Distribution, population dynamics and estimates of production for the estuarine mysid, Rhopalophthalmus terranatalis

Distribution, population dynamics and estimates of production for the estuarine mysid, Rhopalophthalmus terranatalis

Estuarine, Coastal and Shelf Science (1986) 23,205-223 Distribution, Population Estimates of Production Mysid, Rhopalophthalmus Dynamics and for...

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Estuarine,

Coastal

and Shelf

Science

(1986) 23,205-223

Distribution, Population Estimates of Production Mysid, Rhopalophthalmus

Dynamics and for the Estuarine terranatalis

T. H. Wooldridge Department of Zoology, University Port Elizabeth 6000, South Africa Received

16 May

Keywords:

1985 and in revised

of Port form

Elizabeth,

P.O.

24 September

Box

1600,

1985

mysid; secondaryproduction; estuaries

The biology of the mysid shrimp Rhopalophthalmus terranatalis is described from a warm temperateestuaryin southernAfrica. Intensive quantitative field samplingcontinued over 21 monthswhile laboratory culture provided detailed information for production estimates.Three generationsareproducedannually and individual femalesproducemultiple broods.The overwintering generation hasa lifespanof 9-10 months and is characterizedby low population density, but individuals are relatively large with femalesproducing large broods.The summergenerationsurvives for 6 months. Population density is high (maximum may exceed4000m- 3 of water) but individuals attain a.smallersizeand producefewer progeny. The spring generationhascharacteristicswhich may generally be describedas intermediate between the other two generations. Daily production valuesof 2.69, 6.93 and 13.97mgmm3were calculatedfor the overwintering, spring and summergenerations,respectively. Daily P/B coefficientsvaried between0.020and 0.026. The P/B ratio for the overwintering generationwas5.86; for the spring generation,3.06 and for the summer generation4.74. The annual P/B ratio for the whole population was 7.85. Comparativevaluesusinga secondmethodof populationproduction are provided. The biology of R. terranatalis allowsfor rapid recovery of the population in a regionwherecatastrophicaperiodicfresh-waterflooding occurs. Introduction

The euryhaline mysid shrimp Rhopalophthalmus terranatalis is endemic to southern Africa. Although reported from many localities, data are mostly non-quantitative and only fragmentary details on the biology of the speciesare known. Sampling strategies in the past have also underestimated the general abundance of this large mysid. Recent studies in the Sundays River estuary (Wooldridge 8z Bailey, 1982) have shown it to be the principal mysid present, particularly during the summer when concentrations may exceed 4000 individuals m-3 of water. Together with Mesopodopsis slabberi, R. terranatalis in this estuary contributed substantially to zooplankton standing stock. Their combined contribution when sampled monthly over twenty-one months was rarely less than 700,$of the total and in most months exceeded 9O”/b of total standing stock. Mysids were also major components of the plankton in adjacent coastal waters 205 0272-7714/86/080205

+ 19 $03.00/O

0 1986 Academic

Press Inc. (London)

Limited

206

T. H. Wooldridge

3 km

SUNDAYS

RIVER ESTUARY

Figure 1. Map of Sundays River estuary indicating the location of sampling sites.

around the margins of Algoa Bay (Wooldridge, 1983). In these inshore waters M. slubberi was the principal species with maximum recorded concentrations exceeding 15 000 individuals m - 3. In both the estuary and bay, mysids contributed significantly to the diets of fishes (Wooldridge & Bailey, 1982; Lasiak, 1983; McLachlan, 1983). Biologists have previously focussed little attention on mysids asprey organisms, although the significance of their role in shallow waters is becoming increasingly more evident. For the Indian Ocean region, Mauchline (1980) lists only the work of Whitfield & Blaber (1978). More recently, Blaber (1979) discussedthe significance of Mesopodopsisufricana in the food web of Lake St Lucia, while the role of Gustrosuccuspsummodytes has been quantified for open sandy beaches(McLachlan et al., 1981). In the Sundays a co-ordinated multi-disciplinary research effort is underway to investigate processeswithin the estuary and includes trophic interactions. Considering the abundance and prominence of R. terrunutulis, it is suggestedthat this mysid plays a significant role in the estuarine food web. The present investigation reports on the biology of R. terrunutalis and includes estimates of production. Much of the work was carried out on live animals in the laboratory and complements information derived from field studies. A general description of the estuary aswell as details on the zooplankton are given in a previous publication (Wooldridge & Bailey, 1982). Field sampling and analysis of preserved material Between August 1979 (late winter) and April 1981 (autumn), monthly samples were taken at ten stations in the estuary (Figure 1). Collections were made from just below the

