern anchovy, this didnot result in significantly reduced predationrates (in comparisons between predator types)until larvae were >8.5 mm in length. This sug-gests that other factors related to predator de-tection of prey, such as prey morphology, waterclarity, and alternative prey abundance, may beas important as predator type in controlling vul-nerability of small white seabass larvae. Physicalbackground and morphological conspicuousnessof prey can be important factors controlling pre-dation rates of planktivorous fishes (Vinyard andO'Brien 1976), while relative abundance of al-ternative prey has been shown to have signifi-cant effects on fish consumption rates on smallwhite perch larvae (Margulies in press).

One disadvantage of laboratory studies is thatrealistic encounter rates between larval preyand fish predators are difficult to simulate. Al-though the main purpose of this study was todelineate the developmental basis for larvalavoidance behaviors, it is important to recognizethe limitation of predicting total vulnerability oflarvae based on laboratory trials only. Total vul-nerability to predation is a function of the prob-ability of encounters between predator and prey,the probability of capture of prey and the prob-ability of attacks by a predator (O'Brien 1979).My data provide reliable estimates of probabilityof prey capture and, to a lesser degree, probabil-ity of attacks by the experimental fish predators.Encounter rates. however, are affected by a

549

number of larval growth-related parameters, in-cluding increased larval swimming speeds andsearch volumes and increased conspicuousness oflarger larvae (Hunter 1981). It is possible thatincreasing encounter rates between a suite ofpredators and larger white seabass larvae in na-tural systems would offset the observed steadyincrease in detection and escape responses ob-served in larger larvae in laboratory trials. Thiscould occw' until larvae became invulnerable toattacks. My laboratory data provide some hint ofthis pattern in the slightly increased predationrates on larvae in the 4.5--7.5 mm size range (seeFigures 2A, 3A). However, white seabass lar-vae are relatively inactive and become increas-ingly demersal during ontogeny, thus, theymight not be subject to significantly higherencounter rates with predators. This remainsspeculative, however, and is an area for futureinvestigation.

Implications for White Seabass EarlyLife History

Compared with white seabass larvae, Cali-fornia sardine, Sardinaps sagaa~, and northernanchovy larvae (co-occurring pelagic larvae innearshore southern California waters) appearbetter able to detect and avoid attacks by adultnorthern anchovy predators at comparablestages of larval development (Folkvord andHunter 1986; Butler and Pickett 1988). Thesetwo clupeoid species also exhibit schooling be-havior in the later larval stages. Many speciesexhibit a combination of larval adaptations tominimize fish predatioJl, including long peliodsof transparency (e.g., dover sole, Microsfom:u.spaC"ificus; Hunter!), rapid development of avoid-ance capabilities (northern anchovy and sardine)and schooling (clupeoids). During early feedingstages, white seabass larvae develop a robust,highly pigmented body form and exhibit limitedmobility. During the early postflexion stage(7-10 mm), white seabass start to abandon astrictly pelagic distribution and become notice-ably more demersal. By the late larval and earlyjuvenile stage, they are found almost exclusivelyassociated with submerged cover (often driftalgae) or near-bottom habitats (pers. obs.; Allenand Franklin 1988; Orhun2; KramerS). In near-shore waters of southern California, other

IJ. R. Hunter. UnpubI. data. Southwest FisheriesCenter La Jolla Laboratory, National Marine Fisheries Ser-vice. NOAA, La Jolla, CA 92038.

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FISHERY BULLETIN: VOL. 87. NO.3. 1989

sciaenid larvae show a marked vertical size dis-tribution during daylight hours, with largerlarvae (postflexion and larger) occurring in high-est densities in suprabenthic habitats andsmaller larvae occurring higher in the water col-umn (Love et aI. 1984; Jahn and Lavenberg1986). The suprabenthic distribution of largerlarvae has been characterized as a possible adap-tation to high concentrations of food, for preda-tor-avoidance or for maintenance of position onthe continental shelf. However, recent studies ofwhite croaker, Genyo·menu.s linecLfus, larvae in-dicate that the suprabenthic distribution of oldersciaenid larvae is probably not related to feeding(Jahn et aI. 1988).

My results indicate that this ontogenetic shiftdeeper into the water column by older whiteseabass larvae (and other sciaenids) may be re-lated to their predator-avoidance capabilities.The dominant planktivorous species encounteredin midwater habitats of nearshore southern Cali-fornia waters are fast-swimming, shoalingpelagics such as northern anchovy, sardine, andPacific mackerel, Scom.ber japonkus. Potentialplanktivores in near-bottom habitats includesciaenids, gobiids, embiotocids, clinids, ser-ranids, and various flatfishes (Eschmeyer et aI.1983). All of these demersal species exhibit sometype of ambush, hovering, discontinuous, orclose-range mode of predatory behavior, similarto the attack behavior of juvenile white seabass,and all attack at slower speeds than the shoalingpelagics. Based on my experimental evidence, itis likely that, as they drop out of the plankton,older white seabass larvae maximize their preda-tor-detection and avoidance capabilities whenencountering demersal predators. Remaining inthe plankton in later larval stages and beingexposed to pelagic, shoaling fish predators wouldprolong a peliod of extreme vulnerability, whileshifting to a demersal disttibution would placewhite seabass in habitats to which they are bet-ter suited developmentally.

ACKNOWLEDGMENTS

I would like to thank Refik Orhun. ChrisDonohoe, and Donald Kent of the Hubbs MarineResearch Center in San Diego for providing

2R. Orhun. Unpubl. data. Hubbs Marine ResearchCenter, Sea World, San Diego. CA 92109.

3S. Kramer. UnpubI. data. Southwest FisheriesCenter La Jolla Laboratory, National Marine FisheriesService. NOAA, La Jolla, CA 92038.

MARGULIES: VULNERABILITY AND SENSORY DEVELOPMENT OF WHITE SEABASS

white seabass eggs and juveniles. Many staffmembers of the Southwest Fisheries Center inLa Jolla provided laboratory facilities or helpfuladvice during the study; they are Roger Leong,Eric Lynn, Bev Macewicz, Carol Kimbrell,Sharon Kramer, Steve Swailes, Mark Draw-bridge, Gail Theilacker, and Geoffrey Moser.Henry Orr, Roy Allen, and Ron Keefe providedgraphics assistance. John Hunter and twoanonymous referees reviewed earlier versions ofthe manuscript. I am especially grateful to JohnHunter and the late Dr. Reuben Lasker for pro-viding the opportunity to undertake this re-search project. Financial support was providedby a NOAA postdoctoral fellowship through theAssociateships Program of the National Re-search Council.

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