The Larval Development of the Sand Crab Emerita rathbunae Schmitt

(Decapoda, Hippidae) !

MARGARET D. KNIGHT

Two SPECIES of the sand crab Emerita have beenfound on the western coasts of N orth and SouthAmerica. Emerita analoga (Stimpson) has beenrecorded from Vancouver Island, British Colum­bia (Butler, 1959) to Magdalena Bay, BajaCaliforn ia, and from Salavery, Peru to EdenHarbor, Territory of Aysen, Chile (Haig,1955) . Dr. Ian Efford (personal communica­tion of unpublished observations) has foundthat the northern limit of the species may beKodiak Island, Alaska, and that the southernlimit of its range in South America is the Straitof Magellan. E. ratbbunae Schmitt has beenfound from La Paz, Baja California to Capon,Peru (Schmitt , 1935) . Specimens of E. ratb­bunae have also been collected at San Francis­quito Bay, on the east coast of Baja Californiaabove La Paz (Steinbeck and Rickets, 1941).

The larvae of Em erita analoga were describedby Johnson and Lewis ( 1942) . Th e first zoeawas obtained from eggs hatched in the labora­tory and one individual molted to the secondstage. Later stages were described from pre­served plankton samples. Larvae of the specieshave subsequently been cultured from egg tomegalopa by Dr . Ian Efford (pe rsonal com­munication) . During the present study, larvaeof the tropical species Em erita ratbbun ae werecultured in the laboratory and compared withspecimens from the plankton to provide adetailed descript ion of the sequence of larvaldevelopment and a means of differentiating thelarvae from those of the amphi-tropical speciesE. mzaloga.

The larvae of three other species of Emeritahave been investigated. Menon (1933) ob­tained five zoeal stages of E. em erita (1.) fromthe plankton, the larvae of E. talpoida (Say)have been described both from laboratory cuI-

1 Contribut ion from Scripps Institution of Ocean­ography, Uni versity of California , San D iego. Manu­script received January 18, 1966 .

58

tures (Rees, 1959) and from the plankton(Smith , 1877), and larvae of E. boltbnisiSankolli have been studied in the laboratoryby Sankolli (1965) .

METHODS

An ovigerous female of Emerita ratbbunaewas collected from a sandy beach near La Playa,Mazatlan, Mexico, on 20 September 1963 dur­ing a cruise in the Gulf of California aboardR/V "Alexander Agassiz" of the Scripps In­stitution of Oceanography. The female was heldaboard ship in a 3-gallon aquarium . Hat chingof the eggs began 12 hours after capture. Thelarvae were maintained in groups of 10- 25 in4-inch glass finger bowls of 1200 cc capacityor in plastic containers of 400 cc capacity. Theywere transferred daily to fresh sea water andfed newly hatched nauplii of A rtemia salina(1.) . All larvae molted once during the sixdays' culture period aboard ship. In addition,one second zoea of the species was sorted froma plankton tow taken earlier near shore belowCape Corrientes, Mexico (19° 22' N , 105° 03'W ) , and was maintained in isolated cultureaboard ship for 11 days. A surface temperatureof 29.6° C and salinity of 33 .9%0 wererecorded for the water from which the larvawas taken. The salinity of water used for cul­tures was 33. 8- 33 .9%0' As the ship returnednorth from the collecting area, the temperatureof the water held in the cultures dropped from29° to 23° C, subjecting the larvae to consider­able cooling during the early zoeal stages.

At the conclusion of the cruise, the approxi­mately 100 larvae hatched aboard ship ( then instages II and III) , and the single larva takenfrom the plankton were transferred to the lab­oratory and isolated either in compartmentedplastic trays holding 50 cc per compartment, orin plastic boxes of 400 cc capacity. The y weretransferred daily to sea water filtered through

Larval Development of Emerita rathbtmae-KNIGHT 59

glass wool, and fed newly hatched Artemianauplii. The laboratory cultures were main­tained at room temperature which, because ofseasonal cooling, decreased gradually from 22°to 19° C, with daily fluctuations of 1° C or less.The salinity range during the culture period was33.5-33.8%0' The larvae were kept undernatural illuminat ion but away from direct sun­light.

Both aboard ship and in the laboratory, allexuviae and some specimens of each develop­mental stage were removed and preserved in5% formaldehyde buffered with hexamethylenetetramine. The casts were transferred to glyc­erine for study. The cultures, the preservedspecimens, and the exuviae were maintained insuch a way that the individual history of eachlarva could be followed. In the course of thestudy, 328 exuviae and 50 specimens of rearedlarvae were examined and dissected.