Estuarine mysidRhopalophthalmus terranatalis

207

water surface and between midwater and the substrate at each of the deeper stations (1-7) using two WP2 nets (57 cm diameter and 200 urn mesh) towed simultaneously. Sampling was done at night and all sampleswere quantitative. At these stations depth varied between 2 and 6 metres. Above station 7 the estuary was shallow ( < 2 m depth) and only near-surface sampleswere taken. Mysid abundance was calculated using 3-5 subsamplesin each case. Animals were examined under a stereo microscope; measured (anterior tip of carapace to posterior tip of telson, excluding spines) and classified into one of seven classes.These categories relate to body size, sex and in the caseof brooding females, to larval development stage. Details are given in Wooldridge & Bailey (1982). To calculate mysid standing stock (mg dry massmw3) it was necessaryto establish the relationship between body massand length by oven-drying 50-60 individuals of known length for 24 h at 60 “C. Mysids were then individually weighed on a Sartorius microbalance. Since the number of embryos produced by parent females in positively correlated with body size, brood contribution to total parent masswas calculated separately after establishing the massof an individual larva by weighing 30 oven-dried broods. The relationship between the number of embryos and parent size was derived for each generation once generation times were established. Brood size of a female of a particular mass and representing the overwintering generation could then be statistically compared with brood size of a female of the samemassrepresenting a later generation. Similarly, female size and fecundity from different parts of the estuary could be compared within each generation to determine whether these parameters were statistically different between regions of the estuary. In all casesbrood size was determined for females with rounded embryos and hence newly extruded into the pouch. Mysid standing stock (mg me3) was derived by converting length of all individuals in sub-samples to weight by means of the length-weight relationship. Results for individuals were raised to a value which was representative for the whole sample. The data pertaining to brood massof brooding femaleswere included. Laboratory

culture of mysids and data analysis

Details on the life history of R. terranatalis such as growth, lifespan, number of broods produced by an individual, brood development time and interval between broods were carried out in the laboratory. Mysids collected in the estuary were transported in 20-litre plastic containers and maintained for 24 h in aerated water in a temperature-controlled room set at field water temperature. Water used in experiments was also collected from specific points in the estuary where salinity corresponded to 14,21,28 and 35%. These salinities spanned the recorded range of R. terranatalis (Wooldridge & Bailey, 1982). Two brooding females bearing embryos at an advanced stage of development (eyed larvae) were introduced with two adult malesinto each of eight 15-litre rectangular glass tanks. Tank water corresponded to a specific salinity previously mentioned, sothat studies at each salinity were carried out in duplicate. Water was renewed every two weeks. Temperature and photoperiod in the environmental room were regularly adjusted according to ambient conditions. Temperature was raised by approximately 2 “C per month from 14 “C in mid-winter (Jun-Jul) through to 26 “C in Jan-Feb (Wooldridge & Bailey, 1982). This allowed for comparison of laboratory and field data. Additional experiments were carried out on batches of mysids periodically collected and introduced at specific stagesof their lifespan into tanks. Supplementary details, derived in this way,

208

T. H. Wooldridge

included age or massat which females extruded their first brood, the number of broods produced by individuals of a specific generation aswell asinformation on the fate of early summer broods (growth during a period of increasing temperature) compared to broods releasedin late summer or autumn when temperatures were decreasing. Diet was an important consideration in laboratory experiments and was based on previous work (Wooldridge & Bailey, 1982) which indicated the omnivorous habit of R. terranatalis. During the summer months phytoplankton blooms were present in the estuary, so that experimental water collected from the field contained concentrations of these cells. Additional live phytoplankton food was provided by Dunaliella salina and Thalassiosira weisflogii cultured in the laboratory and fed thrice-weekly. Commercially available ProNutro vitamin-enriched cereal and Tetra Min fish flakes were finely ground and also presented. Species of estuarine copepods which were introduced as nauplii in water samplesalso provided a source of nutrition. Pseudodiaptomus hessei and Acartia longipatella are naturally preyed upon by R. terranatalis (Wooldridge & Bailey, 1982) and these flourished in laboratory tanks, providing mysids with a source of natural live prey. In addition, commercially available brine shrimp eggs(Artemia salina) were added to the tank water every 4-5 days. Following the emergency of juveniles from the parent brood pouch, growth and development were followed by removing individuals bi-monthly and measuring total length. After brood release, femalesinvariably extruded a further batch of eggs. Interval between broods as well as the number of broods produced per individual could be established. These data were integrated with information from supplementary tank experiments and from field collections. The mortality rate during the time-span of a generation was low; the longest surviving individuals attained an age of 9 months during the duration of the experiments. In this casemortality was due to a mechanical fault in the temperature regulator, but in most instances was due to physical damage during handling. Results Population

distribution

and abundance

Spatial and temporal abundance of different classesof R. terranatalis are given for consecutive regions in Figure 2. Station 1 represents the mouth, stations 2-3 the lower estuary, 4-7 the middle estuary and the remaining stations, the upper estuary. Although data represent homogeneousdistribution in the water column, maximum abundance was nearly always present below mid-water level (Wooldridge & Bailey, 1982). On occasions vertical differences in abundance varied by two orders of magnitude between the surface and near-bottom. This is in contrast to Mesopodopsis slabberi which was usually more abundant nearer the surface at the time of sampling. R. terranatalis does not undergo a general migration into surface waters irrespective of the state of the tide and/or light intensity (Wooldridge & Erasmus, 1980). Spatially, R. terranatalis occurred in greatest numbers in the middle and lower estuary where salinity varied between 15 and 30%0.In the upper regions (stations 8-10 and < 2 m in depth), salinity was generally below 10%0. Here R. terranatalis was present in low numbers only (Figure 2) and consequently this area is excluded from further discussion. Temporal changes are evident. Sampling commenced in August 1979 (late winter) after river-flooding when numbers did not exceed lOme anywhere in the estuary. Abundance increased from October onwards and attained a maximum in March 1980

