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Feeding of two mysid species on plankton in a temperate South African estuary
Journal
ELSEVIER
of Experimental Marine Biology and Ecology 188 (1995) 243-259
Feeding of two mysid species on plankton South African estuary
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
in a temperate
H. L. Jerling”, T. H. Wooldridge Department of Zoology and Institute for Coastal Research, University of Port Elizabeth. P.O. Box 1600, Port Elizabeth 6000, South Africa Received
23 June 1994; revision received 5 December 1995; accepted 19 December
Abstract sympatric mysid species, Mesopodopsis wooldridgei and Rhopalophthalmus terranatalis, dominate mesozooplankton biomass in the Sundays River estuary, South Africa. This study aimed to investigate the food and feeding rates of the two mysids on naturally occurring phytoplankton and microzooplankton assemblages, and on copepod instars, using laboratory based feeding and predation experiments. Maximum clearance rates calculated for different size classes of M. wooldridgei on microplankton were on average 34.2, 15.8 and 18.6 ml.ind-i.h-’ for adults, immatures and juveniles respectively. For the same R. terranatalis size classes clearance rates were 8.5, 13.0 and 13.5 ml’ind-‘.h-’ respectively. Thus, all size classes of the smaller M. wooldridgei had higher maximum clearance rates compared to any of the stages of the larger R. terranatalis, indicating that the former species fed more successfully on phyto- and microzooplankton and that these prey assemblages probably constitute the lower limit of the food particle size range consumed by the latter species. R. terranatalis is more successful in preying on larger plankton such as adult copepods and juvenile mysids. Microzooplankton was generally more important in mysid diet than phytoplankton. Apparent selection for microzooplankton species was probably due to an inability to feed efficiently on the smaller phytoplankton cells. Copepod nauplii were readily consumed by all mysid size classes. Predation rates, in terms of weight specific carbon ingestion, increased linearly with copepod instar prey concentration. Two
Keywords:
Estuary;
Feeding;
Mysids;
Plankton;
* Corresponding author. Present address: Department X1001, Kwadlangezwa, 3886, South Africa. Elsevier Science B.V. SSDI 0022-098 1(95)00007-O
South Africa
of Zoology,
University
of Zululand,
Private
Bag
244
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. EA.
I88 11995) 243-259
1. Introduction Mysids live in a large variety of aquatic habitats and exploit a diversity of food sources very successfully (Mauchline, 1980). They are generally considered to be omnivorous, although herbivory, in the form of phytoplankton (Bowers & Grossnickle, 1978; Webb et al., 1987) or carnivory (Cooper & Goldman, 1980; Johnston & Lasenby, 1982; Fulton, 1982; Wooldridge & Webb, 1988) have been reported for some species. There is currently a paucity of data on potential feeding of mysids on microzooplankton. Species sharing the same habitat may rely on differences in the utilization of food resources to avoid competition (Schoener, 1974). Two co-existing mysid species, Mesopodopsis wooldridgei (previously M. slabberi, Wittmann, 1992) and Rhopalophthalmus terranatalis, dominate mesozooplankton biomass in the Sundays River estuary, South Africa (Wooldridge & Bailey, 1982). Comprehensive descriptions of this estuary are given in Wooldridge & Bailey (1982), Hilmer & Bate (1990) and Mackay & Schumann (1990). Although Wooldridge & Webb (1988) reported evidence of spatial separation of both species, especially between juvenile M. wooldridgei and adult R. terranatalis, overlap in spatial and temporal distribution occurs in the middle estuarine reaches (Jerling & Wooldridge, 1995) which may lead to resource partitioning. Wooldridge & Bailey (1982) suggested that a major part of the foodweb in the Sundays River estuary was centred in the water column. Due to their relatively large size mysids would be amongst the top predators of the mesozooplankton in this planktonic foodweb with phytoplankton, microzooplankton and copepod instars as potential prey. The feeding of M. wooldridgei on two diatom species which dominate surfzone phytoplankton assemblages along the Sundays River beach (Talbolt et al., 1990) was studied by Webb et al. (1987). These two diatom species do not occur in estuaries. Instead, estuarine phytoplankton was dominated by an entirely different community, mainly composed of flagellates (Jerling & Wooldridge, 1995). Previous studies on R. terranatalis feeding were restricted to predation on juveniles of M. wooldridgei and adults of the copepod Pseudodiaptomus hessei in the Sundays River estuary (Wooldridge & Webb, 1988). However, the abundant phyto- and microzooplankton of the water column in the estuary may also contribute significantly to the diet of R. terranatalis, especially for the smaller size classes. Copepod nauplii formed a significant and consistent food item in the diet of Mysis relicta in Lake Michigan (Bowers & and Vanderploeg, 1982). Since copepod nauplii were highly abundant in the water column of the Sundays (Jerling & Wooldridge, 1991; Jerling & Wooldridge, 1995) they would also be readily available as a food source for mysids. This study aimed to investigate, using laboratory based feeding and predation experiments, whether phytoplankton, microzooplankton and copepod instars (nauplii and copepodid stages) formed significant components in the diet of any of the different developmental stages of M. wooldridgei and R. terranatalis.
