- Email: [email protected]
Estuarine retention of larvae of the crab Rhithropanopeus harrisii
Estuarine,
Coastal and Shelf Science (1982) ~5, 207-220
Estuarine Retention of Larvae of the Crab Rhithropanopeus hamkii
Thomas W. Croniff Duke University Marine Laboratory, North Carolina 28516, U.S.A. Received IzJanuary
Beaufort,
1981 and in revised form 4 November 1981
Keywords: plankton distribution; crabs; estuarine organisms; North
population dynamics; Carolina coast
larval
stages;
Larvae of estuarine organisms continually face possible export from the parent estuary. Retention of larvae of the estuarine crab Rhithropanopeus hawisii was investigated in the upper Newport River estuary, North Carolina. All of the developmental stages occurred in the same area of the estuary with similar horizontal distributions, and the concentrations of intermediate and late stages were not greatly reduced from those of the first larval stage. This was strong evidence for the continuous retention of larvae in the upper estuary. To determine mechanisms by which retention might be effected, field studies of the vertical distributions and migrations of these larvae were made. The four zoeal stages had similar but complex vertical migration patterns, which varied from study to study. These migrations centered on the depth of no net flow, reducing longitudinal transport during development. Cross-spectral analysis of the larval migrations and the environmental cycles of light, salinity and current speed revealed that each of these external cycles affected larval depth. Megalopae of R. ha&ii also migrated vertically, but they were present in much lower concentrations than the zoeal stages, an indication of a change to benthic existence in this final larval form.
Introduction The net flow of water in estuaries is seaward due to the continual input of freshwater to an estuary from its drainage basin. As a result, estuarine planktonic organisms risk export into coastal waters. The problem is severe for the planktonic larvae of benthic estuarine invertebrates, for unless they can remain near the parent populations or move back into an estuary once exported, they may be transported to unfavorable habitats. Some estuarine species which are excellent swimmers as adults can return from coastal waters following metamorphosis, but populations of species with sessile or relatively immobile adults cannot persist unless larvae metamorphose near suitable adult habitats. Since crabs attach their developing eggs to their pleopods until hatching, larval activities alone determine whether retention or dispersal occurs. The crab Rhithropanopeus hawisii, which passes through four zoeal larval stages plus a megalopa (Connolly, rgq), is found only in estuaries (reviewed in Costlow et al., 1966). Its larvae probably remain near parent populations throughout development (Pinschmidt, 1963 ; Sandifer, 1973, 1975 ; Williams, ‘Present Address: Connecticut 06511,
Yale Department U.S.A.
of Biology,
P-0.
Box
6666,
New
Haven,
207 027277I4/82/080207+14
$03.00/O
@ 1982 Academic
Press Inc.
(London)
Liited
T. W. Cmnin
208
1971).Bousfield (1955)found that zoealarvae of R. hmrisii occurred near the depth of no net flow in the Miramichi estuary, thus enhancing their chancesfor retention. The meansby which this vertical distribution was maintained were not studied. Larval migrations between the water near the surface, which hasa net seawardflow, and the lower landward-moving layer would be effective in reducing export from many estuaries (Ketchum, Ig54), and could produce the vertical distributions observed by Bousfield (1955). However, vertical migrations of estuarinelarvae or even of the holoplankton of estuarieshave rarely been demonstrated (Bosch & Taylor, 1973 ; DeCoursey, 1976). The present study confirms that the larvae of R. harrisii remain within the estuary throughout development,and reveals the importance of larval vertical migrations for retention. Relating the behavioural physiology of the larvae to their vertical migrations suggestssome of the mechanisms controlling larval behavior in the field. Methods All field work was carried out in the Newport River estuary, near Beaufort, North Carolina (Figure I). Sampling and collection of hydrographic data were done in the Newport Narrows, where preliminary surveys located the greatest concentrations of larvae of Rhithropanqkus harrisii. To monitor the abundanceand horizontal distribution of R. harrisii larvae, plankton tows were made at approximately z-week intervals at eight stations spaced 1-2 km apart in the Newport Narrows (Figure I). Salinity and temperature were alsomeasuredat each station I SALE
012345
/
J\
/
NEWPORT -
.I;
3K
-
NARROWS
(\
I
.
-
-
“h
ATLANT/C OC I 76O45' Figure
I 76.40
I 76.3Y
J
1. The Newport River estuary, North Carolina. ( l ), locations of sampling the horizontal survey. (0), location of fixed station, study I. ( x), of fixed stations, studies z, 3 and 4.
stationsof location
L-AN
Retention of crab larvae
209
using a YSI model 23 Salinity-Conductivity-Temperature meter. All sampleswere taken at midday high tides (10.00-14.00 h, EST), using a r2.5-cm Clarke-Bumpus plankton sampler. Samplesfrom volumes of about 15001were taken just beneaththe surface and at a depth of 1-1.5 m, and were preserved in borate-buffered formalin. Complete sampleswere counted for each of the larval stagesof R. harrisii, unlesslarvae were extremely abundant (>500 larvae in a sample),in which caseat least four subsampleswere taken for a total of at least 200 larvae. On four occasions,when the results of the plankton tow seriesindicated that R. harrisii larvae were abundant in the Newport Narrows, a small trawler was employed as a fixed sampling station, occupied for 56-100 h (Figure I). At hourly intervals, the total depth was recorded, temperature and salinity were measuredat o-5-m depth intervals using a YSI S-C-T meter, currents were measured at 1.0 m depth intervals using a current drag (Pritchard & Burt, 1951), and downwelling light was measuredat o25-m depth intervals using a Kahl Scientific Instrument Corporation submersible radiometer. The spectral sensitivity of the radiometer was adjustedwith a Coming 4-72 filter to match the phototactic responsespectrum of R. harrisii larvae (Forward & Costlow, 1974). The instrument was calibrated at the larval responsepeak (500 nm) so that it actually measuredlarval units of luminance.The threshold intensity for phototaxis of R. harrisii larvae is known (IO-’ W m-s at 500 nm; Cronin, 1979); consequently, the depth of the phototactic threshold isolumecould be calculated from the data obtained by this radiometer. During study 4, measurementsof night-time irradiance in air from the direction of the zenith were made using an EG & G radiometer, which was alsofiltered and calibrated to measurelarval luminance units. Simultaneously with the physical measurements,successiveplankton sampleswere taken at four depths: just beneath the surface, I m, 2 m and just above the bottom (2.5-3.5 m). In study I only three depths were samplednear somelow tides, due to the shallow water column at this location. A gasoline-driven centrifugal pump was used, with the output filtered through a # 2 plankton net. The pumping time was 5 min per sample,providing a volume of 1210-12751. Sampleswere counted in the laboratory. For each hour, the average concentration of larvae in the water column wascalculatedby totalling the larvae collected in the four samplesand dividing by the total water volume pumped. In order to define statistically the associationsbetweenthe larval vertical distributions and the environmental cycles, multivariate spectral analyses(Fuller, 1976) were performed. Hourly depth-averaged meanswere calculated for the individual larval stagesand for the combined zoeal stages.The useof mean values to representhourly vertical distributions of larvae was reasonablebecausemost larvae were generally taken at a single depth, vertical profiles were smoothly reduced above and below this depth, and a secondmaximum rarely occurred. To remove the cyclic influence of tidal height on larval mean depth, and to have increasing values correspond to upward movements, mean depths were converted to normalized heights between o (bottom) and I (surface) by dividing by the depth of the bottom sampleof each hour and subtracting the quotient from I. In study I, the spectral analyseswere performed on the first 41 h of data, when larvae were present at all but 2 h. In study 4, no larvae were taken on 5 of the 74 samplehours. Since spectralanalysisrequires a completetime seriesof data, and sincea depth-averagedmeancould not be calculatedwhen no larvae were found, thesesevenmissingvalueswere replacedwith valuesmidway between those of each surrounding pair. Studies 2 and 3 were selectedfor portrayal of results in Figures 2, 3 and 5 since they illustrate most of the variation in results obtained, and sincemore larvae were taken in them than in studies I and 4.
210
T. W. Crottin
Results A brief description of the Narrows, derived from hydrographic data obtained during the presentstudy, will be provided here. The data upon which this general description is based can be obtained from the author. The lower Newport River estuary is a broad, shallow, generally well-mixed basin(average high-tide depth = 1.2 m; Hyle, 1976), but in the Narrows the estuary becomesa deeper, meanderingchannelsurrounded by salt marshand forest (Figure I). The Narrows is troughshaped,with a width of about 20 m and a depth of 3-5 m at meanhigh water. Approximately 10~ m3 of water moved through this channel with each ebb or flood of the tide, producing relatively rapid currents which varied with depth. Near the bottom, the flood currents were stronger and had a longer duration than ebb currents; while near the surface, ebb currents had the greater influence [e.g., seeFigures a(b), 3(b)]. Th e resulting net flow was an input of water near the bottom and an output of fresher water near the surface. The depth of no net flow was usually near the center of the water column.