Estuarirze mysid Rhopalophthalmus

terranatalis

209

20 20 60 Stations

1oc

2 - 3

60 20 20 60 100

300 500 100

60 20 20 60 100

400 800 Stations

100

6 - 7

60 20 20 60 100 400 ,

,

,

,

,

I

I

,

,

)

,

,

, , Stations

,

,

,

, 8 -

10

(

I,

20 I1 I I ASONDJFMAMJJASONDJFMA

cl Adult

n

cP

I

I

,

(

Brooding P

Figure 2. Spatial and temporal regions animals

,

of the Sundays below the line

estuary.

abundance Adults

,

,

,

Immature dB

,

,

/TJ Juveniles P

of Rhopalophthalmus terranatalis in different are shown above the line, sexually inactive

210

T. H. Wooldridge

(summer) at stations 2-3 (mean of the four sampleswas 1171mm3). Highest density in a single sample was 4100 rnd3 near the bottom at station 2. On the sameoccasion abundance near the surface was 500m- 3 (Wooldridge & Bailey, 1982). Numbers declined during the winter (Apr-Aug 1980) with population density not exceeding 65 animals mm3in any region. The pattern in the following spring and summer was similar to that recorded during the corresponding period in the previous year, with maximum density in the middle estuary (1125 m- 3 at stations 4-5 in January and 1504m- 3 in February at stations 6-7). Highest abundance at a single station was 3500 mm3in the bottom sample at station 7 (surface 50 me3). Body size, ageand growth Rhopalophthalmus terranatalis was reproductively active during most months of the year. Analysis of empirical and laboratory growth data indicated that three overlapping generations are produced annually. Individual females also produce multiple broods. These basic strategies are summarized in Figure 3 which also represents a framework for the following detailed discussion. A cessationof egg releaseand hence recruitment into the population during the colder months (May-Aug, Figure 2) is reflected in size-class distribution in late winter. Animals are then mostly adults and are referred to as the overwintering generation. Females ranged from 15.0 mm to 20.5 mm total length, the smallestrepresenting the last brood of the previous summer generation. Larger mysids represent earlier broods of the samegeneration. Males attain a smaller size than females and ranged between 14.5 mm and 18.5 mm in length. Brooding females brought into the laboratory in late summer (April) release young which represent the overwintering generation. Since experimental temperatures follow ambient and reproduction ceasesin winter, it is possible to compare growth directly between field and laboratory animals during this period as well as between broods produced in early spring. Such a comparison gives an indication of the reliability of laboratory data. Growth rates in different salinities in the laboratory showed no sequential variation, consequently data from all tanks during the time-span of a generation were pooled. Mysids released from the brood pouch in April were 140 days old in August. Females had a mean length of 17.3mm and males 16.0mm (see Figure 5). They therefore fall within the size range of animals collected in August in the estuary. Embryo-bearing femalesappear in the estuary in late August, their brood size showing a linear relationship to body length (Figure 4). These overwintering mysids are large and consequently produce large broods (Table 1). The population is composedof individuals from all broods of the previous summer generation (the youngest brood was about 140 days old) and accounts for the higher mean length of 18.2 mm (females only) compared to experimental animals which represent a specific age class with a mean length of 17.3 mm. The first brood of overwintering generation animals are released after 28-29 days incubation. Females moult and extrude a further batch of eggs, usually within 24 h of releasing the previous brood. Since growth continues after attainment of sexual maturity, fecundity of any female increases progressively. Up to five broods are produced, the development time of each decreasing as summer temperatures increase. Consequently the fifth brood is releasedby about mid-November after remaining in the pouch for about 21 days. Individuals of the overwintering generation then begin to die off, giving a life span of 9-10 months.

APr

C_ -

Figure

June

days

months

by

representation

July

Jan-Feb

December

intervals

in early

at

8 Immature

10

out

3. Diagrammatic

Juvemles

May

cycle

Life

3 140

Q-

span=

Life

produced

dies

brood

Fifth

produced days

Gene:ation

broods 30-21

Five

mid-August

GENERATION

numbers of large fecundity

commences

Relatively low individuals-high

Breeding

OVERWINTERING

Aug



21brood

cycle

Ott

by

Breeding

days

months

out

NO-J

spring

- early Feb

Adults

Jan

intervals

end

end

at

November

cycle for overwintermg,

180

dies

produced

produced days

end

GENERATION commences

Sept

span=5-6

of the annual

Life

Life

Generation

Fifth

Five

broods 14

SPRING

Breeding

2

Dee

Over-winter, mid-Aug

GENERATION

at intervals by early mid-May

generation

-b

Broods

R. terranaraks.

Feb

commence breeding after=140 days

- 7 months 65 days this generation

produced dies out

produced

in

produced

March

April

commences mid - February high numbere of smaller lower fecundity

Jan

Life span=6 Life cycle= Progeny of

Fifth brood Generation

Five broods 14-21days

and summer

Feb

SUMMER

Breeding Relatively individuals-

3

T. H. Wooldridge

212

24 ).-A

22

q l -

OVERWINTERING -

-

0 SPRING

-0

SUMMER

A

GENERATION .