In order to compare zoeal stages occurringnaturally in the plankton with those obtainedin the laboratory, 143 zooplankton samples(taken in August-September and November­December in the area between Cape San Lucasand Cape Corrientes, north into the Gulf ofCalifornia to Tiburon Island, and along thewest coast of Baja California north to Magda­lena Bay) were examined. The majority ofsamples were taken with a I-meter net towedobliquely from 140 m to the surface, filteringapproximately 500 m", during cruises 5612(SIO Ref. 61-22, 1961), 6108 (SIO Ref. 62­16, 1962), 6208-9, Azul II and El Golfo(Snyder and Fleminger, 1965). A total of 150specimens were obtained for comparison withcultured larvae. In addition, 70 larvae ofEmerita analoga were sorted from zooplanktonsamples taken off Point Conception, on cruises32 (SIO Ref. 52-1, 1952a) and 33 (SIO Ref.52-7, 1952b) and off the Coronado Islands,for detailed comparison of the two species.

Larvae were dissected in glycerine. Drawingsof whole specimens and appendages were pre­pared with the aid of a camera lucida. Youngstages were stained with lignin pink to facilitatedissection and study.

RESULTS

The cultured larvae molted 7, 8, or 9 timesbefore metamorphosis to megalopa, with the

majority passing through 8 zoeal stages. Thestages became progressively longer and the dura­tion of the last stage was twice that of the pre­ceding one (Table 1). Of the larvae cultured42% completed zoeal development and moltedsuccessfully to megalopa. The highest mortality(20%) occurred in the terminal stage.

Within stages I, II, and III morphologicaldevelopment was similar for all individuals. Insubsequent stages, slight variation was foundamong individuals that completed developmentin seven zoeal molts, but larvae passingthrough eight or nine stages showed consider­able individual variation in relative growth andsetation of appendages, so that the number ofstages through which an individual had pro­gressed could be positively ascertained, beyondstage IV, only by a study of its molting history.Despite this variability, the order of develop­mental events was similar for all larvae. Thedegree of growth attained with each molt be­yond stage III decreased with an increase in thenumber of zoeal stages in the larval period,but the terminal zoeas were alike in develop­ment of appendages (addition of pleopods,growth of thoracic appendages and flagellumof second antenna, etc.) and differed mainly indetails of setation and size. No larvae inter­mediate between the terminal zoea and mega­lopa were observed.

The variation among the cultured larvae innumber of zoeal stages, and in morphology ofindividuals with similar molting histories,prompted detailed examination of specimensfrom preserved plankton samples. The ratios ofcarapace length to rostrum length (Table 2),together with study of appendages, were usedfor identification of planktonic specimens. Thestage of development was determined by exami­nation of the natatory setation of the first andsecond maxillipeds and of relative change inother appendages. The cultured larvae, hatchedwith four natatory setae on the exopodites ofthe first and second maxillipeds, added twosetae with each molt through stage III. Eitherone or two setae were added with each succes­sive molt. Rees (1959:368) and Sankolli(1965:39) found similar patterns of progres­sive increase in setation in cultured larvae ofE. talpoida and E. boltbuisi. Planktonic larvaeof E. ratbbunae, with rare exceptions, had only

TABLE 1

D URATION AND N UMBER OF ZOEAL STAGES FOR LARVAE COMPLETING THE MOLT TO MEGALOPA(Means given for isolated cultures only )

DAYS IN STAGENO. OF ZOEAL NO. OF

STAGES LARVAE I II III IV V VI VII

Cultured lar vae7 4 mean - - - 5.3 9.3 11.5 31.8

range 5 5-6 4-6 5-6 8-10 10-13 22-43

8 22 mean - - 5.3 6.5 9 .0 8 .9 12.4range 5 5-6 4- 6 5-8 7- 11 7- 12 11-16

9 3 mean - - - 7 8 9 .7 9.7ran ge 5 5-6 4-6 7 7- 9 8-12 9-10

Plankto nic larva8 3 3 7 8 14

D uration megalopa stage for 6 individu als: mean 12.5 daysrange 10- 13 days

0\o

VIII IX

30.7 'i:i>

22-43 ()-13.3 29.3 'T.I-11-16 27-31 ()

C/l()-?30 tTlZ()

Fl<:~

XX.r-'-'I>'

;:)

I:I>'....

'<......\00\-...J

Larval Development of Em erita rathbtmae- KNIGHT 61

ZO EA I (Fig. 1 ): The zoea is colorless andtranslucent, the rounded carapace has a short,

FIG. A. Average length of carapace (posteriormargin to tip of rostral spine ) for zoeal stages ofcultured and plankton ic larvae of Emerita ratbbunae,X, Planktonic larvae ; 0 , cultured larvae ; T, termina lzoeal stage; (), average based on less than 10 speci­mens.

X T

XT OT

ron( Xl

( 0)

6( 0 )

5

EE (0)

4

only a single specimen, it provides a link be­tween the cultured and planktonic forms as wellas an indication of the potential variability inthe larval development of E. ratbbunae ,

D escription of Larval Stages

To facilitate identification of the larvae ofE. ratbb unae in the plankton, the descriptionsof intermediate stages IV and V are based uponplanktonic specimens rather than upon the vari­able forms obtained in the laboratory. Thedescriptions of stages I-III and the terminalzoea are based upon both cultured and plank­tonic larvae for structure and development ofappend ages; the setation is based upon zoealstages from the plankton. Measurements of thezoeal stages are given in Table 2. Averagefigures are based upon measurements of 10 ormore specimens, except for zoea VI (n ot ter­minal) , for which only 5 specimens were avail­able. The length of rostrum and carapace weremeasured from the posterior margin of eyestalk.The length of telson excludes telson processes.