-~-loo-'~d
'
E-50. . 22 0 E &p&PJyJ-j// t50
(b)’
. .P,’
-*
L+lcmEW 3 S-’
27 August
___.__
. .._
__. ..-.
28 August
29
(cl
August
Date (1977) Figure a. Results of study a, to show physical variables and larval vertical migrations. N = noon, M = midnight. (a) Salinity. -, surface salinity; - - - -, bottom salinity. (b) Currents. -, surface current; ---, bottom current. (c) Depth of the isolume representing the threshold luminance for larval phototaxis. - - - -, surface light readings below the measuring range of the submersible radiometer. (d) Mean depth of R. harrisii larvae, all zoeal stages combined.
Retention of crab larvae
211
During the seasonwhen larvae were available, the water temperatures in the Newport Narrows ranged from 20 to 32 “C. The daily temperature changewas2-5 “C, being generally lowest at high tide and near dawn. The water column was slightly stratified following high and low tides, the salinity difference between surfaceand bottom being I-@&, but it usually becamewell-mixed and vertically homogeneousat midtide [Figures 2(a), 3(a)]. The gradient of salinity along the length of Narrows was steep,falling from above 20%~ at the entrance at high tide to ox0 within IO km upstream. However, the salinity was strongly affected by weather; after periods of continuous rain it fell to near zero throughout the Narrows. Larval concentrationsof R. hzrrisii were high in the Narrows from mid-May to September whenever the salinity exceeded5x0 (Figure 4). The position of the maximum larval concentration was usually located within the Narrows, but the salinity at the larval maximum was variable. When the salinity was high, the larval maximum moved further upstream (Figure 4); but during periods of very low salinity, the larval concentration decreasedwith distance into the Narrows, implying that the larval maximum had moved seaward. The effect of weather on salinity and larval distributions wasapparent in the first fixed station study, when heavy rains fell for the first two nights. The salinity in the Narrows decreasedfrom an initial high of 28x,, to a constant ox, after the secondnight, and larval concentration concurrently fell from 301 mm3to 0.
h 30” 20. 10. 7 301 50O50. m-t S-l
I-
z-
3ST
l-
2-
34
7 July
9 July
8 July
KY July
II July
Date(1978) Figure
3. Results
of study
3. Symbols
as in Figure
z.
212
T. W. Cronin
Figure 4. Results of the horizontal sampling series. All values refer to surface samples. (a) Maximum larval concentration (log scale) on each date, all zoea larvae of R. harriri~ combined. (b) Location of the larval maximum, in km upstream from the entrance to the Narrows. (c) Salinity value at the location of the larval maximum.
At the fixed stations, larval concentrations generally changed in phase with the salinity cycle, though there was often a decrease at the time of the salinity peak (Figure 5). The second study was exceptional in that the concentration of the first zoeal stage roughly paralleled the salinity cycle, while the concentration profile of zoea IV was almost exactly one-half cycle out of phase with it; stages II and III had more complex time-concentration profiles. The total numbers of late-stage larvae collected in the fixed studies equalled 15--95% of stage I, implying that losses to export, predation, and other causes of mortality were relatively low, but few megalopae were collected (Table I). Since salinity decreases along the length of the Newport estuary from about 35x,, at the inlet to ox0 in the upper regions of the Narrows, the association between larval concentration and salinity is a measure of larval horizontal position in this estuary. In all fixed station studies, the larval concentration became maximal in intermediate salinities [Figure 6(a)]. All zoeal stages had similar salinity distributions except in study 2, where the first zoea had its maximum concentration in IO-20%~ salinity, but each successive stage peaked in a lower salinity range [Figure 6(b)]. The larval vertical migration patterns varied between studies, but in each case all zoeal stages migrated similarly, with simultaneous ascents and descents to very similar depths. Therefore, hourly depth-averaged means were calculated for the combined zoea larvae as well as for individual stages. Although marked vertical movements of the larvae were always observed, each study had distinctive features [see Figures z(d), 3(d) for examples]. The grand mean depths of the larval stages were obtained from the hourly means (Table 2). Each successive stage usually had a slightly greater average depth, and the fourth stage was deeper than the first for a significant number of hours in each of the studies 2, 3 and 4 (x2 test, P
Retention
14
of crab
larvae
M
N
213
M
N
M
N
M
mc’
N I
(a)
20IO-
(b)
IOx310l., ODolOl,’ O? lhte
(1978)
Figure 5. Results of study 3, 7-xr July 1978, illustrating changes in larval concentrations. N = noon, M = midnight. (a) Surface salinity. (b) Concentrations of zoeal stages I (-) and IV (- - - -) of R. harrisii (log scale). The results for stages I and IV generally represent the extremes for the zoeal stages. (c) Concentration of the megalopa of R. hmrisii (log scale).
TABLE I. Total numbers of larvae of each stage taken in each of the fixed station field studies. Percentages of stage I are given in parentheses. Study dates were (I) r-5 WY 1977; (2) 27-29 Ausust 1977; (3) 7-11 July 1978; and (4) 29 AugustI September 1978. The first three were near spring tides; the last near neap tides Total Field study I
2
Total
Zoea 5x75 15 266
3
43 500
4
9037 72 977
I
Zoea
II
5492
(106)
number
of larvae
Zoea
III
5.593
(108)
12 027
10 398
(79) 27 57.5 (63) 3670 (41) 48 764 (67)
24 771 (57) 2669 (30) 43 431 (W
(68)
taken Zoea 4923 (95) 4487 (29) zo 415 (47) 1375 (15) 31200 (43)
IV
Megalopa 209 (4-o) (0.: 2108
W3) (0~~
2486 (3’4)
214
T. W. Cvonin
the depth of no net flow in three studies and somewhat below it in the fourth (Table 2). Therefore, larval populations experienced either no net transport or actual upstream transport throughout each study. Cross-spectral analysis (Fuller, 1976; Platt & Denman, 1975) was used to examine the relationships between the transformed larval depth series (see Methods) and the estuarine cycles at the frequencies of the physical cycles. Analyses were performed on the combined zoeal data for all studies and on the data for individual larval stages when sufficient numbers of larvae of each stage were taken. The analytical results varied among studies, but larval
.,I.7
., ;;: .:.
;
.>‘. Ia , . ‘,.....
‘.
Study .;’ . ..‘. .. :
‘. :
2
‘.‘.: ‘. .,
;.
:
;.
I .
-d 2 3
Kxx)
Zoea I
(b)
loolo. 1. 01.‘.
. . ‘. ._ .: _. ..
.
.
. zoeam
: . -... .i . .. * ‘:. a:. -. . . .:. :’
.
..
. ’
.
Zoeo N
,.: n- . . .. . .. : : .: .,:
..
K)-
Zoeo II .. .;.. ‘. .,; ,:
-’
lOO0. lm-
.
.. . ..’ . . . . ..i . : . . . . .. . :. *... . f : ,,. . .
:
.::
. .. . : ,‘. :
l01
10
20
10
Salinity
Figure scales) samples. usually studies.
20
)
(%0)
6. Relationship of larval concentration of zoeal stages of R. harrisii (log and salinity at 2 m. Each point represents the results for a single hour’s The salinity value at a m was selected because the larval mean depths are near a m. (a) Results for the combined zoeal stages in the four fixed station (b) Results for the individual zoeal stages in study a, 27-29 August 1977.
Retention
of crab larvae
TABLB 2. Average flow was calculated
depths (m) of the larval by depth-interpolating
Zoeal Study
I
21.5
stages of R. hmrisii. The depth tidally time-averaged currents
stage
Depth of no net flow
II
III
IV
1’51
I .69 2.08
1'70
1.60
2.04 2.09
1.97
2’01
2’01
2.18
2.07
I'94
2.13
2.39
2.32
2.08
2'15
I'45
was no depth
of no net flow
I
1’52
2
I.94
3
1-72
1’4.5 1’99 I.99
4
2.03
2.31
Megalopa
Combined zoeal stages
of no net
“First two tidal cycles only. Following this time, due to massive input of rain water runoff.
there
(1.56)’
migrations were significantly associatedwith at least one of the three environmental cycles tested in every case(Table 3). Most frequently, the associationwas with the 6.2-h current flow cycle, representedby the absolute value of the bottom current. Here, the greatest larval ascentoccurred about 1.3 h after the maximum current speed, and all zoeal stageshad similar results (Table 3). The megalopalserieswhich was tested was not signticantly associatedwith the current cycle. For analysis,the 12.4-h salinity cycle wasrepresentedby the 2-m salinity value, sincethe overall larval meandepths were near 2-m (Table 2). The zoeal migrations were significantly related to this cycle only in study 2 (Table 3). During the first 2 days of study 3, the combined zoeal stagesand individual stages(except zoea 11) alsohad significant associationswith this cycle (Pco-OS, phase= $0.35 h), when the salinity structure resembledthat of study z (see Figures 2, 3). During the second2 days of study 3, the water column wasmore stratified and only zoea IV had a significant associationwith the salinity cycle. The megalopamigrated in associationwith this cycle throughout study 3. The depth of the phototactic threshold isolumewas usedto representthe 24-h die1cycle, since larval phototaxis cannot occur below it. This isolume was seldom deeper than 3 m [Figures 2(c), 3(c)], becauseof the rapid attenuation of light in the Newport Narrows by suspendeddebris and dissolved organic matter. While the lower part of the water column was rarely bright enough for larval phototaxis, near the surface there was always sufficient light for this behavior. During study 4, night-time readingsof light from a clear moonless sky gave values in air from 26 to 46 times the phototaxis threshold. Since lossat the surface during the day was about 50%, at night there would be enough light for phototaxis in the upper part of the water column. Only in study 4 did the combined zeal stagesmigrate in associationwith the light : dark cycle, although occasionalassociationsbetween individual stagesand this cycle were indicated in studies 2 and 3 (Table 3). In all of these cases,the minimum depth was reachedbetween twilight and midnight.