GENERATION

. *

.

GENERATION

* .

.

2c

/

IE

IE

q oo*r( k! z s 0

A

a

14

1;

ii IC

8

6

4

2 I

I

1

I

13

14

15

16

BODY

LENGTH

t

17

I

1

18

19

2.0

(mm)

Figure 4. Relationship between body length (mm) and brood size (newly extruded eggs) for the three generations of R. rerranatalis. For statistical treatment of data, see Table 1. There was no significant difference for slope and elevation (analysis of covariance) between animals in different regions of the estuary, consequently data are given for the middle regions where population density was greatest. Statistical treatment of data comparing parent size and brood size between generations is discussed in the text.

By mid-November the first spring generation brood matures (Figure 3), individuals being about 80 days old (Figure 5). Females have attained a body length of 15.0mm while males are smaller with a length of 14.0 mm. Five broods are produced by the spring generation, the young emerging from the pouch after 21 days at the time of the first brood. Incubation time also decreasesprogressively to 14 days after the fifth brood due to increasing water temperatures. Brood size is given in Figure 4 and Table 1. The last

Esruarine

Rhopalophthalmus

mysid

213

terranatalis

TABLE 1. Comparison of brood size and body length for terranaralis. Brood size of a standard animal of 18.Ornm generation also shown. Data from middle estuary region

Generation

Relationship Y=a+bx

three total

generations of R. length from each

Mean body length (mm) of sample animals

Mean brood size (mm) of sample animals

Brood size of standard animal 18.0 mm length

Overwintering

a= - 13.1316 b= 1.6435 r= 0.714 N=66

18.2

16.7

16.5

Spring

a = - 16.2797 b= 1.7125 r=0%31 N= 142

16.9

12.7

14.5

Summer

a= - 12.1370 b= 1.3303 r=0.831 N= 126

15.5

8.4

11.8

18-

OVERWINTERING

6-

SPRING SPRING

3

1

SUMMER SUMMER

c

30

I

60

I

90

I

I

120

150

AGE

GENERATION ---

GENERATION GENERATION GENERATION GENERATION

I

180

-------

I

210

240

270

-

300

(days)

Figure 5. Growth curves (mm) for male and female R. terranatalis representing the overwintering, spring and the summer generations (vertical bars represent + 1 SD).

214

T. H. Wooldridfe

brood is produced by the end of January after which the parent generation begins to die off, giving them a lifespan of 5-6 months. Progeny of the spring generation attain sexual maturity after 65 days and are referred to as the summer generation. Females are 13-3 mm and males 125 mm body length (Figure 5). These 3rd-generation mysids attain sexual maturity at a smaller size than individuals of previous generations, reflected in Figure 4. Breeding of summer generation animals commencesin early February when water temperatures peak at 25-26 “C. This results in a development time of 14 days for the first brood. Five broods are ultimately produced, the relationship between brood and parent size shown in Figure 4 and Table 1. During March water temperatures begin to decreaseresulting in a concomitant increase in brood development time. The last brood emergesin mid-April. In addition to statistical treatment of data (length vs brood size) from the lower and middle estuary within generations, it was necessary to compare body length and brood size between generations. Treatment by analysis of covariance of overwintering and summer generation data showed that the slopesof the two regression lines differed significantly and that egg production was lower in summer (P
Estimates of production were calculated using two methods. The first followed the graphical technique (2nd variant) described by Winberg (197 1) and was applied to each generation to give estimates of daily production. Production for a generation as well as annual production using a weighted mean of the three daily production estimates could also be computed. The following parameters representing each generation were required: 1. Construction of an individual growth curve-change in massover time. 2. Construction of an absolute growth increment curve-daily growth increment at different stagesof development. 3. The size frequency of the population which reflects cumulatively the abundance me3 of different cohorts. The duration of each cohort corresponds to the time interval between the upper and lower limits in mg of that cohort.