H.J. Jerling, T.H. Wooldridge / J. Exp. Mar. Biol. Eeol. 188 (1995) 243-259
245
2. Methods 2. I. Feeding experiments on phyto- and microzooplankton Mysids and water samples containing natural assemblages of phyto-and microzooplankton were collected at night from the middle reaches of the Sundays estuary (salinity 20-25%,). All samples were transported to the laboratory where they were maintained overnight in 20-l containers at the same temperature from which they were collected (18 ‘C). Experiments commenced the next day. Water samples were filtered through a 90 pm sieve to remove any copepod instars that may have been present. Mysids used as predators were first sorted into three functional groups: adults (secondary sexual characteristics fully developed, R. terranatahs - z 15-18 mm, M. wooldridgei - G 8- 10 mm), immatures (secondary sexual characteristics not fully developed, mm) and juveniles (no sexual R. terranatalis - z S- 10 mm, M. wooldridgei - ~6-7 distinction possible, R. terranatalis - ~4-6 mm, M. wooldridgei - z 2-4 mm) (Mauchline, 1980; Wooldridge & Bailey, 1982). Experimental feeding rates have been shown to be suppressed when conducted in small containers (Peters, 1984). A preliminary experiment, using R. terranatalis adults as predators feeding on rotifers and microciliates, indicated an increase in filtration rate with container volume which tapered off at a container size of 500 ml (Fig. 1). In this experiment predator density was kept constant at 1 mysid per 50 ml and only the volume of estuarine water in the feeding containers increased. The experimental procedure was similar as that described below. Assuming a similar response to container volume in M. wooldridgei, the minimum volume used in the final experiments was 500 ml for both species. Adults of both species as well as immature R. terranatalis (similar in size to adult M. wooldridgei), were placed in buckets containing 1 1 of estuarine water. Containers of 500 ml capacity were used for all other mysid size classes. Five adults (males and females mixed, gravid females were not used), or 10 individuals representing smaller mysid classes were introduced as predators into experi16 ,:... '."'.....,.,,,' ,:' ,:' . ,:' ,:' ,:' ,:' ,:' . .... . :' ,.: .:' . ..~'~"".......,.. ,,,,
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.... ,_..,......:~.~.;::“:~~” I I 50
Feeding
100
container
I
I
500
volume
.
1000
(ml)
Fig. 1. The effect of container size on clearance rates for adult R. terrunatalis feeding on rotifers microciliates (m). Dotted lines connect the average values of duplicate runs.
(A) and
246
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
mental buckets. This represented mysid densities up to twice that of the maximum densities recorded in the field (Wooldridge & Bailey, 1982; Wooldridge & Webb, 1988). Containers were not sealed and rotated since prey species were motile (rotifers, ciliates and the various flagellates). Three to five replicates were run for each mysid size class. Three sub-samples (30 ml each) of the estuarine water used in experiments were preserved with 1 y0 acid Lugols (Parsons et al., 1984) at the start of each experimental run in order to establish initial phyto- and microzooplankton concentrations. Mysids were allowed to feed overnight for 13 h. In addition, three control containers from which mysids were excluded were treated in the same manner as experimental containers. At the end of the feeding period live mysids were counted. The concentration of phyto- and microzooplankton present at the beginning and after the 13 h feeding period was established with the aid of an inverted microscope, using the Utermiihl technique according to the recommendations by Hobro & Willen (1977). Flagellates, dinoflagellates and ciliates were divided into separate size groups based on morphology and size (Table l), using the terminology suggested by Sieburth et al. (1978): These groups were nanoplankton (2-20 pm) and microplankton (20-200 pm), All dinoflagellates were classified as phytoplankton and all ciliates were assumed to belong to the microzooplankton. Two categories within the microciliate group were recognized: microciliates and large microciliates (Table 1). Prey size (length and width) within each category was measured using an eyepiece micrometer. At least 10 individuals representing each prey category were measured. These measurements were used to construct scale models from clay enabling average volume of each prey category to be calculated. Flagellate and dinoflagellate carbon content was estimated from Log C= - 0.460 + 0.866(log V) (Strathmann, 1967), where C is the carbon content (pg) and V the cell volume (pm3). Rotifer dry mass was considered to be 10% of wet mass (assuming a density of 1.0) (Bottrell et al., 1976). Ciliate volumes were converted to dry mass using the factor 0.17 pg.prn-” (Laybourn & Finlay, 1976). Carbon content of rotifers and ciliates was assumed to be 40% of dry