Discussion If larvae of a particular speciesare retained in a restricted area of an estuary, larvae should be abundant in the vicinity of the parent stocksbut rare near the estuary mouth, and intermediate and late stagesof larvae should occur in about the sameareasas the early stages. Further evidence for larval retention is provided if the concentrationsof later stagesare not greatly reduced from those of newly hatched larvae. These conditions are all observed for Rhithropampeus ha&ii larvae in the upper Newport River.
Combined study 2 Combined Zoea I Zoea II Zoea III Zoea IV shuiv 3 Combined Zoea I Zoea II Zoea III Zoea IV Megalopa S&Y 4 Combined
StudyI
Larval
stages
zoeal
represents intervals
b ‘Phase’ confidence
the
cycle
statistical
-
-1.13*0.43 -
--1.12*0.86
-1.71+0.62 -
- 1’3410.44
-1.23fO.31 -1.16ko.4g
(h)
ko.26
-x.20-&0.28
-1.3x+0.39
-r.r3
-11’45zto.77
Phase*
(6.2 h)
significance
level
ns
ns ns I-IS ns ns *
*** **
***
***
***
of the
(h)
squared
-
--I’53*0’95
-
-
coherency
+2.06 ho.28 + 1.78 +o.43 + 1.83 ho.59
+2.14*o.44
+ x.78 io.37
-
Phaseb
Significance’
Ix3
cycle (12.4 h)
Salinity
(ns,
not
significant;
*
ns
l *
ns ns ns ns
ns ns ns
ns *
ns
Significance” ___---
~.
-
-.
with
*, P
f1.42f2.67
(h)
f3.02
‘- 1.26fr.83 -
f6.71
Phase*
Die1 cycle (24 h)
the time delay or advance of the larval cycle relative to the environmental cycle, and is given (’ + ’ indicates that the larval cycle is advanced with respect to the environmental cycle).
represents
P
l **,
E ‘Significance’
P
ns
ns
ns * **
** *
** ** ** ** *
*
Significance”
stages
zoeal stages
zoeal
zoal stages
time series
Current
95%
**,
TABLE 3. Results of cross-spectral analyses of larval mean depth series and environmental series. Spectra were smoothed over three adjacent frequencies (for methods, see Fuller, 1976). The actual frequencies tested were not exactly those of the environmental cycles, since the method of analysis employed is useful only at harmonics of the length of the total time series. The frequency closest to that of the environmental cycle was the one tested in each case
Retention of crab lurerae
217
The larval concentration reached a maximum (often >IOOO individuals m-s; Figure 4) within the length of the Narrows at high tide on most days of horizontal sampling. Furthermore, all larval stagesusually occurred in the sameregion of the estuary. Sometimesthe later stageswere actually concentrated further up the estuary than the early ones [Figure 6(b)]. The horizontal distribution pattern was one of maximal abundance in low to medium salinities(5-24x,), but not a rigid associationof high larval concentrationswith a particular salinity (Figures 4, 6). Other work in the Newport River supports the conclusion that R. harrisii larvae do not normally move into the high salinity waters of the lower estuary. In Pinschmidt’s (1963) r-year survey of this estuary, most larvae of R. harrisii were taken near the entrance of the Narrows, in salinities of 8-28x,,. No larvae of this specieswere found at the inlet to the estuary, and the four zoeal stageshad similar salinity ranges. Extensive sampling by Dudley & Judy (1971) in coastalwaters adjacent to the Newport River inlet found no R. harrisii larvae, while other xanthid crab larvae were abundant. Other estuaries contain high concentrationsof R. harrisii larvae only in their upper regions(Bousfield, 1955 ; Tagatz, 1968; Sandifer, 1973, 1975). Such distributions parallel those of the adult crabs, which inhabit estuarine regions of o-5-25%,,salinity (reviewed in Costlow et al., 1966; Williams, 1965). In the Newport River, Pinschmidt (1963) collected them from oyster flats near the entrance to the Narrows. Adult crabs, including ovigerousfemales,have alsobeencollected in the lower 5 km of the Newport Narrows (R. Forward, personal communication), the samearea where the present study located high concentrations of larvae. The stage to stage decreasein concentration of zoea larvae of R. harrisii was moderate (Table I). Changesin relative concentration are not a direct measureof larval lossesto export, predation and mortality, since the later stagescollected developed from earlier populations of newly hatched larvae. Nevertheless,studies2-4 had similar trends. Also, the numbers of first-stage zoea larvae were stable from day to day (Figure 5) except in study I, when larvae were flushed out of the Narrows by freshwater runoff. This implied that larval releasewas rather constant over several days, further supporting the interpretation that stage-to-stagechangesin concentration indicate changesin the numbers of remaining larvae. The results agreewell with Pinschmidt’s (1963) data for this estuary (total zoea IV equalled 29.8% of zoea I) and with data Chamberlain (1962) obtained elsewhere(zoea IV = 36.4% of zoea I). Rapid larval development cannot account for the observed larval distributions in this estuary. The typical flushing time of the Newport River estuary is 62 days (Hyle, 1976), but larvae of R. hurrisii require some12 days for development at summertemperatures(Costlow & Bookhout, 1971). Similarly, it is difficult to imagine that larvae could be imported into such a dynamic system rapidly enough to causethe observed patterns, particularly sinceno stocks of adult crabs live near the estuary’s inlet. Larvae could maintain the observeddistributions by migrating into the water column from the substratum only when exposed to water of a particular salinity or tidal height, and sinking out at other times. This behavior explains the estuarine retention of oyster larvae (Wood & Hargis, 1971), but it is probably not employed by R. harrisii larvae. The salinity at the larval maximum was quite variable, and sometimesindividual larval stagesreachedpeak concentrationsin very different salinities [Figure 6(b)]. Such variations make it unlikely that these larvae enter the water column at a particular fixed salinity value. Brachyuran zoea larvae seembest adapted for a pelagic existence, and have not been reported in benthic samples.Under constant laboratory conditions, zoea larvae of this speciesremain planktonic for days (Cronin & Forward, 1979). Also, if zoea larvae migrate to and from the substrate
218
T. W. Cronin
with changing tidal state, they should ascendas larval numbers increaseand descendas numbers decrease.This was not observed(cf. Figures 3, 5). Some speciesof estuarine larvae are known to occupy successivelygreater depths as development proceeds.Such an ontogenetic migration accounted for the estuarine retention of barnacle larvae (Bousfield, 1955). A similar pattern has been described for larvae of R. harrisii and other crabs in the ChesapeakeBay (Sandifer, 1975). In contrast, laboratory experimentswith R. harrisii larvae from the Newport estuary found no downward movement during development (Cronin & Forward, 1979). The present study extends these results to the field; since later larval stageswere, on average, only slightly deeper than earlier ones (Table 2), the horizontal movementsof all larvae will be similar. The cyclical changesin vertical position of the zoea larvae best explain their restricted horizontal range in the Newport estuary. Since larvae were monitored at a fixed point in the moving estuarine flow, apparent vertical movements could arise both from vertical migrations of larval populations and from advection of stable but horizontally varying larval vertical distributions past the sampling station. However, tidally advected stable layers would produce a tidal cycle of vertical change,which seldomoccurred (Table 3). Even when such a cycle wasobserved, the vertical position curve wasdisplacedrelative to the tidal cycle (Figure 2, Table 3), so that when similar salinities(and thus water masses) were sampledon the flood and ebb, the larval vertical position was different. A stable vertical distribution would have produced a time seriessymmetrical about high or low tide, asdid the horizontal larval distributions (seeGagnon & Lacroix, 1981). I conclude that the observed changesin vertical position were mostly, if not entirely, due to larval vertical migrations. These migrations were most often affected by the alternating slack and flow of currents. Although barnacle larvae can become dynamically entrained in tidal currents (DeWolf, 1973), it is unlikely that R. harrisii larvae are similarly affected sincetheir changesin concentration follow tidal cycles, not current speedcycles (Figure 5). It is possiblethat turbulence in the water stimulates upward swimming, as proposed for clam larvae (Carriker, 1961). The lack of a current responsein study 4 would reflect the more stable water column conditions of neap tides. Responsesof planktonic organismsto turbulence have not been widely studied, and researcheffort in this areacould prove rewarding. The salinity cycle affected zoeal migration only when the vertical salinity structure alternated between conditions of moderate