VIIIVIIVIVIV

ZOEAL STAGES

III

XO

an even number of setae on the exopodites ofthe maxillipeds. This setation, therefore, ap­peared to be a reliable indication of the numberof molts through which an individual hadprogressed.

In samples examined, 67% of the planktoniclarvae of E. ratbbunae apparently would havemolted to megalopa after six zoeal stages, 33%after seven zoeal molts. This represents, on theaverage, an abbreviation of the zoeal develop­ment observed in the laboratory-reared animals.Comparatively few differences were observedbetween individuals in comparable zoeal stages.

There were no detectable morphological dif ­ferences between cultured and planktonic larvaewithin stages I, II , and III. In intermediate in­stars IV- VI, a detailed comparison of the larvalcycle of seven zoeal stages, common to bothcultured and planktonic forms, showed that cul­tured larvae were less advanced in growth andsetation of some appendages than were plank­tonic larvae in equivalent stages. The terminalzoeas again were similar. The cultured larvaewere smaller than planktonic larvae at compar­able stages of development beyond stage I(Fig. A) , but the distinctive proportions ofthe carapace and its rostral and lateral spineswere consistent in both cultured and plank tonicforms throughout zoeal development.

The second zoea of E. ratbbunae, sorted fromliving plankton, was cultured for 7 of the 11days aboard ship under condit ions comparablewith its natural environment. During this periodit molted three times, following exactly the pat­tern of growth and setation observed in plank­tonic specimens preserved from the same area.The larva was transferred to the laboratory instage V and died in stage VIII , before the moltto megalopa (indicated by segmentation of post­larval appendages visible beneath the cuticle) .In stages V-VII, the rate of development ofappendages was retarded in relation to theregular progressive setation ( 2 setae per molt)of the first and second maxillipeds. This larvadeveloped more rapidly than did larvae hatchedand cultured aboard ship which had been sub­jected to environmental change at an earlier age,but it was less advanced in the late instars thanwere larvae studied from the plankton. Al­though the evidence for modification of moltcycle midway in zoeal development is based on

TABLE 2

MEASUR EMENTS (IN M M ) OF Z OEAL STAGES OF Emerita ratbbunae, AND OF STAGES I-IV AN D THE T ERMINAL Z OEA OF E. analoga (IN ITALICS)

0\N

Larval Development of Emerita rathbtmae-KNIGHT 63

5

0.5 mm

0 .5 mmI-----i

3-5

FIGS. 1- 5. Emerita ratbbunae, Zoea I-V.

64

broad rostral spine; the lateral spines character­istic of later stages are absent. The large eyesare stalked.

Th e first antenna (antennule) (F ig. 11) isconical and unsegmented, tapering distally toa blunt tip which bears 3 aesthetes and 2 hair­like setae.

Th e protopodite of the second antenna ( Fig.17) is produced into a strong lateral spine andbears a slender inner spine of approxi mately thesame length. A small spine is situated ventrallyat the base of the medial spine.

The mandibles (Fig. 23) are armed withstrong ventral teeth, short triangular teeth, andslender spines. The ventral tooth of the leftmandible is split shallowly at the tip. Thereis little change except growth durin g zoealdevelopment.

The coxal endite of the first maxilla (maxil­lule) (Fig. 24) bears 3 terminal setae with 1small seta subterminally on the inner margin.The basal endite bears 2 strong curved spinesarmed with tiny spines, the small unsegmentedendopodite bears a single long seta.

Th e protopodite of the second maxilla ( Fig.26) is tr iangular, bearing 3 setae on the bluntanterior margin , 1 set slightly apart toward thescaphognathite, and 1 small seta subterminallyon the inner margin. In later stages, the anteriortip becomes more pointed and the 3 setae moreevenly spaced ( Fig. 27) . The scaphognathitebears 7- 8 plumose setae on the anterior-outermargin ; one-third of the specimens dissected,from both hatching and plankton, had 7 setae.

The short coxopodite of the first maxilliped( Fig. 29) is unarmed. Th e basipodite bears 7setae along the medial margin in groups of1- 1-2- 3 progressing distally. Th e endopoditeis 4-segmented; the first three segments arearmed along the inner margin as follows: firstsegment with a group of 3 setae, one conspicu­ously stronger than others and armed with tinyspines ; second segment with 2 setae, again onebeing stout and armed with spinules; third seg­ment with 2 setae spaced around the distal mar­gin of the segment. Th e fourt h segment bears4 terminal setae ; the outer 2 setae are quitelong and armed with spinules on the innermargin. Th ere is also a short hairlike seta placedsubterminally on the outer margin which fre­quently curves in between the terminal setae

PACI FIC SCIENCE, Vol. XXI, January 1967

and is difficult to see without high magnifica­tion. Th e exopodite consists of 2 segments; thevery short, often weakly delineated, terminalsegment bears 4 long plum ose natatory setae.