Table 1 Length (pm) and estimated in the feeding experiments Prey
volume (pm3) of phyto- and microzooplankton
Abbreviation
Length
WI (E)
8.7 17.4 17.4 29.0
(1.7) (2.8) (2.7) (2.5)
215 567 1664 8715
11.6 26.1 33.1 54.0 59.9
(5.1) (8.1) (3.4) (3.8) (7.5)
798 7534 3098 42956 103236
WV
(PDF) W)
(PC) WV (PC*) (R) SD = one standard
deviation,
present as prey species for mysids
II = 10, P = phytoplankton,
M = microzooplankton
(SD)
Volume
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
241
mass, a conversion factor generally used for zooplankton (e.g. Robertson, 1983; Lampert, 1984; Gifford & Dagg, 1988). Mysids were measured along the dorsal midline from the anterior margin of the carapace to the tip of the telson, excluding spines. Measurements were done using a stereo dissecting microscope fitted with an eyepiece micrometer. Dry mass was calculated using length to dry mass relationships (Wooldridge & Bailey, 1982). Carbon content was assumed to be 40% of dry mass (Wooldridge, unpubl. data). The term clearance rate, indicating the volume of ambient medium from which cells are completely removed by mysids, will be used in this study. Clearance rate is synonymous with volume swept clear, filtering, filtration or grazing rates (Frost, 1972; Peters, 1984). Clearance rates, F (mleind-‘.h-‘) and ingestion rates, I (cells.ind-‘.h-‘) were calculated using the equations of Frost (1972). These equations incorporate changes in prey abundance in the control containers due to cell growth. Using the carbon estimates described above, carbon ingestion rates CI (ngeind-‘.h-‘) could be calculated. Care should be taken when estimating feeding rates, not to work over the incipient limiting level of food particle concentration (Peters, 1984), where animals pass from a concentration where ingestion rate is constant to one where clearance rate is constant. From the literature this concentration seems to lie between 1 and 10 ppm (v/v) (Peters, 1984). In this study the concentrations of individual prey groups were all below 1 ppm, with the highest concentration attributed to rotifers (Z 0.3 ppm v/v). 2.2. Predation on copepod nauplii and copepodid stages Predation on natural assemblages of nauplii and copepodids was determined for juvenile, immature and adult R. terranatalis and M. wooldridgei. Prey groups were collected in the estuary using a modified WP2 net fitted with 90 pm mesh during daylight hours. Due to the demersal behaviour of the adult copepods (Grindley, 1972) samples collected in the water column contained predominantly nauplii and copepodids of the calanoid copepods Acartia longipatella and P. hessei. The samples collected with the plankton net were carefully introduced into a container holding 20 1 of estuarine water. This provided a relatively concentrated mixture of copepod nauplii and copepodids for experimental purposes. Two to five subsamples were removed from this concentration with a 5 ml wide-bore (8 mm diameter) pipette and a 20 ml Perspex tube (after gentle mixing). Samples were introduced into 5 1 experimental feeding buckets containing 2 1 estuarine water to provide prey assemblages at various concentrations for mysid predators. On average, copepod nauplii and copepodid stages contributed between 5 and 60 pg*l-’ to the zooplankton carbon during the year in the estuary (calculated from unpublished data). Experimental prey carbon concentrations spanned this range, in most cases, and maximum concentrations were in some cases more than double the average field concentrations. Water volumes in the feeding buckets corresponded to those used by Wooldridge & Webb (1988). All experiments were conducted at ambient summer temperatures ranging between 20 and 25 o C. Five adult, 10 immature or 15 juvenile M. wooldridgei were added to experimental containers. Corresponding numbers for the R. terranatalis size classes were 3, 5 and