stratification at the tidal extremes and homogeneity at intermediate times. Phototaxis and geotaxis of R. ha&ii larvae are altered by salinity changesof only 1-2x, (Lam & Forward, 1977). Although the ratesof salinity change required for thesealterationsare unknown, during the times of mixing of previously stratified water, salinity values throughout the water column could well change rapidly enough to influence larval behavior. The larval movementsassociatedwith the tidal cycle could alsobe initiated by tidal variations in dissolvedorganics,turbidity or other water quality parameters. For example, zoea larvae of fiddler crabs (Ucu) had a tidal vertical migration in an estuary having negligible salinity variations (DeCoursey, 1976), so the larvae were evidently influenced by other tidally related features. Estuarine larvae should be responsiveto tidal and current fluctuations, which characterize their habitat. However, considering their strong phototactic behavior, the light : dark cycle had surprisingly little effect on them. Time seriesanalysispoorly resolvesperiods which are a large fraction of the total length of the data series, but the associationsbetween larval migrations and the die1cycle which were indicated in severalinstanceswere, at best, weak. Longer sampling programs would be needed to understand these 24-h migrations. The results here obtained suggestthat zoea larvae of R. ha&ii seldommove above the depth of
Retention of crab larvae
219
the threshold isolume[seeFigures 2(c), (d), 3(c), (d)], and thus are only occasionallyin water sufficiently well lit for phototaxis. Perception of dim light of natural underwater radiance distributions could lead to avoidancebehavior or to sinking, except when mixing events or other conditions mask or override these responses;this should be investigated under laboratory conditions. Since R. harrisi? larvae do not require light to find food (Cronin & Forward, 1980), remaining in darker waterswould allow them to feed while avoiding visually oriented predators. Thus, by migrating vertically, R. harrisii larvae can explore the water column, avoid visual predators, and maintain an average depth near the depth of no net flow. In somespeciesof crabs in which the zoea larvae are exported from estuaries,the megalopa could serve as a reinvasive stage(Tagatz, 1968; Christy, 1978). Zoeal retention makes such a role unnecessaryfor R. harrisii megalopae.The decreasein planktonic numbers of megalopaemight reflect a changein lifestyle. Megalopae seemadapted for benthic existence and probably spendlittle time in the water column. The hydrography of the Newport River estuary is sensitive to local weather, and larval behavior is not always sufficient to ensureretention. After a heavy rainfall, large amounts of freshwater are fed into the upper estuary, forcing larvae to enter the lower estuarineregions and even to be exported. Larvae of this specieshave been reported in coastal plankton samples(Nichols & Keney, 1963). Although R. harrisii larvae can be flushed out of the Newport estuary at such exceptional times, they appearadaptedfor retention during typical summer conditions. Acknowledgements This study would not have beenpossiblewithout the help of the staff of the Duke University Marine Laboratory. I particularly thank R. Forward for his continued aid and encouragement in all stagesof the project. The help of D. Stearns,M. Swift, P. Whaling and J. Dickens during the field studiesis gratefully acknowledged,while K. Doble and J. Beni assistedin counting samples. S. Wainwright, R. Barber, L. Buss, T. Goldsmith, L. Roth and R. Grossbergprovided useful commentson the manuscript. This material is basedon research supported by the National Science Foundation under grant no. OCE-77-26838; R. B. Forward, Jr., principal investigator. References Bosch, H. F. & Taylor, W. R. 1973 Diurnal vertical migration of an estuarine cladoceran, Podon polyphemoides, in the Chesapeake Bay. Marine Biology 19, 172-181. Bousfield, E. L. 1955 Ecological control of the occurrence of barnacles in the Miramichi estuary. Nation& Museum of Canada Bulletin No. 137, Biological Series No. 46. Carriker, M. R. 1961 Interrelation of functional mophology, behavior, and autecology in early stages of the bivalve Mercenuria mercenatia. Journal of the Elisha Mitchell Society 77, 168-241. Chamberlain, N. W. 1962 Ecological studies of the larval development of Rhithropanopeus hmkii (Xanthidae, Brachyura). Chesapeake Bay Institute Technical Report 28. Christy, J. H. 1978 Adaptive significance of reproductive cycles in the fiddler crab Uca pugilator: A hypothesis. Science 1~~453-455. Connolly, C. J. 1925 The larval stages and megalopa of Rhithropanopeus harrisii (Gould). Contributions to Canadian Biology 2, 329-334. Costlow, J. D., Jr. & Bookhout, C. G. 1971 The effect of cyclic temperature on larval development of the mud-crab Rhithropanopeus hawisii. In Fourth European Marine Biology Symposium (Crisp, D. J., ed.). Cambridge University Press, Cambridge. pp. 211-220. Costlow, J. D., Jr., Bookhout, C. G. & Monroe, R. J. 1966 Studies on the larval development of the crab, RhitJwopanopeus harrisii (Gould). I. The effect of salinity and temperature on larval development. Physiological Zoology39,81-100.
T.
220
W. Cromh
Cronin, T. W. 1979 Factors contributing to the retention of larvae of the crab Rhithropano~eus harrisii in the Newport River estuary, North Carolina. Ph.D. Thesis, Duke University. 206 pp. Cronin, T. W. & Forward, R. B., Jr. 1979 Tidal vertical migration: An endogenous rhythm in estuarine crab larvae. Science 205, 1020-1022. Cronin, T. W. & Forward, R. B., Jr. 1980 The effect of starvation on phototaxis and swimming by larvae of the crab Rhithropanopeus harrisii. Biological Bulletin x58,283-294. DeCoursey, P. J. 1976 Vertical migration of larval Uca in a shallow estuary. American Zoologist 15,244 (Abstract). DeWolf, P. 1973 Ecological observations on the mechanisms of dispersal of barnacle larvae during planktonic life and settling. NetherlandsJournal of Sea Research 6, 1-129. Dudley, D. L. & Judy, M. H. 1971 Occurrence of larval, juvenile, and mature crabs in the vicinity of the Beaufort Inlet, North Carolina. NOAA (U.S.), National Marine Fisheries Service, Special Scientifi Report Fisheries No. 637. Forward, R. B., Jr. & Costlow, J. D., Jr. 1974 The ontogeny of phototaxis by larvae of the crab Rhithropa?wpeus &ii. Marine Biology 26, 27-33. Fuller, W. A. 1976 Introduction to Statistical Time Series. John Wiley, New York. 470 pp. Gagnon, M. & Lacroix, G. 1981 Zooplankton sample variability in a tidal estuary: An interpretative model. Limnology and Oceanography 26,401~413. Hyle, R. A., II. 1976 Fishes of the Newport River estuary, North Carolina; their composition, seasonality and community structure. Ph.D. Thesis, University of North Carolina, Chapel Hill. 205 pp. Ketchum, B. H. 1954 Relation between circulation and planktonic populations in estuaries. Ewlogy 35, 191-200.
M. I. & Forward, R. B., Jr. 1977 The effect crustacean. Biological Bulletin 153, 163-179. Nichols, P. R. & Keney, P. M. 1963 Crab larvae M/V Theodore N. Gill, South Atlantic Coast and Wila’l$e Service, Special Scientific Report Pinschmidt, W. C., Jr. 1963 Distribution of crab in the Newport River estuary, North Carolina. Platt, T. & Denman, K. L. 1975 Spectral analysis La@
of salinity
upon
phototaxis
and geotaxis
in a larval
(Callinectes), in plankton collections from cruises of of the United States, 1953-1954. United States Fish Fisheries 448. larvae in relation to some environmental conditions Ph.D. Thesis, Duke University. I I 2 pp. in ecology. Annual Review of Ecology and Systematics
6,189-210.
Pritchard, D. W. & Burt, W. V. I 95 1 An inexpensive and rapid technique for obtaining current profiles in estuarine waters. Journal of Marine Research IO, 18~~89. Samlifer, P. A. 1973 Distribution and abundance of decapod crustacean larvae in the York River estuary and adjacent lower Chesapeake Bay, Virginia, 1968-1969. Chesapeake Science 14 235-237. Sandifer, P. A. 1975 The role of pelagic larvae in recruitment to populations of adult decapod CNStaceans in the York River estuary and adjacent lower Chesapeake Bay, Virginia. Estuarine and Coastal Marine Science 3,269-279. Tagatz, M. E. 1968 Biology of the blue crab Calfinectes sapiduc Rathbum in the St. John’s River, Florida. United States Fish and Wildlife Service Fishery Bulletin 57, 17-33. Williams, A. B. 1965 Marine decapod c~staceans of the Carolinas. United States Fish and Wildlife Service Fishery Bulletin 65, 1-298. Williams, A. B. 1971 A ten-year study of the meroplankton in North Carolina estuaries: Annual occurrence of some brachyuran developmental stages. Chesapeake Science 12,53-61. Wood, L. & Hargis, W. J. I971 Transport of bivalve larvae in a tidal estuary. In Fourth European Marine Biology Symposium (Crisp, D. J., ed.). Cambridge University Press, Cambridge, pp. 29-4.4.