The coxopodi te of the second maxilliped( Fig. 28) is unarmed, the basipodite bears 3setae on the inner margin in groups of 1- 2progressing distally. The endopodite consists of4 segments. Along the medial margin , the firstsegment bears 3 setae distally, the second seg­ment bears 1 seta, and the th ird segment has2 setae around the distal margin of the segment.The fourth segment bears 4 terminal setae and1 small subterminal seta on the outer margin asdescribed for the first maxilliped. The exopoditeis 2-segmented, the small terminal segment bears4 plum ose natatory setae.

The abdomen consists of 5 segments. The firstis very weakly differentiated. The sixth segmentis consolidated with the telson, as shown bythe position of the uropods in subsequent stages.

The telson ( Fig. 34) is rounded, slightlyconcave, and usually about as wide as long, occa­sionally slightly longer than wide. Th ere are 2prominent posterior-lateral spines notched nearthe tip on the outer margin . Between the lateralspines there are 25-27, usually 26, spinesaround the posterior margin of the telson, witha series of very small denticles between thespines. Th e eigh th spine from either side issomewhat longer and more prominent than theremaining spines; all are armed near the basewith small spinules. Ther e is little changethroughout zoeal development except for anincrease in number of denticles between theterminal spines.

In the following stages, unless noted, thereis no change in setation and form of appendagesdescribed and figur ed for zoea 1.

ZOEA II ( Fig. 2): There is now a pair ofshort lateral spines on the carapace.

Th e first antenna ( Fig. 12) terminates with1 large aesthete and app roximately 3 smallhairlike setae.

The second antenna ( Fig. 18) bears a smallsubterminal spine on the medial margin of thelateral spine.

Th e basal endite of the first maxilla ( Fig.25), with the addit ion of 1 spine, now bears3 strong curved spines armed with spinules;

Larval Development of Emerita rathbllllae-K NIGHT 65

I mmI-------i

7 -8

7

8

I mm

9

10

FIGs. 6-10. Emerita rathbunae, 6, Zoea VI ; 7, zoea IV, dorsal; 9, zoea IV, telson. Emerita analoga, B,Zoea IV, dorsal; 10, zoea IV, telson.

66

the inner two spines are articulated at the base.There is no other change and the first maxillamaintains this form throughout zoeal develop­ment.

The scaphognathite of the second maxillabears usually 8, occasionally 9, plumose setaeon the anterior-outer margin.

The exopodites of the first and second maxil­lipeds bear 6 plumose natatory setae.

ZOEA III (Fig. 3) : The first antenna (Fig.13) bears 3 aesthetes and 3 small setae on thetip. One aesthete is slightly larger and set apartfrom the other two in the terminal groupingfound throughout further zoeal development.

Small spines have been added distally onboth lateral and medial spines of the secondantenna (Fig. 19).

The scaphognathite of the second maxillamay have 9 or 10, rarely 11, plumose setae onthe anterior-outer margin.

The exopodites of the first and second maxil­lipeds bear 8 plumose natatory setae.

A pair of uniramous, 2-segmented uropods(Fi g. 31) are now present on the anterior­ventral portion of the telson. Each of the distalsegments bears 2 slender curving terminal setaearmed with tiny spines distally ; the inner seta islongest.

ZO EA IV (Fi gs. 4, 7) : The first antenna (Fig.14) now bears a subterminal tier of 2 aestheteson the medial margin.

Th e flagellum of the second antenna (Fig.20) appears in this stage as a slight roundedprominence to a small bud.

Th e number of plumose setae along the outermargin of the scaphognathite of the secondmaxilla ranged from 15 to 21; most specimenshad 17-20.

The exopodites of the first and second maxil­lipeds bear 10 natatory setae, and the basipoditeof the first maxilliped may have 8 setae alongthe inner margin in groups of 1- 2- 2-3 pro­gressing distally.

Small buds of the third maxilliped and tho­racic appendages are present beneath the cara­pace, posterior to the second maxilliped.

The exopodites of the uropods (Fig. 32)now bear 4 terminal setae of varying lengths;the third seta is the longest. Th e endopodite

PACIFIC SCIENCE, Vol. XXI, January 1967

may appear in this stage as a rudiment or asmall bud.

The telson (Fig. 9) has become somewhatlonger than wide and remains so in subsequentzoeal stages.

ZOEA v (Fig. 5) : The first antenna (F ig.15) bears usually 2, occasionally 3, subterminalgroups of aesthetes along the medial margin;only one-fourth of the specimens dissected had3 tiers of aesthetes. The majority of larvae had4 subterminal aesthetes in groups of 2- 2 ; rarelyan additional aesthete was added to form groupsof 2- 3 progressing distally. Those larvae with3 subterminal tiers of aesthetes added them ingroups of 2-2-3, rarely 1- 2-3.

The flagellum of the second antenna (Fig.21) is now slightly shorter than to slightlylonger than the 2 spines of the protopodite.

The scaphognathite of the second maxillabears 24-39 plumose setae along the outermargin ; most individuals had between 30 and34 setae.