248
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. I88 (1995) 243-259
10, respectively. Adult and immature densities were similar to those used by Wooldridge & Webb (1988). Predators were allowed to feed for 24 h before termination of experiments. Ambient light was dimmed by covering experimental buckets with opaque plastic lids. Three replicate experiments were conducted at each prey concentration. Three subsamples representing each experimental prey concentration were preserved before the start of each experimental run to determine initial concentrations. Two control buckets without predators were treated in a similar way at each experimental concentration. At the end of each 24 h experimental run, predators were checked for condition and any dead mysids were ignored for calculation purposes. Formalin was added (Z 10% final concentration) to experimental containers, preserving remaining prey animals. Prey preserved in this manner were carefully sieved out and counted. Nauplii and copepodids of A. longipatella were counted separately. Adults of this species were sometimes present and these were also counted separately. Nauplii of P. hessei were divided into two groups representing developmental stages N2-N4 and N5-N6, respectively. Copepodids of P. hessei consisted entirely of stages Cl-C3 since the prey were collected during daylight hours in near-surface waters. Predator length was measured using an eyepiece micrometer of a dissecting microscope. Animals were measured from the anterior margin of the carapace to the end of the telson, excluding spines. Mysid dry mass was determined using length-mass equations (Wooldridge & Bailey, 1982). The dry mass of nauplii and copepodids was estimated from published as well as from unpublished data (Wooldridge & Bailey, 1982; Jerling & Wooldridge, 1991). Carbon content of prey was assumed to be 40% of dry mass. Predation rate was calculated as the number of prey consumed per predator per day. Using predation rate and predator dry mass the mass specific carbon ingestion rate was expressed as FgC ingested.(mg predator dry mass))‘.day -‘. Electivity indices Ei* (Vanderploeg & Scavia, 1979b) were calculated from predation rates [ = feeding rate (Gi), Vanderploeg & Scavia, 1979a] to determine possible selection for nauplii or copepodid prey.
3. Results 3.1. Feeding on phyto- and microzooplankton Composition of phyto- and microzooplankton in the estuarine water used in the feeding experiments is indicated in Fig. 2. Potential prey organisms ranged from = 9 pm (nanoflagellates) to 60 pm (rotifers) in length (Table 1). Nanoflagellates were the most abundant of all groups present in the water; microdinoflagellates contributed most to total phyto- and microzooplankton carbon (Fig. 2). Other important contributors to phyto- and microzooplankton carbon were nanoflagellates, microciliates and rotifers. No predator mortality occurred during the feeding experiments. Although nanoflagellates were the most abundant prey group, they were not predated upon by M. woold-
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 350
-
300
-
250
-
200
-
249
25
20 L
q
Ei = : -0 sj Q 0
15
: 0
3
150-
10
100
-
50
-
7
5
o-
0 nF
E
-Phytoplankton-
nDF
PDF
nC
/JC
/JZF
(AC*
R
--Microzooplankton-
Prey Fig. 2. Abundance (open bars) and carbon contribution (shaded bars) of microplankton in the estuarine water used in feeding experiments. Refer to text (Table 1) for prey abbreviation and ranking.
ridgei (Fig. 3). Most of the other phytoplankton groups present in the estuarine water were consumed by juvenile M. wooldridgei, although at a relatively low rate (generally less than 5 ml.ind-‘.h-‘). Immature and adult M. wooldridgei only consumed microdinoflagellates in the phytoplankton category. All three size classes consumed microzooplankton, with each class showing increasing clearance rates with increasing prey size. Clearance rates were maximal for rotifers, the calculated average values being 34.2, 15.8 and 18.6 ml.ind-‘.h-’ for adults, immatures and juveniles, respectively. Clearance rates for adults were in general double the values calculated for juvenile and immature mysid classes (Fig. 3). Rotifers also contributed most to phyto- and microzooplankton carbon ingested by M. wooldridgei, the calculated averages being 228.7, 45.5 and 47.5 ngind-‘.h-’ for adult, immature and juvenile mysids respectively (Fig. 3). Phytoplankton was