Coastal and Shelf Science (1982) ~5, 207-220
Estuarine Retention of Larvae of the Crab Rhithropanopeus hamkii
Thomas W. Croniff Duke University Marine Laboratory, North Carolina 28516, U.S.A. Received IzJanuary
Beaufort,
1981 and in revised form 4 November 1981
Keywords: plankton distribution; crabs; estuarine organisms; North
population dynamics; Carolina coast
larval
stages;
Larvae of estuarine organisms continually face possible export from the parent estuary. Retention of larvae of the estuarine crab Rhithropanopeus hawisii was investigated in the upper Newport River estuary, North Carolina. All of the developmental stages occurred in the same area of the estuary with similar horizontal distributions, and the concentrations of intermediate and late stages were not greatly reduced from those of the first larval stage. This was strong evidence for the continuous retention of larvae in the upper estuary. To determine mechanisms by which retention might be effected, field studies of the vertical distributions and migrations of these larvae were made. The four zoeal stages had similar but complex vertical migration patterns, which varied from study to study. These migrations centered on the depth of no net flow, reducing longitudinal transport during development. Cross-spectral analysis of the larval migrations and the environmental cycles of light, salinity and current speed revealed that each of these external cycles affected larval depth. Megalopae of R. ha&ii also migrated vertically, but they were present in much lower concentrations than the zoeal stages, an indication of a change to benthic existence in this final larval form.
Introduction The net flow of water in estuaries is seaward due to the continual input of freshwater to an estuary from its drainage basin. As a result, estuarine planktonic organisms risk export into coastal waters. The problem is severe for the planktonic larvae of benthic estuarine invertebrates, for unless they can remain near the parent populations or move back into an estuary once exported, they may be transported to unfavorable habitats. Some estuarine species which are excellent swimmers as adults can return from coastal waters following metamorphosis, but populations of species with sessile or relatively immobile adults cannot persist unless larvae metamorphose near suitable adult habitats. Since crabs attach their developing eggs to their pleopods until hatching, larval activities alone determine whether retention or dispersal occurs. The crab Rhithropanopeus hawisii, which passes through four zoeal larval stages plus a megalopa (Connolly, rgq), is found only in estuaries (reviewed in Costlow et al., 1966). Its larvae probably remain near parent populations throughout development (Pinschmidt, 1963 ; Sandifer, 1973, 1975 ; Williams, ‘Present Address: Connecticut 06511,
Yale Department U.S.A.
of Biology,
P-0.
Box
6666,
New
Haven,
207 027277I4/82/080207+14
$03.00/O
@ 1982 Academic
Press Inc.
(London)
Liited
T. W. Cmnin
208
1971).Bousfield (1955)found that zoealarvae of R. hmrisii occurred near the depth of no net flow in the Miramichi estuary, thus enhancing their chancesfor retention. The meansby which this vertical distribution was maintained were not studied. Larval migrations between the water near the surface, which hasa net seawardflow, and the lower landward-moving layer would be effective in reducing export from many estuaries (Ketchum, Ig54), and could produce the vertical distributions observed by Bousfield (1955). However, vertical migrations of estuarinelarvae or even of the holoplankton of estuarieshave rarely been demonstrated (Bosch & Taylor, 1973 ; DeCoursey, 1976). The present study confirms that the larvae of R. harrisii remain within the estuary throughout development,and reveals the importance of larval vertical migrations for retention. Relating the behavioural physiology of the larvae to their vertical migrations suggestssome of the mechanisms controlling larval behavior in the field. Methods All field work was carried out in the Newport River estuary, near Beaufort, North Carolina (Figure I). Sampling and collection of hydrographic data were done in the Newport Narrows, where preliminary surveys located the greatest concentrations of larvae of Rhithropanqkus harrisii. To monitor the abundanceand horizontal distribution of R. harrisii larvae, plankton tows were made at approximately z-week intervals at eight stations spaced 1-2 km apart in the Newport Narrows (Figure I). Salinity and temperature were alsomeasuredat each station I SALE
012345
/
J\
/
NEWPORT -
.I;
3K
-
NARROWS
(\
I
.
-
-
“h
ATLANT/C OC I 76O45' Figure
I 76.40
I 76.3Y
J
1. The Newport River estuary, North Carolina. ( l ), locations of sampling the horizontal survey. (0), location of fixed station, study I. ( x), of fixed stations, studies z, 3 and 4.
stationsof location
L-AN
Retention of crab larvae
209
using a YSI model 23 Salinity-Conductivity-Temperature meter. All sampleswere taken at midday high tides (10.00-14.00 h, EST), using a r2.5-cm Clarke-Bumpus plankton sampler. Samplesfrom volumes of about 15001were taken just beneaththe surface and at a depth of 1-1.5 m, and were preserved in borate-buffered formalin. Complete sampleswere counted for each of the larval stagesof R. harrisii, unlesslarvae were extremely abundant (>500 larvae in a sample),in which caseat least four subsampleswere taken for a total of at least 200 larvae. On four occasions,when the results of the plankton tow seriesindicated that R. harrisii larvae were abundant in the Newport Narrows, a small trawler was employed as a fixed sampling station, occupied for 56-100 h (Figure I). At hourly intervals, the total depth was recorded, temperature and salinity were measuredat o-5-m depth intervals using a YSI S-C-T meter, currents were measured at 1.0 m depth intervals using a current drag (Pritchard & Burt, 1951), and downwelling light was measuredat o25-m depth intervals using a Kahl Scientific Instrument Corporation submersible radiometer. The spectral sensitivity of the radiometer was adjustedwith a Coming 4-72 filter to match the phototactic responsespectrum of R. harrisii larvae (Forward & Costlow, 1974). The instrument was calibrated at the larval responsepeak (500 nm) so that it actually measuredlarval units of luminance.The threshold intensity for phototaxis of R. harrisii larvae is known (IO-’ W m-s at 500 nm; Cronin, 1979); consequently, the depth of the phototactic threshold isolumecould be calculated from the data obtained by this radiometer. During study 4, measurementsof night-time irradiance in air from the direction of the zenith were made using an EG & G radiometer, which was alsofiltered and calibrated to measurelarval luminance units. Simultaneously with the physical measurements,successiveplankton sampleswere taken at four depths: just beneath the surface, I m, 2 m and just above the bottom (2.5-3.5 m). In study I only three depths were samplednear somelow tides, due to the shallow water column at this location. A gasoline-driven centrifugal pump was used, with the output filtered through a # 2 plankton net. The pumping time was 5 min per sample,providing a volume of 1210-12751. Sampleswere counted in the laboratory. For each hour, the average concentration of larvae in the water column wascalculatedby totalling the larvae collected in the four samplesand dividing by the total water volume pumped. In order to define statistically the associationsbetweenthe larval vertical distributions and the environmental cycles, multivariate spectral analyses(Fuller, 1976) were performed. Hourly depth-averaged meanswere calculated for the individual larval stagesand for the combined zoeal stages.The useof mean values to representhourly vertical distributions of larvae was reasonablebecausemost larvae were generally taken at a single depth, vertical profiles were smoothly reduced above and below this depth, and a secondmaximum rarely occurred. To remove the cyclic influence of tidal height on larval mean depth, and to have increasing values correspond to upward movements, mean depths were converted to normalized heights between o (bottom) and I (surface) by dividing by the depth of the bottom sampleof each hour and subtracting the quotient from I. In study I, the spectral analyseswere performed on the first 41 h of data, when larvae were present at all but 2 h. In study 4, no larvae were taken on 5 of the 74 samplehours. Since spectralanalysisrequires a completetime seriesof data, and sincea depth-averagedmeancould not be calculatedwhen no larvae were found, thesesevenmissingvalueswere replacedwith valuesmidway between those of each surrounding pair. Studies 2 and 3 were selectedfor portrayal of results in Figures 2, 3 and 5 since they illustrate most of the variation in results obtained, and sincemore larvae were taken in them than in studies I and 4.
210
T. W. Crottin
Results A brief description of the Narrows, derived from hydrographic data obtained during the presentstudy, will be provided here. The data upon which this general description is based can be obtained from the author. The lower Newport River estuary is a broad, shallow, generally well-mixed basin(average high-tide depth = 1.2 m; Hyle, 1976), but in the Narrows the estuary becomesa deeper, meanderingchannelsurrounded by salt marshand forest (Figure I). The Narrows is troughshaped,with a width of about 20 m and a depth of 3-5 m at meanhigh water. Approximately 10~ m3 of water moved through this channel with each ebb or flood of the tide, producing relatively rapid currents which varied with depth. Near the bottom, the flood currents were stronger and had a longer duration than ebb currents; while near the surface, ebb currents had the greater influence [e.g., seeFigures a(b), 3(b)]. Th e resulting net flow was an input of water near the bottom and an output of fresher water near the surface. The depth of no net flow was usually near the center of the water column.