The exopodites of the first and second maxil­lipeds bear 12, rarely 11, natatory setae. Thebasipodite of the first maxilliped now bears 8setae along the medial margin in groups of1-2- 2-3 progressing distally.

The third maxilliped and thoracic append ageshave increased in size, curving under towardthe thor ax.

Th e exopodites of the uropods (Fig. 33)now bear 5 or 6 setae of unequal length ; thethird seta is very long. More larvae had 5 than6 setae, a few had 5 on one side and 6 on theother. The endopodite now varies in size froma small to prominent bud approx imately 1/3the length of the exopodite.

ZOEA VI (Fig. 6) : N ow the first antenna(Fig. 16) usually has 4 subterminal tiers ofaesthetes in groups of 2- 3-4-4 or 2-2-4-4progressing distally. Of 19 specimens 5 hadonly 3 tiers in groups of 2-3-4 or 2-4-4.

The flagellum of the second antenna (Fi g.22) has increased greatly in length and nowdwarfs the spines on the protopodite. In speci­mens close to molting to megalopa, the seg­mentation of postlarval peduncle and flagellumcan be seen beneath the cuticle.

The scaphognathite of the second maxilla

Larval Development of Emerita rathblmae- K NIGHT 67

15/41312"16

/7 18 19 20 21

22

25

26

24

23

0. 1mm

0 .1mm~

14 -16, 20 -22, 27

0 .1 mmf--------I

/1-13,17-19, 24 -26

23

27

FIGS. 1I -27. Emerita ratbbunae, 11-16, First antenna, zoea I-VI ; 17-22, second antenna, zoea I-VI;23, mandible, zoea I ; 24-25, first maxilla, zoea I and II ; 26- 27, second maxilla, zoea I and VI.

68

(Fi g. 27) has 43-55 plumose setae along theouter margin .

The exopodites of the first and second maxil­lipeds now bear 14 plum ose natatory setae.

The th ird maxill iped and thor acic legs (Fi g.30) have increased greatly in size ; the fifth leg,curved up and behind the first four, is slightlybifid at the tip .

Now each of the segments 2, 3, 4, and 5 ofthe abdomen bears a pair of unir amous, un­segmented pleopods.

The exopodites of the uropods (Fig. 35)bear 7 or 8 setae of varying lengths ; twice asmany larvae had 7 as had 8 setae; a few hadboth 7 and 8 setae. The endopodit es are quitelong, usually 3/4 the length of the exopodites.

ALT ERN ATE ZOEAL STAGES: Of the larvae ofEmerita ratbbunae studied from preserved sam­ples, 49 had at least 14 setae on the exopoditesof the first and second maxillipeds. While 33of these larvae were in the described stage VI,with pleopods on abdominal somites, and were,in many cases, close to molting to megalopa,sixteen of the larvae seemed to have prolongedthe larval cycle to seven zoeal stages. Fivelarvae with 14 natatory setae on the maxillipedsdid not have pleopods on abdominal segments.They had only 6 setae on the exopodites of theuropods, 3 tiers of aesthetes on the first antenna,and in all other respects (measurements , de­velopment of appendages, etc.) were inter-

PACIFIC SCIENCE, Vol. XXI, January 1967

mediat e between the forms described as zoea Vand zoea VI. The remaining 11 larvae had 16setae on the exopodites of the maxill ipeds (onehad only 15) , had pleopods on abdominalsomites, and were slightly larger and moreadvanced than the form described as zoea VI.

Two zoea IV and two zoea V were foundwhich corresponded with the described stagesin over-all proportions and in setation . Theywere slightly smaller, however, and some ap­pendages were somewhat less developed (flagel­lum of second antenn a and thoracic legs) ,which suggests that they might be the earlystages of such an extended larval cycle.

The variation in development and setationof some appendages of cultured larvae with instage VI is summarized in Table 3.

ME GALOPA (F ig. 36) : The megalopa is color­less, slightly translucid and very much like theadult in form. The most noticeable differencesare presence of setose pleopods on abdominalsegments and relatively large eyes. The aver­age size of carapace in reared individuals was:length, 2.65 mm; width, 1.98 mm. No speci­mens from the plankton were available.

The first antenna ( Fig. 37) consists of a 3­segmented peduncle and a flagellum . The sec­ond and third segments of the peduncle havesmall ventral processes armed with setae andthat of the third segment is 2-segmented. Theflagellum usually consists of 10 segments armed

TABLE 3

COMPARISON OF SOME FEATURES OF CULTURED LARVAE IN STAGE VIFROM SERIES WITH 7, 8, AND 9 ZOEAL STAGES

HATCHED LARVAE PLANKTONIC LARVA

FEATURE 7 STAGES 8 STAG ES 9 STAGES 8 STAGES

First antenna : range 2 1-2 1-2N o . of subtermi na l majorit y 2 2 1 and 2 3tiers of aesthe tes

Second an tenna : rudiment toDevelopment of flagellum range spines = spi nes 0 to ru dimentin relat ion to spines on majority spi nes = ~ sp ines 0 sp inesprotopodite

First an d second range 13- 14 11-14 12-14maxillipeds: m ajority 14 13 and 14 12 an d 13 14

N atatory se tae

Urop ods : Exopod setae r ange 6-7 5-7 5-7maj or ity 6 6 6 6 and 7

Larval De velopment of Em erita l'athbtmae-KNIGHT 69

c

33

b

e

30

a

d

32

C-...