Estuarine mysid Rhopalophthalmus

terranatalis

215

Male and female growth curves for each generation are shown in Figure 5. The ratio of males to females throughout the year in field samples deviated little from 1 : 1 so that differences in rate of growth are plotted as averaged values. Length data were transformed into mass, described by log,, mass (mg)=2.81 log L (mm)-2.69752, where L = length; r = 0.99, p < 0.005 and n = 61. Individual growth rates in mg averaged for the sexesare shown in Figure 6. Incorporated into each graph are cumulative values of all eggs extruded after each brood. Data also reflect increasing fecundity with increasing body size obtained from Figure 4. Thus for the overwintering generation [Figure 6(a)], the mass of an individual female and all eggs produced up to the fifth brood in 17000x 10m3mg. The daily growth increment for an individual from each generation [curve 1 in Figure 7(a), (b) and (c)] was constructed from Figure 6 and includes all sexual products released into the pouch. Change in body massduring any given interval divided by the number of days during that interval reflects the daily growth rate which was plotted at the mid-interval point. Also shown in Figure 7 is the abundance m -3 day-’ for three life stages(juveniles, immature and adults-curve 2 for each generation). Data are basedon field observations of population densities (Figure 2). Although generations overlap, it was necessary to designate specific months to particular age classes.For example, overwintering juveniles and immatures were present in the estuary in April, May and June (seeFigure 3). All samplescollected during these months (surface and near-bottom at all stations in both years of study) were pooled and the average number m - 3 for each of these classescalculated. The abundance for each stagewas plotted opposite the Y-intercept (left hand side of Figure 7) and the maximum massof an individual of each classalong the abscissa.All adults present in the estuary in July through November were treated as overwintering animals. Other generations were treated in a similar manner, the respective months shown in Figure 3. For example, the overwintering generation was represented by 56 juveniles, 23 immatures and 11 adults me3 of water in any part of the estuary. The total of 79 individuals was plotted opposite the maximum body mass attained by adults (9000 mg x 10e3). The range in body massfor overwintering generation juveniles included all individuals up to 0.96 mg dry body mass,immatures from 0.97 and up to 3.68 mg and adults between 3.69 and 8.83 mg. Corresponding values for spring generation animals were 0.96 mg, 0.97-3.68 mg and 3.69-7.87 mg. For the summer generation values were 0.96 mg, 0.97-2.85 mg and 2.86-7.30 mg. The third curve (curve 3 in Figure 7) represents cumulative egg production plotted after eachbrood; for example, after the third brood the massof the parent plus total massof three broods (12 000 mg x lo- 3 from Figure 6) was plotted opposite the point on curve 2 which corresponds to the massof the parent at the time of producing the third brood. Daily production can now be calculated. For any chosen weight class, e.g. O-500 mg x lo-” of the overwintering generation (Table 2), the number of individuals (29 from curve 2 Figure 7) x the mean individual growth increment for that weight class (curve 1 in Figure 7, Table 2), gives daily production for that weight class.Total daily production for each generation is obtained by the summation of the products for all categories (Table 2). The product of total daily production and lifespan in days for each generation gives generation production, shown in Table 3. Standing stock was calculated from curve 2 in Figure 7 and is described by the product of mysid abundance and the corresponding mean massof that class. For example, in the

216

T. H. Wooldridge

m

&OL x 6lJJ SSQVU Aaoa

Estuarine mysid Rhopalophthalmus

terranatalis

217

OVERWINTERING

0 ‘0

I

0’

2000

4000

6000 BODY

6000

10000

MASS

12000

1400016000

m g X 1O-3 -260

76 SPRING

:

-220 -200

x E”

54

-180

;

E u) tc w z

46

-160

:

-140

F

-120

,” -

zj

30

66 60 :

:

-240

72

GENERATION

42 36

24 18 12 6 2000

4000 BODY

320)

6000

6000

MASS

m9

10000 x

12000

1C3

C)

60

1000

3000 BODY

Figure 7. The daily growth

5000 MASS

7000 mg x

? 3

so<

1O-3

increment (curve l), the size frequency 2) and the contribution of egg production to total body mass (curve (a), spring (b) and summer (c) generation I?. terrantalis.

distribution (curve 3) of overwintering

218

T. H. Wooldridge

TABLE 2. Estimates (Ov), spring (Spr) for each generation

of daily production for different and summer (Sum) generations is given in Table 3

Size of weight class in each generation (no. m-s)

Mean individual daily growth increment 1O-3 mg per weight class in each generation

ov.

Spr

Sum

Ov

Spr

Sum

0- 500 500- 1000 lOOO- 2000 2000- 4000 20003500 20003000 4000- 6000 35o(r 5500 3000- 4000 6000-17000 5500- 8500 4000- 6000 850&l 2850 6000- 9400

29 17 15 10

20 4 5

134 36 38

15.75 33.25 37.75 43.50

16.25 35.50 44.25

17.50 39xlO 49.00

Total

79

Weight (10-s

class mg)

3

weight classes of the overwintering of R. tetranatalis. Total production

Daily

production 1O-3 mg m-s per weight class in each generation

ov

Spr

Sum

456.75 565.25 566.25 435.00

325.00 142.00 221.25

2345.00 1404.00 1862.00

61.50 28

4

184.50 66.00

1848.00

73.50 7

294.00 798.00

114.00 104.00

14 4

1456.00 371.00

92.75 13

1852.50

142.50 20

112.00

30

2240.00

115.00 32

82

3450.00 88.00

2816.00 2688.25

302

6973.25

13971.00

3. Standing stock and estimates of production for Rhopalophthalmus terranatalis. Data include daily production and P/B estimates, and production and P/B estimates for each of the three generations, and annual production and the P/B coefficient for the whole population