-~-loo-'~d
'
E-50. . 22 0 E &p&PJyJ-j// t50
(b)’
. .P,’
-*
L+lcmEW 3 S-’
27 August
___.__
. .._
__. ..-.
28 August
29
(cl
August
Date (1977) Figure a. Results of study a, to show physical variables and larval vertical migrations. N = noon, M = midnight. (a) Salinity. -, surface salinity; - - - -, bottom salinity. (b) Currents. -, surface current; ---, bottom current. (c) Depth of the isolume representing the threshold luminance for larval phototaxis. - - - -, surface light readings below the measuring range of the submersible radiometer. (d) Mean depth of R. harrisii larvae, all zoeal stages combined.
Retention of crab larvae
211
During the seasonwhen larvae were available, the water temperatures in the Newport Narrows ranged from 20 to 32 “C. The daily temperature changewas2-5 “C, being generally lowest at high tide and near dawn. The water column was slightly stratified following high and low tides, the salinity difference between surfaceand bottom being I-@&, but it usually becamewell-mixed and vertically homogeneousat midtide [Figures 2(a), 3(a)]. The gradient of salinity along the length of Narrows was steep,falling from above 20%~ at the entrance at high tide to ox0 within IO km upstream. However, the salinity was strongly affected by weather; after periods of continuous rain it fell to near zero throughout the Narrows. Larval concentrationsof R. hzrrisii were high in the Narrows from mid-May to September whenever the salinity exceeded5x0 (Figure 4). The position of the maximum larval concentration was usually located within the Narrows, but the salinity at the larval maximum was variable. When the salinity was high, the larval maximum moved further upstream (Figure 4); but during periods of very low salinity, the larval concentration decreasedwith distance into the Narrows, implying that the larval maximum had moved seaward. The effect of weather on salinity and larval distributions wasapparent in the first fixed station study, when heavy rains fell for the first two nights. The salinity in the Narrows decreasedfrom an initial high of 28x,, to a constant ox, after the secondnight, and larval concentration concurrently fell from 301 mm3to 0.
h 30” 20. 10. 7 301 50O50. m-t S-l
I-
z-
3ST
l-
2-
34
7 July
9 July
8 July
KY July
II July
Date(1978) Figure
3. Results
of study
3. Symbols
as in Figure
z.
212
T. W. Cronin
Figure 4. Results of the horizontal sampling series. All values refer to surface samples. (a) Maximum larval concentration (log scale) on each date, all zoea larvae of R. harriri~ combined. (b) Location of the larval maximum, in km upstream from the entrance to the Narrows. (c) Salinity value at the location of the larval maximum.
At the fixed stations, larval concentrations generally changed in phase with the salinity cycle, though there was often a decrease at the time of the salinity peak (Figure 5). The second study was exceptional in that the concentration of the first zoeal stage roughly paralleled the salinity cycle, while the concentration profile of zoea IV was almost exactly one-half cycle out of phase with it; stages II and III had more complex time-concentration profiles. The total numbers of late-stage larvae collected in the fixed studies equalled 15--95% of stage I, implying that losses to export, predation, and other causes of mortality were relatively low, but few megalopae were collected (Table I). Since salinity decreases along the length of the Newport estuary from about 35x,, at the inlet to ox0 in the upper regions of the Narrows, the association between larval concentration and salinity is a measure of larval horizontal position in this estuary. In all fixed station studies, the larval concentration became maximal in intermediate salinities [Figure 6(a)]. All zoeal stages had similar salinity distributions except in study 2, where the first zoea had its maximum concentration in IO-20%~ salinity, but each successive stage peaked in a lower salinity range [Figure 6(b)]. The larval vertical migration patterns varied between studies, but in each case all zoeal stages migrated similarly, with simultaneous ascents and descents to very similar depths. Therefore, hourly depth-averaged means were calculated for the combined zoea larvae as well as for individual stages. Although marked vertical movements of the larvae were always observed, each study had distinctive features [see Figures z(d), 3(d) for examples]. The grand mean depths of the larval stages were obtained from the hourly means (Table 2). Each successive stage usually had a slightly greater average depth, and the fourth stage was deeper than the first for a significant number of hours in each of the studies 2, 3 and 4 (x2 test, P
Retention
14
of crab
larvae
M
N
213
M
N
M
N
M
mc’
N I
(a)
20IO-
(b)
IOx310l., ODolOl,’ O? lhte
(1978)
Figure 5. Results of study 3, 7-xr July 1978, illustrating changes in larval concentrations. N = noon, M = midnight. (a) Surface salinity. (b) Concentrations of zoeal stages I (-) and IV (- - - -) of R. harrisii (log scale). The results for stages I and IV generally represent the extremes for the zoeal stages. (c) Concentration of the megalopa of R. hmrisii (log scale).
TABLE I. Total numbers of larvae of each stage taken in each of the fixed station field studies. Percentages of stage I are given in parentheses. Study dates were (I) r-5 WY 1977; (2) 27-29 Ausust 1977; (3) 7-11 July 1978; and (4) 29 AugustI September 1978. The first three were near spring tides; the last near neap tides Total Field study I
2
Total
Zoea 5x75 15 266
3
43 500
4
9037 72 977
I
Zoea
II
5492
(106)
number
of larvae
Zoea
III
5.593
(108)
12 027
10 398
(79) 27 57.5 (63) 3670 (41) 48 764 (67)
24 771 (57) 2669 (30) 43 431 (W
(68)
taken Zoea 4923 (95) 4487 (29) zo 415 (47) 1375 (15) 31200 (43)
IV
Megalopa 209 (4-o) (0.: 2108
W3) (0~~
2486 (3’4)
214
T. W. Cvonin
the depth of no net flow in three studies and somewhat below it in the fourth (Table 2). Therefore, larval populations experienced either no net transport or actual upstream transport throughout each study. Cross-spectral analysis (Fuller, 1976; Platt & Denman, 1975) was used to examine the relationships between the transformed larval depth series (see Methods) and the estuarine cycles at the frequencies of the physical cycles. Analyses were performed on the combined zoeal data for all studies and on the data for individual larval stages when sufficient numbers of larvae of each stage were taken. The analytical results varied among studies, but larval
.,I.7
., ;;: .:.
;
.>‘. Ia , . ‘,.....
‘.
Study .;’ . ..‘. .. :
‘. :
2
‘.‘.: ‘. .,
;.
:
;.
I .
-d 2 3
Kxx)
Zoea I
(b)
loolo. 1. 01.‘.
. . ‘. ._ .: _. ..
.
.
. zoeam
: . -... .i . .. * ‘:. a:. -. . . .:. :’
.
..
. ’
.
Zoeo N
,.: n- . . .. . .. : : .: .,:
..
K)-
Zoeo II .. .;.. ‘. .,; ,:
-’
lOO0. lm-
.
.. . ..’ . . . . ..i . : . . . . .. . :. *... . f : ,,. . .
:
.::
. .. . : ,‘. :
l01
10
20
10
Salinity
Figure scales) samples. usually studies.
20
)
(%0)
6. Relationship of larval concentration of zoeal stages of R. harrisii (log and salinity at 2 m. Each point represents the results for a single hour’s The salinity value at a m was selected because the larval mean depths are near a m. (a) Results for the combined zoeal stages in the four fixed station (b) Results for the individual zoeal stages in study a, 27-29 August 1977.
Retention
of crab larvae
TABLB 2. Average flow was calculated
depths (m) of the larval by depth-interpolating
Zoeal Study
I
21.5
stages of R. hmrisii. The depth tidally time-averaged currents
stage
Depth of no net flow
II
III
IV
1’51
I .69 2.08
1'70
1.60
2.04 2.09
1.97
2’01
2’01
2.18
2.07
I'94
2.13
2.39
2.32
2.08
2'15
I'45
was no depth
of no net flow
I
1’52
2
I.94
3
1-72
1’4.5 1’99 I.99
4
2.03
2.31
Megalopa
Combined zoeal stages
of no net
“First two tidal cycles only. Following this time, due to massive input of rain water runoff.
there
(1.56)’
migrations were significantly associatedwith at least one of the three environmental cycles tested in every case(Table 3). Most frequently, the associationwas with the 6.2-h current flow cycle, representedby the absolute value of the bottom current. Here, the greatest larval ascentoccurred about 1.3 h after the maximum current speed, and all zoeal stageshad similar results (Table 3). The megalopalserieswhich was tested was not signticantly associatedwith the current cycle. For analysis,the 12.4-h salinity cycle wasrepresentedby the 2-m salinity value, sincethe overall larval meandepths were near 2-m (Table 2). The zoeal migrations were significantly related to this cycle only in study 2 (Table 3). During the first 2 days of study 3, the combined zoeal stagesand individual stages(except zoea 11) alsohad significant associationswith this cycle (Pco-OS, phase= $0.35 h), when the salinity structure resembledthat of study z (see Figures 2, 3). During the second2 days of study 3, the water column wasmore stratified and only zoea IV had a significant associationwith the salinity cycle. The megalopamigrated in associationwith this cycle throughout study 3. The depth of the phototactic threshold isolumewas usedto representthe 24-h die1cycle, since larval phototaxis cannot occur below it. This isolume was seldom deeper than 3 m [Figures 2(c), 3(c)], becauseof the rapid attenuation of light in the Newport Narrows by suspendeddebris and dissolved organic matter. While the lower part of the water column was rarely bright enough for larval phototaxis, near the surface there was always sufficient light for this behavior. During study 4, night-time readingsof light from a clear moonless sky gave values in air from 26 to 46 times the phototaxis threshold. Since lossat the surface during the day was about 50%, at night there would be enough light for phototaxis in the upper part of the water column. Only in study 4 did the combined zeal stagesmigrate in associationwith the light : dark cycle, although occasionalassociationsbetween individual stagesand this cycle were indicated in studies 2 and 3 (Table 3). In all of these cases,the minimum depth was reachedbetween twilight and midnight.