29

31

28

0.1 mmf--I

3 1- 3 3

0 .1 mm

28- 2 9, 34

I mm

3 0 ,35

L

34 35

FIGs. 28-35 . Emerita ratbbunae, 28, Second maxill iped , zoea I ; 29, first maxill iped, zoea I; 30a, thirdmaxill iped, b-], thoracic legs 1- 5, zoea VI ; 31-33, uropod, zoea III-V ; 34-35, telson, zoea I and VI.

70 PACIFIC SCIENCE, Vol. XXI , January 1967

1 mm

36

0.1 mm1---1

37 -38,41

0 .1 mmI

39-40

39

36

37

38

40 4/

FIGS. 36-41. Emerita ratbbunae, Megalopa. 36, Dorsal ; 37, first antenna ; 38, second antenna; 39, man­dible ; 40, first maxilla ; 41, second maxilla.

Larval Development of Emerita rathbunae- K NIGHT 71

laterally and ventrally with strong setae. Thedistal 5 segments bear aesthetes between theventral setae.

The basal segments of the second antenna(Fig. 38) are similar to those of the adult.The flagellum consists of 23-25 segments eachbearing 7 processes: 2 long plumose filteringsetae, 2 strong setae armed with comblikespines, and 3 shorter unarmed setae.

The mandible (Fig. 39) consists of a lightgnathal lobe and a palp of 2 segments. Thefirst segment of the palp has 3, rarely 2, stoutsetae on the lateral margin, and the terminalsegment bears setae along the medial and ante­rior margins.

The basal endite of the first maxilla (Fig.40) is armed with short, stout teeth and numer­ous setae ; 1 long plumose seta is conspicuouson the anterior-outer corner. On the coxal en­dite, a series of long setae curve sharply downtoward the mouth region. The endopod is un­segmented and saclike. There is 1 long seta onthe lateral angle of the protopodite below theendopodite.

The scaphognathite of the second maxilla(Fig. 41) has a dense fringe of approximately95 setae along the outer margin . Th e coxalendite is now bilobed; the small distal lobebears 1 long seta. The proximal lobe and thebasal endite bear many setae. The small tri­angular endoped is unarmed.

The anterior port ion of the protopodite ofthe first maxiIliped (Fig. 42) is produced intoa flat blade armed with rows of small setae anda series of long plumose setae on the basal por­tion. Th e exopodite consists of 2 segments ; thebladelike terminal segment is fringed withplumose setae. The rudimentary endopod isunarmed.

Th e exopodite of the second maxilliped (Fig.43) is 2-segmented; the first segment bears3-4 strong setae on the lateral margin and thesmall oval terminal segment is fr inged withplumose setae. The endopodite consists of 4segments with setation as figured.

Th e meropodites of the third maxilliped(Fig. 44) are broad and opercular. The 3 slen­der terminal segments bear plumose and bristlesetae ; the inner surfaces are covered with denserows of setae to form a brushlike structure.

The pereiopods are like those of the adult

in form, with the first three pairs directed for­ward and the fourth pair directed posteriorly.The fifth legs, slender and chelate, are curvedup beneath the carapace.

The abdomen now consists of 6 segments;segments 2, 3, 4, and 5 bear biramous pleopodsand segment 6 carries biramous uropods. Thepleopods (Fig. 45) decrease in length posteri­orly. Th e exopodites bear plumose setae; thefirst pair has 14-15 setae, the second pair bears15-16 setae, and the third and fourth pairshave 17-18 setae. The knoblike endopoditesincrease in length from the first to the fourthpair and have tiny median hooks which inter­lock with those of the opposite pleopod to forma single swimming unit of the pair.

The oval exopodites and endopodites of theuropods ( Fig. 46) are fringed with plumoseand small unarmed setae. The triangular telson(Fig. 46) has plumose setae along the lateralmargins.

Comparison of Species

Among larvae of Emerita analoga studiedfrom preserved plankton samples, the earlystages, I-IV (the "low stage IV" described byJohnson and Lewis ( 1942 :79) with usually10 , occasionally 9 or 11, setae on the first andsecond maxillipeds) , were found to be consis­tent in detail and degree of development, butlater stages showed such variation in setationand development of appendages that the num­ber of molts through which any individual hadprogressed could not be ascertained with con­fidence. Th e terminal zoeas, with indicationsof postlarval appendages beneath the cuticle,were consistent in possession of pleopods, anextremely long flagellum on the second antenna,and 5 tiers of subterminal aesthetes on the firstantenna, as described by Johnson and Lewis.From 16-19 setae were found on the exopoditesof the maxillipeds. Groupings of the late stagelarvae by size and relative growth of appen­dages suggested that there were at least 7 zoealinstars in the planktonic larval life of thespecies.