TABLE

Overwintering generation Mean standing stock (mg m - 3, Daily production (mg m-s) Total production (daily production x life-span in days) for the generation (mg m- 3, Daily P/B coefficient Generation P/B coefficient and lifespan

123.900 2,688

725.828 0.0217 5.86 9 months

Weighted mean daily production (mg me3) for all generations Mean

anual production

Mean

annual

Annual

standing

P/B coefficient

(mg m-3) stock (mg m- ‘)

Spring generation

Summer generation

342.275 6,973

530.300 13.971

1045.990 0.0204 3.06 5 months

2514.780 0.0263 4.74 6 months

=7.1442 7.1442

x 365

=2875.11 =332,185 =7.85

O-500 x 100e3 mg weight classof the overwintering generation there were 29 individuals with a mean individual massof 250 x 10m3mg. Standing stock for that classwas therefore 7 250 x 10d3 mg m- 3. Summation of data for all classeswithin generations gives total standing stock (Table 3).

Estuarine

mysid Rhopalophthalmus

terranatalis

219

TABLE 4. Standing stock (mg dry mass me3), Production (mg dry mass m-3) and P/B coefficients for the Rhopalophthalmus terranatalis population in the Sundays estuary using Crisp’s (1971) summation method for populations with continuous breeding

Month

Standing stock (mg me31

Jan

634.44

Feb Mar

582.91

Apr May

51.86

July Aug

85.61 80.12

Sept Dee Total

P/B

504.39 406.67 292.29 137.90 57.01 20.34 20.20 16.72 26.67 56.48 85.98 309.69

0.80 0.70 0.68 0.61 0.58 0.39 0.24 0.21 0.29 0.46 0.48 0.77

429.89 227.04 99.03

June

Ott Nov

Production (mg me3)

91.03 123.49 178.48 402.55

1934.34

2986.45

Mean monthly standing stock = 248.87 mg m 3 Annual P/B coefficient = 7.77

An estimate of daily and generation P/B ratios was then calculated (Table 3). The annual P/B coefficient (Table 3) is derived from the equation: 365 x

weighted mean daily production mean annual

standing

stock for all generations

A second estimate of population production was obtained using the method of Crisp (1971): Annual production = c c fi Gi q At, f=o 0 where fi refers to the number of individuals of development stagesi, LVi to the mean mass (in mgme3) of that-class and Gi to the instantaneous growth rate which is measured independently: G,=2.303 dlog,,W dt



The development time (At) of stagei is derived from the growth curve (Figure 5). Annual production using this method (Table 4) is lower than that calculated graphically. Although both are based on the growth rate of individuals, Crisp’s summation method is sensitive to the range within size classes;in this case data were separated into three groups. Production values are therefore likely to be underestimated, particularly for juveniles. The summation method also ignores larvae prematurely lost during marsupial development. In the graphical method brood losswas minimized since data were derived from females with newly extruded eggs. The summation technique gives monthly production estimates for the population, the values of which ranged from less than 25mgme3 (ml‘d -winter, June-Aug) to over 500 mg m-3 in January.

220

T. H.

Wooldridge

Discussion In the Sundays estuary Rhopalophthalmus terranatalis breeds continuously for eight months of the year producing three generations. A relatively long-lived overwintering group is succeeded by two further generations in the spring and summer respectively (Figure 3). During the lifespan of the former group, water temperatures ranged between 14 and 20 “C; and for the latter two, between 20 and 27 “C. The size attained by adults of different generations and generation density (numbers me3) were inversely related. In mid-to-late summer adults were relatively small in size but population density was high. Individuals of the over-wintering group attained a larger body size, but density mP3 was low. Fecundity was positively correlated with body size. This relationship was significantly different between generations, the size of the brood decreasing differentially between generations for a female of any given length. Although changesin body size and fecundity occur during the year, female R. terranatalis all produce up to five broods. Additional broods are sometimes extruded, but these were not included in calculations since marsupial contents are occasionally ejected by individuals. Ejection may occur in any female, and is possibly due to non-fertilization of eggsafter extrusion into the pouch. Such complex life history patterns in continuously breeding populations where there is no synchrony in larval releaseand egg extrusion makes it impossible to identify and track cohorts. More commonly applied methods for estimating secondary production are therefore excluded. Alternative methods include Winberg’s graphical technique (197 1) which has been applied to small crustaceans such as copepods (see Winberg, 1971). Amongst the Peracarida, the method has been used by Venables (1981) for the sandbeach amphipod, Talorchestia margaritae. The method requires detailed information on the biology of the organism under investigation, but this may be difficult to obtain. Details required include body growth rates which may be derived from animalsmaintained in the laboratory. These do not necessarily reflect growth in natural assemblages,so that some measure of the reliability of experimental data is essential. In R. terranatalis, breeding is discontinued from mid-April through mid-August in the estuary and allows young size-class cohorts to be identified and their growth followed. The disappearance of summer generation adults in May further aided tracking of cohorts during the succeeding winter months. Since experimental temperatures followed ambient conditions, direct comparison of growth between field and laboratory animals was possible. Successful rearing in the laboratory was also dependent on diet and food was always present in excess.The food given was based on an extensive study of the contents of the buccal cavity (Wooldridge & Bailey, 1982). When breeding commenced in August, cultured mysids had attained a body length of 17.3 mm. Their counterparts in the estuary ranged between 17.0 and 20.5 mm, but these individuals were from all five broods produced by the previous generation. Since growth continues after mysids become sexually mature, four of the five broods were larger than reared mysids which correspond to the youngest brood (about 140 days old). Thereafter, brood releasein the field population was asynchronous and it was not possible to follow a specific cohort. Growth and body sizebetween field and laboratory overwintering animalscorresponded closely so that extrapolation of experimentally-derived information was considered acceptable. Production was estimated for each generation and this allowed for the incorporation of characteristics specific to a generation. To calculate annual production a weighted mean of daily production of the three generations was derived. Annual