Discussion If larvae of a particular speciesare retained in a restricted area of an estuary, larvae should be abundant in the vicinity of the parent stocksbut rare near the estuary mouth, and intermediate and late stagesof larvae should occur in about the sameareasas the early stages. Further evidence for larval retention is provided if the concentrationsof later stagesare not greatly reduced from those of newly hatched larvae. These conditions are all observed for Rhithropampeus ha&ii larvae in the upper Newport River.
Combined study 2 Combined Zoea I Zoea II Zoea III Zoea IV shuiv 3 Combined Zoea I Zoea II Zoea III Zoea IV Megalopa S&Y 4 Combined
StudyI
Larval
stages
zoeal
represents intervals
b ‘Phase’ confidence
the
cycle
statistical
-
-1.13*0.43 -
--1.12*0.86
-1.71+0.62 -
- 1’3410.44
-1.23fO.31 -1.16ko.4g
(h)
ko.26
-x.20-&0.28
-1.3x+0.39
-r.r3
-11’45zto.77
Phase*
(6.2 h)
significance
level
ns
ns ns I-IS ns ns *
*** **
***
***
***
of the
(h)
squared
-
--I’53*0’95
-
-
coherency
+2.06 ho.28 + 1.78 +o.43 + 1.83 ho.59
+2.14*o.44
+ x.78 io.37
-
Phaseb
Significance’
Ix3
cycle (12.4 h)
Salinity
(ns,
not
significant;
*
ns
l *
ns ns ns ns
ns ns ns
ns *
ns
Significance” ___---
~.
-
-.
with
*, P
f1.42f2.67
(h)
f3.02
‘- 1.26fr.83 -
f6.71
Phase*
Die1 cycle (24 h)
the time delay or advance of the larval cycle relative to the environmental cycle, and is given (’ + ’ indicates that the larval cycle is advanced with respect to the environmental cycle).
represents
P
l **,
E ‘Significance’
P
ns
ns
ns * **
** *
** ** ** ** *
*
Significance”
stages
zoeal stages
zoeal
zoal stages
time series
Current
95%
**,
TABLE 3. Results of cross-spectral analyses of larval mean depth series and environmental series. Spectra were smoothed over three adjacent frequencies (for methods, see Fuller, 1976). The actual frequencies tested were not exactly those of the environmental cycles, since the method of analysis employed is useful only at harmonics of the length of the total time series. The frequency closest to that of the environmental cycle was the one tested in each case
Retention of crab lurerae
217
The larval concentration reached a maximum (often >IOOO individuals m-s; Figure 4) within the length of the Narrows at high tide on most days of horizontal sampling. Furthermore, all larval stagesusually occurred in the sameregion of the estuary. Sometimesthe later stageswere actually concentrated further up the estuary than the early ones [Figure 6(b)]. The horizontal distribution pattern was one of maximal abundance in low to medium salinities(5-24x,), but not a rigid associationof high larval concentrationswith a particular salinity (Figures 4, 6). Other work in the Newport River supports the conclusion that R. harrisii larvae do not normally move into the high salinity waters of the lower estuary. In Pinschmidt’s (1963) r-year survey of this estuary, most larvae of R. harrisii were taken near the entrance of the Narrows, in salinities of 8-28x,,. No larvae of this specieswere found at the inlet to the estuary, and the four zoeal stageshad similar salinity ranges. Extensive sampling by Dudley & Judy (1971) in coastalwaters adjacent to the Newport River inlet found no R. harrisii larvae, while other xanthid crab larvae were abundant. Other estuaries contain high concentrationsof R. harrisii larvae only in their upper regions(Bousfield, 1955 ; Tagatz, 1968; Sandifer, 1973, 1975). Such distributions parallel those of the adult crabs, which inhabit estuarine regions of o-5-25%,,salinity (reviewed in Costlow et al., 1966; Williams, 1965). In the Newport River, Pinschmidt (1963) collected them from oyster flats near the entrance to the Narrows. Adult crabs, including ovigerousfemales,have alsobeencollected in the lower 5 km of the Newport Narrows (R. Forward, personal communication), the samearea where the present study located high concentrations of larvae. The stage to stage decreasein concentration of zoea larvae of R. harrisii was moderate (Table I). Changesin relative concentration are not a direct measureof larval lossesto export, predation and mortality, since the later stagescollected developed from earlier populations of newly hatched larvae. Nevertheless,studies2-4 had similar trends. Also, the numbers of first-stage zoea larvae were stable from day to day (Figure 5) except in study I, when larvae were flushed out of the Narrows by freshwater runoff. This implied that larval releasewas rather constant over several days, further supporting the interpretation that stage-to-stagechangesin concentration indicate changesin the numbers of remaining larvae. The results agreewell with Pinschmidt’s (1963) data for this estuary (total zoea IV equalled 29.8% of zoea I) and with data Chamberlain (1962) obtained elsewhere(zoea IV = 36.4% of zoea I). Rapid larval development cannot account for the observed larval distributions in this estuary. The typical flushing time of the Newport River estuary is 62 days (Hyle, 1976), but larvae of R. hurrisii require some12 days for development at summertemperatures(Costlow & Bookhout, 1971). Similarly, it is difficult to imagine that larvae could be imported into such a dynamic system rapidly enough to causethe observed patterns, particularly sinceno stocks of adult crabs live near the estuary’s inlet. Larvae could maintain the observeddistributions by migrating into the water column from the substratum only when exposed to water of a particular salinity or tidal height, and sinking out at other times. This behavior explains the estuarine retention of oyster larvae (Wood & Hargis, 1971), but it is probably not employed by R. harrisii larvae. The salinity at the larval maximum was quite variable, and sometimesindividual larval stagesreachedpeak concentrationsin very different salinities [Figure 6(b)]. Such variations make it unlikely that these larvae enter the water column at a particular fixed salinity value. Brachyuran zoea larvae seembest adapted for a pelagic existence, and have not been reported in benthic samples.Under constant laboratory conditions, zoea larvae of this speciesremain planktonic for days (Cronin & Forward, 1979). Also, if zoea larvae migrate to and from the substrate
218
T. W. Cronin
with changing tidal state, they should ascendas larval numbers increaseand descendas numbers decrease.This was not observed(cf. Figures 3, 5). Some speciesof estuarine larvae are known to occupy successivelygreater depths as development proceeds.Such an ontogenetic migration accounted for the estuarine retention of barnacle larvae (Bousfield, 1955). A similar pattern has been described for larvae of R. harrisii and other crabs in the ChesapeakeBay (Sandifer, 1975). In contrast, laboratory experimentswith R. harrisii larvae from the Newport estuary found no downward movement during development (Cronin & Forward, 1979). The present study extends these results to the field; since later larval stageswere, on average, only slightly deeper than earlier ones (Table 2), the horizontal movementsof all larvae will be similar. The cyclical changesin vertical position of the zoea larvae best explain their restricted horizontal range in the Newport estuary. Since larvae were monitored at a fixed point in the moving estuarine flow, apparent vertical movements could arise both from vertical migrations of larval populations and from advection of stable but horizontally varying larval vertical distributions past the sampling station. However, tidally advected stable layers would produce a tidal cycle of vertical change,which seldomoccurred (Table 3). Even when such a cycle wasobserved, the vertical position curve wasdisplacedrelative to the tidal cycle (Figure 2, Table 3), so that when similar salinities(and thus water masses) were sampledon the flood and ebb, the larval vertical position was different. A stable vertical distribution would have produced a time seriessymmetrical about high or low tide, asdid the horizontal larval distributions (seeGagnon & Lacroix, 1981). I conclude that the observed changesin vertical position were mostly, if not entirely, due to larval vertical migrations. These migrations were most often affected by the alternating slack and flow of currents. Although barnacle larvae can become dynamically entrained in tidal currents (DeWolf, 1973), it is unlikely that R. harrisii larvae are similarly affected sincetheir changesin concentration follow tidal cycles, not current speedcycles (Figure 5). It is possiblethat turbulence in the water stimulates upward swimming, as proposed for clam larvae (Carriker, 1961). The lack of a current responsein study 4 would reflect the more stable water column conditions of neap tides. Responsesof planktonic organismsto turbulence have not been widely studied, and researcheffort in this areacould prove rewarding. The salinity cycle affected zoeal migration only when the vertical salinity structure alternated between conditions of moderate