No differences in morphological detail weredetected between larvae of Em erita rathbunaeand E. analoga in stages I and II . In stage III,the uropods of E. analoga may bear 3 setae but7 out of 10 specimens examined had only 2

72 PACIFIC SCIENCE, Vol. XXI, Janu ary 1967

0 .5 mm

f----I46

0.5 mm

4 2 - 45 I

44

ba

4 5 46

FIGs. 42-46. Emerita ratbbunae. Megalopa. 42, First maxi llip ed ; 43, second maxilliped ; 44, third rnaxil­liped ; 45, pleopods (a, fourth, b, first) ; 46, uropods and telson .

setae as found in the equivalent stage of E.ratbbnnae. In stage IV, the setation of the ex­opodites of the uropods becomes consistent anda usefu l character for differentiati on of thespecies: larvae of E. analoga have 5 setae andthose of E. ratbbnnae have 4 setae on this ap­pendage. In all subsequent instars, the setationof the coxal endite of the first maxilla may be

used. The larvae of E. analoga develop a strongfifth seta subterminally on the proximal margin ,while larvae of E. ratbbunae apparently main­tain 4 setae throughout zoeal development.

Differences in terms of size of carapace, ratioof length of carapace to rostral spine, and pro­portions of the telson increase between larvaeof E. al1aloga and E. ratbbnnae as zoeal devel-

Larval Development of Em erita rathbmzae-K NIGHT 73

opment proceeds. The larvae of E. anologa be­come progressively larger than those of E.ratbbunae, and the carapace spines are consider­ably shorter in relation to the length of thecarapace. The posterior margin of the telson ofE. analoga larvae becomes increasingly pointedand triangular between the promi nent eighthmarginal spines, while that of E. ratbbunae re­mains smoothly rounded. Measurements of thefirst four stages and of the terminal stage oflarvae of E. analog a are given in T able 2 forcomparison with equivalent stages of E . ratb­bnnae, The carapace and telson of both speciesin stage IV are shown in Figures 7-10.

The larvae of Eme rita emerita, described byMenon (1 933) , and E. talpoida, described byRees ( 1959 ) and Smith (1 877) , and those ofE. rathbunae and E. analoga appear to be verysimilar in structure of appendages and in formof carapace and telson. The pattern of develop­ment may be common for all species throughstage III, and through stage IV (with specificvariation in setation ) for those species describedfrom the plankton. Larvae of E. emerita, and E.talp oida apparently pass direct ly from zoea IVto terminal zoea in the plankton. Those of E.talpoida in the laboratory and of E. ratbbtmaeand E. analoga in both laboratory and field havea variable series of intermediate instars be­tween stage IV and the terminal zoea in whichthere is progressive growth and setation with­out addition of appendages. Th e zoeal stageswhich appear to be common to all larvae of thegenus are as follows:

1. Uropods absent

a. Lateral spines on carapace absent,4 natatory setae onmaxillipeds .. . . . .. Stage I

b. Lateral spines on carapace present,6 natatory setae onmaxillipeds Stage II

2. Uropods present

a. Pleopods absent, 8 natatory setaeon maxiIIipeds . . . . Stage III

b. Pleopods absent, 10 natatory setaeon maxillipeds .. . . . . . . . . . . Stage IV

c. Pleopods present , 12 or morenatatory setae onmaxillipeds Terminal Stage

D istribution of Larvae

The locations of zooplankton samples exam­ined and the distr ibution of Em erita larvae aregiven in Figure 47. Larvae of E. analoga werefou nd in samples taken near Magdalena Bay,and those of E. ratbb nnae usually in samplestaken south and east of Cape San Lucas. Agroup of stage I larvae were found in near­shore samples from the west coast of BajaCalifornia below Magdalena Bay. From mea­surements, they appeared to be larvae of E.ratbb nnae, but lack of morph ological featureswith which to different iate stage I larvae of thetwo species makes identification tentative. Inaddition, 16 larvae of E. ratbb unae, rangin gfrom zoea II to terminal zoea VI, were foundjust south of Magdalena Bay. It seems likely,inasmuch as the range of developmental stageswas found in the sample, that the larvae werehatched locally and that pop ulations of the spe­cies might be found in the sandy beaches be­tween Cape San Lucas and Magdalena Bay.

Twenty larvae were foun d in samples takenin N ovember and December in the Gulf ofCalifornia, the majority north of La Paz, which,although slight ly smaller, were almost identicalwith those of the coastal E. analoga in morpho­logical detail and proportions. Onl y late stageswere obtained. These showed variation in seta­tion and development of appendages similar tothat found in larvae of E. analoga. During Au­gust to December, the movements of surfacewater along the western coast of Baja Californiaare pred ominantly offshore and westerly(Wyrtki , 1965). It therefore seems unl ikelythat the larvae could have been carried into theGulf from breeding populations near Magda­lena Bay. The appearance of the analoga-likelarvae in a series of samples suggests that eitherEm erita analoga or a closely related species maybe found in the warm temperat e zone of theGulf of Californ ia, extend ing north from AquaVerd e Bay on the west coast and Puerto SanCarlos on the east ( Gar th, 1955, 1960 ).