Estuarine mysid Rhopalophthalmus

5. Summary

TABLE

of production-biomass

ratios currently Daily P/B ratios

Species

221

terranatalis

available Seasonal P/B ratios

for mysid

shrimps

Annual P/B ratios

Mysis relicta (Hakala 1978)

3.0-3.8

Mysis (Sell,

2.2-3.3

relicta 1982)

Neomysis americana (Richards

& Riley,

3.66 1963)

Neomysis mirabilis (Shuskina, 1973)

0.13-0.17

Neomysis integer (Bremer & Vijverberg, 1982) Overwintering generation 1st summer generation 2nd summer generation Paramysis intermedia (Miroshnichenko & Vovk,

max 0.015 max 0.038 max 0.050

12.5 (7 months)

1973)

Rhopalophthalmus terranatalis (Present study) Overwintering generation

0.022

Spring

0.020

Summer

generation generation

4.0 (6 months)

0.026

5.86 (9 months) 3.06 (5 months) 4.74 (6 months)

7.85

production was also calculated using a method of summation described by Crisp (1971) giving production for any month. Production estimates for mysids are available for a few species(Table 5). BesidesR. terranatalis, all are from the northern hemisphere and mostly inhabit cold freshwater lakes. These studies employ a range of techniques and usually refer to part of the year only. In Lake Paarjarvi in southern Finland, embryos of Mysis relicta remained in the brood pouch for about six months through the winter (Hakala, 1978). The young attained maturity in the summer and began breeding with the onset of the following winter. Young releasedrelatively late in the season(extended period of egg extrusion) spent the first winter as immature animals. Thus a relatively shortlived group (1 year) alternated with a second which had a lifespan of two years. The dynamics of each group was ultimately dependent upon the time in summer when young were releasedfrom the brood pouch. In this case M. relictu was shown to have an annual P/B coefficient varying between 3.0 and 3.8 (Hakala, 1978). Comparable P/B ratios of 2.2-3.3 were obtained for the samespeciesin a re-analysis of five Great Lakes studies by Sell (1982). Purumysis intermediu also inhabits cold freshwaters and was shown to have a monthly P/B coefficient varying between 0.91 and 2.25 (Microshnichenko & Vovk, 1973). For the entire period of reproduction (April through October), the P/B coefficient was calculated to be 12.5. The method of calculating production by these authors was based on methods used in the study of fish populations. During the remaining months of the

222

T. H. Wooldridge

year (November through March), reproduction ceased in P. intermedia when water temperatures fell below 10 “C. High P/B values were also computed for Neomysis mirabilis from the Sea of Japan (Shuskina, 1973). Daily P/B ratios were calculated indirectly over short time periods and varied between 0.13 and 0.17 per day. Data are available for two other species of Neomysis. Richards & Riley (1963) estimated the annual P/B ratio of Neomysisamericana to be 3.66 in Long Island Sound. These authors stated that more than a single brood may be produced and suggestedthat the turnover rate of 3.66 was possibly too low. There is evidence that this is so, for in Psammoquoddy Bay, two generations are produced annually and each female is capable of producing two or three broods (Pezzack & Corey, 1979). Estimates of daily production were calculated for Neomysis integer occurring in a shallow Frisian freshwater lake by Bremer & Vijverberg (1982). Calculations were done for the period May through October when water temperatures varied between 15 and 20 “C. By the end of October breeding ceasedwhen temperatures fell to 5 “C. For this speciesthe authors recorded three peaks in population density, designated by them as representative of an overwintering and two summer generations. Maximum daily production/biomass ratios of 0.015, 0.038 and 0.050 were calculated for each, while for the whole research period of 6 months, the P/B ratio was calculated to be 4.0. These data compare well with R. terranatalis for both the daily and medium term. For the whole year the value of 7-85 obtained in the present study is considerably higher than the ratio of 4.0 which was extrapolated for N. integer assuming that no production occurred in winter. Considering the temperature regimes between the two study sitesand the longer breeding period of R. terranatalis a high value obtained for the latter speciesis not unexpected. Furthermore the annual value of 7.85 represents overlapping generations with only a short period of reduced production. The life history of R. terranatalis summarized diagrammatically in Figure 3 is based on the pattern usedby Mauchline (1980). In summary, a longer-lived overwintering generation composedof relatively few, large individuals producing large broods contrasts with a relatively short-lived summer generation composed of many smaller individuals producing smaller broods. Although the spring generation reflects some characteristics of the other two, production may be a slight underestimate due to severe flooding of the estuary in August and again in September during the first year of the field study (Wooldridge & Bailey, 1982). At such times populations may be reduced or even lost to the estuary due to flushing. Such aperiodic events are natural phenomena and must be taken into account. If severe flooding had occurred later in the summer the effect on mysid production would have been considerably greater. Their biology, however, isgeared to accommodate these events and recovery is relatively rapid. Finally, the relatively high turnover rate for R. terranatahs coupled with their abundance in the Sundays contributes to the hypothesis that they play an important role in energy transfer to other trophic levels in the estuary.