stratification at the tidal extremes and homogeneity at intermediate times. Phototaxis and geotaxis of R. ha&ii larvae are altered by salinity changesof only 1-2x, (Lam & Forward, 1977). Although the ratesof salinity change required for thesealterationsare unknown, during the times of mixing of previously stratified water, salinity values throughout the water column could well change rapidly enough to influence larval behavior. The larval movementsassociatedwith the tidal cycle could alsobe initiated by tidal variations in dissolvedorganics,turbidity or other water quality parameters. For example, zoea larvae of fiddler crabs (Ucu) had a tidal vertical migration in an estuary having negligible salinity variations (DeCoursey, 1976), so the larvae were evidently influenced by other tidally related features. Estuarine larvae should be responsiveto tidal and current fluctuations, which characterize their habitat. However, considering their strong phototactic behavior, the light : dark cycle had surprisingly little effect on them. Time seriesanalysispoorly resolvesperiods which are a large fraction of the total length of the data series, but the associationsbetween larval migrations and the die1cycle which were indicated in severalinstanceswere, at best, weak. Longer sampling programs would be needed to understand these 24-h migrations. The results here obtained suggestthat zoea larvae of R. ha&ii seldommove above the depth of
Retention of crab larvae
219
the threshold isolume[seeFigures 2(c), (d), 3(c), (d)], and thus are only occasionallyin water sufficiently well lit for phototaxis. Perception of dim light of natural underwater radiance distributions could lead to avoidancebehavior or to sinking, except when mixing events or other conditions mask or override these responses;this should be investigated under laboratory conditions. Since R. harrisi? larvae do not require light to find food (Cronin & Forward, 1980), remaining in darker waterswould allow them to feed while avoiding visually oriented predators. Thus, by migrating vertically, R. harrisii larvae can explore the water column, avoid visual predators, and maintain an average depth near the depth of no net flow. In somespeciesof crabs in which the zoea larvae are exported from estuaries,the megalopa could serve as a reinvasive stage(Tagatz, 1968; Christy, 1978). Zoeal retention makes such a role unnecessaryfor R. harrisii megalopae.The decreasein planktonic numbers of megalopaemight reflect a changein lifestyle. Megalopae seemadapted for benthic existence and probably spendlittle time in the water column. The hydrography of the Newport River estuary is sensitive to local weather, and larval behavior is not always sufficient to ensureretention. After a heavy rainfall, large amounts of freshwater are fed into the upper estuary, forcing larvae to enter the lower estuarineregions and even to be exported. Larvae of this specieshave been reported in coastal plankton samples(Nichols & Keney, 1963). Although R. harrisii larvae can be flushed out of the Newport estuary at such exceptional times, they appearadaptedfor retention during typical summer conditions. Acknowledgements This study would not have beenpossiblewithout the help of the staff of the Duke University Marine Laboratory. I particularly thank R. Forward for his continued aid and encouragement in all stagesof the project. The help of D. Stearns,M. Swift, P. Whaling and J. Dickens during the field studiesis gratefully acknowledged,while K. Doble and J. Beni assistedin counting samples. S. Wainwright, R. Barber, L. Buss, T. Goldsmith, L. Roth and R. Grossbergprovided useful commentson the manuscript. This material is basedon research supported by the National Science Foundation under grant no. OCE-77-26838; R. B. Forward, Jr., principal investigator. References Bosch, H. F. & Taylor, W. R. 1973 Diurnal vertical migration of an estuarine cladoceran, Podon polyphemoides, in the Chesapeake Bay. Marine Biology 19, 172-181. Bousfield, E. L. 1955 Ecological control of the occurrence of barnacles in the Miramichi estuary. Nation& Museum of Canada Bulletin No. 137, Biological Series No. 46. Carriker, M. R. 1961 Interrelation of functional mophology, behavior, and autecology in early stages of the bivalve Mercenuria mercenatia. Journal of the Elisha Mitchell Society 77, 168-241. Chamberlain, N. W. 1962 Ecological studies of the larval development of Rhithropanopeus hmkii (Xanthidae, Brachyura). Chesapeake Bay Institute Technical Report 28. Christy, J. H. 1978 Adaptive significance of reproductive cycles in the fiddler crab Uca pugilator: A hypothesis. Science 1~~453-455. Connolly, C. J. 1925 The larval stages and megalopa of Rhithropanopeus harrisii (Gould). Contributions to Canadian Biology 2, 329-334. Costlow, J. D., Jr. & Bookhout, C. G. 1971 The effect of cyclic temperature on larval development of the mud-crab Rhithropanopeus hawisii. In Fourth European Marine Biology Symposium (Crisp, D. J., ed.). Cambridge University Press, Cambridge. pp. 211-220. Costlow, J. D., Jr., Bookhout, C. G. & Monroe, R. J. 1966 Studies on the larval development of the crab, RhitJwopanopeus harrisii (Gould). I. The effect of salinity and temperature on larval development. Physiological Zoology39,81-100.
T.
220
W. Cromh
Cronin, T. W. 1979 Factors contributing to the retention of larvae of the crab Rhithropano~eus harrisii in the Newport River estuary, North Carolina. Ph.D. Thesis, Duke University. 206 pp. Cronin, T. W. & Forward, R. B., Jr. 1979 Tidal vertical migration: An endogenous rhythm in estuarine crab larvae. Science 205, 1020-1022. Cronin, T. W. & Forward, R. B., Jr. 1980 The effect of starvation on phototaxis and swimming by larvae of the crab Rhithropanopeus harrisii. Biological Bulletin x58,283-294. DeCoursey, P. J. 1976 Vertical migration of larval Uca in a shallow estuary. American Zoologist 15,244 (Abstract). DeWolf, P. 1973 Ecological observations on the mechanisms of dispersal of barnacle larvae during planktonic life and settling. NetherlandsJournal of Sea Research 6, 1-129. Dudley, D. L. & Judy, M. H. 1971 Occurrence of larval, juvenile, and mature crabs in the vicinity of the Beaufort Inlet, North Carolina. NOAA (U.S.), National Marine Fisheries Service, Special Scientifi Report Fisheries No. 637. Forward, R. B., Jr. & Costlow, J. D., Jr. 1974 The ontogeny of phototaxis by larvae of the crab Rhithropa?wpeus &ii. Marine Biology 26, 27-33. Fuller, W. A. 1976 Introduction to Statistical Time Series. John Wiley, New York. 470 pp. Gagnon, M. & Lacroix, G. 1981 Zooplankton sample variability in a tidal estuary: An interpretative model. Limnology and Oceanography 26,401~413. Hyle, R. A., II. 1976 Fishes of the Newport River estuary, North Carolina; their composition, seasonality and community structure. Ph.D. Thesis, University of North Carolina, Chapel Hill. 205 pp. Ketchum, B. H. 1954 Relation between circulation and planktonic populations in estuaries. Ewlogy 35, 191-200.
M. I. & Forward, R. B., Jr. 1977 The effect crustacean. Biological Bulletin 153, 163-179. Nichols, P. R. & Keney, P. M. 1963 Crab larvae M/V Theodore N. Gill, South Atlantic Coast and Wila’l$e Service, Special Scientific Report Pinschmidt, W. C., Jr. 1963 Distribution of crab in the Newport River estuary, North Carolina. Platt, T. & Denman, K. L. 1975 Spectral analysis La@
of salinity
upon
phototaxis
and geotaxis
in a larval
(Callinectes), in plankton collections from cruises of of the United States, 1953-1954. United States Fish Fisheries 448. larvae in relation to some environmental conditions Ph.D. Thesis, Duke University. I I 2 pp. in ecology. Annual Review of Ecology and Systematics
6,189-210.
Pritchard, D. W. & Burt, W. V. I 95 1 An inexpensive and rapid technique for obtaining current profiles in estuarine waters. Journal of Marine Research IO, 18~~89. Samlifer, P. A. 1973 Distribution and abundance of decapod crustacean larvae in the York River estuary and adjacent lower Chesapeake Bay, Virginia, 1968-1969. Chesapeake Science 14 235-237. Sandifer, P. A. 1975 The role of pelagic larvae in recruitment to populations of adult decapod CNStaceans in the York River estuary and adjacent lower Chesapeake Bay, Virginia. Estuarine and Coastal Marine Science 3,269-279. Tagatz, M. E. 1968 Biology of the blue crab Calfinectes sapiduc Rathbum in the St. John’s River, Florida. United States Fish and Wildlife Service Fishery Bulletin 57, 17-33. Williams, A. B. 1965 Marine decapod c~staceans of the Carolinas. United States Fish and Wildlife Service Fishery Bulletin 65, 1-298. Williams, A. B. 1971 A ten-year study of the meroplankton in North Carolina estuaries: Annual occurrence of some brachyuran developmental stages. Chesapeake Science 12,53-61. Wood, L. & Hargis, W. J. I971 Transport of bivalve larvae in a tidal estuary. In Fourth European Marine Biology Symposium (Crisp, D. J., ed.). Cambridge University Press, Cambridge, pp. 29-4.4.