DISCU SSIO N

This study of planktonic and cultured larvaeof Em erita ratbbunae has shown that the num­ber of zoeal stages in the larval period is vari-

74 PACIFIC SCIENCE, Vol. XXI, January 1967

0 Emerita rath bunae

• 0 E . analaga

[:, ana laga- like larvae

a August - September

• N avember - December

o

I106

FIG. 47. Location of zooplankton samples examined and distr ibut ion of Emerita larvae.

l arval Development of Emerita rathbtmae- K NIGHT 75

able, both in nature and under conditions oflaboratory culture. In the laboratory, althoughthe larvae retained their specific proportionsand pattern of development, as many as threeintermediate instars could be added to the larvalsequences usually observed in specimens fromthe plankton. Variability between individualsat comparable stages of development increasedwith an increase in the number of zoeal moltsin the larval period.

A variable number of zoeal stages has beenfound in the laboratory culture of two otherspecies of Emerita. Dr . Ian Efford (pe rsonalcommunication) has noted 9-11 zoeal moltsamong reared larvae of E. analoga, and larvaeof E. talpoida cultured by Rees (1959) passedthrough 6 or 7 zoeal stages before the molt tomegalopa. Rees, using setation of the maxilli­peds as an indication of the stage of develop·ment, compared the zoeal stages observed inthe laboratory with those described by Smith( 1877) from the plankton and found thatlarvae from the plankton which molted to meg­alopa in the laboratory were apparently only instage V. Rees noted as well that "zoea fromnature possess features (appearance of thoraciclimb buds, pleopods, etc.) which show themto be farther advanced in development than thecorresponding laboratory stages." This relationbetween cultured and "natural" larvae was alsoobserved in the present study.

Some indication of seasonal variation in num­ber of zoeal stages was found in specimens ofE. ratbbunae examined from the plankton. Most(94 %) of the late-stage larvae taken in Augustand September appeared ready to molt to mega­lopa after six zceal stages; in the Decembersamples only 32% would metamorphose aftersix stages and 68% after seven stages.

Differences in setation and development ofappendages between individuals in comparableintermediate stages were not noted by Rees incultured larvae of E. talpoida and were rare inlarvae of E. ratbbunae from the plankton. In­dividual variation became more pronouncedamong reared larvae of E. ratbbnnae with anincrease in the number of zoeal stages, andmight be related to rate of development. larvaeof E. ratbbunae subjected at an early age to lowtemperatures (and perhaps other variables) ofthe laboratory environment had a larval span of

81-94 days. E. talpoida completed zoeal develop­ment in 23-33 days at 30° C. The molting fre­quency of the planktonic larva of E. ratbbunaecultured through two instars at 27°-30°C wasconsistent with that found by Rees for E. tal­poida, and it appears likely that E. ratbbunaewould have a much shorter larval life at thehigher temperatures in its natural environment.Perhaps culture of Emerita larvae over a rangeof controlled temperatures would show a rela­tion between duration and number of zoealstages and degree of individual variability. Theconsistent difference in size found between cul­tured and planktonic specimens suggests thatlarvae of this species are restricted in over-allsize by the conditions of laboratory culture.

Costlow ( 1965) has reviewed accounts inthe literature of variability within larvae ofCrustacea and has discussed effects of environ­mental factors (l ight , diet, temperature, salinity,etc.) on frequency and variability in molting,as well as current investigations of endocrinemechanisms related to molting in larvae ofbrachyuran decapods. Variation in number ofzoeal intermolts has been noted in the laboratoryculture of several anomuran decapods by Pro­venzano ( 1962a, b) for two species of paguridcrabs, and by Boyd and Johnson (1963) forthe galatheid, Pleuroncodes planipes, but ap­parently such variation is rare among brach­yurans. Gurney (1942) suggested that artificialrearing might give misleading results, andstated that, while stages I-III in the develop­ment of larval decapods seemed to be relativelyfixed, the natural course of development afterthat might be disturbed with addition of stagesnot found in nature. He noted as well that thereis no certainty that all stages observed in natureare passed through by all individuals of aspecies. The use of only laboratory-rearedmaterial to investigate the growth patterns of aspecies with such capacity for variability inlarval development as that shown by E. ratb­bnnae would indeed have been misleadingunless supplemented by a study of the larvaetaken from their natural environment.

ACKNOWLEDGME NTS

Th is work was supported by the Marine l ifeResearch Program, the Scripps Inst itution of

76

Oceano graphy's component of the CaliforniaCooperative Oceanic Fishe ries Investigations, aproject sponsored by the Marine Research Com­mittee of the State of California.

I would like to thank Dr. M. W. Johnson,Dr. E. W . Fager , Dr. J. A. McGowan, and Dr.W. A. N ewman for their valuable criticism ofthe manuscript.

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