Acknowledgements This research was supported by funds provided by the Department of Environmental Affairs. The help of Cheryl Bailey in the laboratory is acknowledged, as well as Dan Baird, Anton McLachlan and Ted Donn whose comments improved the manuscript.

Estuarine

mysid

Rhopalophthalmus

terranatalis

223

References Blaber, S. J. M. 1979 The biology of filter feeding teleosts in Lake St Lucia. 3ournal of Fish Biology 15, 37-59. Bremer, I’. & Vijverberg, J. 1982 Production, population biology and diet of Neomysis integer (Leach) in a shallow Frisian lake (The Netherlands). Hvdrobioloaia 93.41-51. Crisp, D. J. 1971 Energy flow measurements. Id(Holme;N. A.‘& McIntyre, A. O., eds) Methodsfor the Study of Marine Benrhos. IBP Handbook No. 16. Blackwell Scientific Publications, Oxford. pp. 197-279. Hakala, I. 1978 Distribution, population and production of Mysis relicta (Loven) in southern Finland. Annales Zoologici Fennici 15: 243-258. Lasiak, T. A. 1983 The impact of surf-zone fish communities on fauna1 assemblages associated with sandy beaches: a review. In (McLachlan, A. & Erasmus, T., eds) Sandy Beaches as Ecosystems. Junk Publishers, The Hague. Mauchline, J. 1980 The biology of mysids and euphausids. In (Blaxter, J. H. S., Russell, S. & Young, M., eds) Advances in Marine Biology 18. Academic Press, London. pp. l-681. McLachlan, A. 1983 The ecology of sandy beaches in the eastern Cape, South Africa. In (McLachlan, A. 81 Erasmus, T., eds) Sandy Beaches as Ecosystems. Junk Publishers, The Hague. McLachlan, A., Erasmus, T., Dye, A. H., Wooldridge, T., van der Horst, G., Rossouw, G., Lasiak, T. A. & McGwynne, L. 1981 Sandy beach energetics: an ecosystems approach towards a high energy interface. Estuarine, Coastal and Shelf Science 13, 1 l-25. Microschnichenko, M. P. & Vovk, F. I. 1973 A model of Mysidae production process as exemplified with Paramysis inrrrmedia (Czem) from Tsimlyanskoye Reservoir. Gidrobiologicheskii Zhurnal9,36-$4. Pezzack, D. S. & Corey, S. 1979 The life history and distribution of Neomysis americana (Smith): Crustacea, Mysidacea. Canadian rournal of Zoology 57,785-793. Richards, S. W. & Riley, G. A. 1967 The benthic epifauna of Long Island Sound. Bulletin of the Bmgham Oceanographc Collection 19(2), 89-129. Sell, D. W. 1982 Size-frequency estimates of secondary production by Mysis relicta in Lakes Michigan and Huron. Hydrobiologia 93,69-78. Venabies, B. J. 1981 Aspects of the population biology of a Venezuelan beach amphipod, Talorchestta margaritae (Talitridae), including estimates of biomass and daily production, and respiration rates. Crustaceana 41,271-285. Whitfield, A. K. & Blaber, S. J. M. 1978 Food and feeding ecology of piscivorous fishes at Lake St Lucia, Zululand. Journal of Fish Biology 13,675-691. Winberg, G. G. (ed.) 1971 Methods for the Estimation of Production of Aquatic Animals. Academic Press, London. Wooldridge, T. 1983 Ecology of beach and surf zone mysid shrimps in the eastern Cape, South Africa. In (McLachlan, A. & Erasmus, T., eds) Sandy Beaches as Ecosysrems. T. Junk Publishers, The Hague. Wooldridge, T. & Bailey, C. 1982 Euryhaline zooplankton of the Sundays estuary and notes on trophic relationships. South AfricanJournal of Zoology 17, 151-163. Wooldridge, T. & Erasmus, T. 1980 Utilization of tidal currents by estuarine zooplankton. Estuarine, Coastal Marine Science 11, 107-l 14.