not extensively utilized as a food source by adult and immature R. terrunatalis (Fig. 4). Consumption of nanoflagellates by adults was evident, but the calculated clearance rate was low (< 1 ml.ind-‘.h-‘) with a large variation between replicates. Juveniles fed on most of the phytoplankton categories although clearance rates were low (< 5 mlind-‘.h-‘). The microzooplankton component was predated upon by all R. terrunatulis size classes. Rotifers formed the most important component, with clearance rates of (8.5, 13.0 and 13.5 ml*ind-‘.h-’ for adult, immature and juvenile mysids respectively) (Fig. 4). Other microzooplankton prey categories were cleared at rates below 5 ml.ind-‘.h-’ by all mysid classes. Rotifers also formed the most important source of carbon for all R. terrunatalis classes (77.9,71,5 and 42.0 ngC*ind-‘.h-’ for adults, immatures and juveniles respectively) (Fig. 4). Contribution by other microplankters to ingested carbon was below 20 ngeind-‘.h-’ for all R. terranatalis instars. Means of the total phyto- and microzooplankton carbon ingested by the three mysid size classes (Table 2) and mysid biomass were used to calculate the weighted carbon ingestion rate for both prey groups (Fig. 5). Microzooplankton contributed on average
250
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 Mesopodopsis 50 -
40
woofdridgei -
Adults
300
- 250
-
- 200 30 - 150 20 - 100 10 -
- 50
I-0
o-
25 -
52
Immatures
20 = ‘L G ; TI .c
15-
g
lo-
IL cl
5-
0
o-
25 -
52
Juveniles
42
31
21
10
0 nF
E
nDF
-Phytoplankton-
uDF
nC
I
I
PC
jG!F
I
MC’
I
R
--Microzooplankton-
Prey Fig. 3. Clearance rates (open bars) and carbon ingestion rates (shaded bars) calculated for the three M. wooldridgei size classes. Refer to text (Table 1) for prey abbreviation and ranking. Vertical lines = 1 SD; n = 4.
more than 70% to the total phyto- and microzooplankton carbon ingested by all classes of both mysid species (Fig. 5). Phytoplankton contributed on average ~20% to the
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
251
Rhopalophthalmus terranatalis 12 -
Adults
10 -
a60 640 420 2-
0
o-
20
60
lmmaturer
T 70
q
60
Q
50
s
40
0 g P
30
2
20
-? ,’
10 0
0
50
20
40 15
30 10 20
5 10
0
0 nF
E
nDF
-Phytoplankton-
I
I
I
I
PDF
nC
PC
pZF
I
PC+
I
R
-Microzooplankton-
Prey Fig. 4. Clearance rates (open bars) and carbon ingestion rates (shaded bars) calculated for the three R. terranatalis size classes. Refer to text (Table 1) for prey abbreviation and ranking. Vertical lines = 1 SD; n = 3 for adults and 4 for immatures and juveniles.
total carbon ingested by juveniles of both species, 10 to 15% of carbon ingested by immature and adult A4. wooldridgei, and less than 10% of carbon ingested by imma-
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
252
Table 2 Mean (x) phyto- and microzooplankton mysid size classes Mysid
carbon
ingestion
rates (ngC.ind
‘,h
Microrooplankton
Phytoplankton
I) calculated
for the various
Mann-Whitney
,Z
P x
SD
x
SD
M. wooldridgei Adult Immature Juvenile
39.2 13.4 14.1
57.1 22.9 15.9
275.3 78.3 66.3
52.6 25.1 29.6
4 4 4
0.03 0.06 0.06
R. terranatalis Adult Immature Juvenile
10.1 5.9 16.2
14.3 10.2 28.0
98.3 65.7 59.3
6.3 39.1 15.4
3 4 4
0.08 0.12 0.18
SD = one standard deviation. Probability (p) of no difference ingested was determined using the Mann-Whitney test.
between phyto- and microzooplankton
carbon
ture and adult R. terranatalis (Fig. 5). Carbon ingestion rates increased with increasing body size of mysids as expected (Figs. 3 and 4), but weight specific carbon ingestion decreased with increasing developmental stage (Fig. 5). Due to the high variations in the total phyto- and microzooplankton ingestion rates (indicated by the large standard deviations, Table 2) the differences between amounts of phyto- and microzooplankton carbon ingested were generally not statistically sigMesopodopsis 1200
Rhopalophthalmus
wooldridgei Adults
terranatalis
Adults
900 i-
600
4
300
i P
0
0+
1200
I: ? .g
900
;:
300
P
25 i-
rl
0’
-I
el
-
Immature5
lmmaturcs
600
0
Juveniles
I Phytoplankton
Microzooplankton
Phytoplankton
Microzooplankton
Fig. 5. Weight specific phytoplankton and microzooplankton carbon ingested by the three size classes of M. wooldridgei and R. terranatalis. Vertical lines = 1 SD; II = 3 for adult R. terranatalis and 4 for other size classes.
253
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 Mesopodopsis
Rhopalophthalmus
wooldridgei
1
Adults
1
-
terranatalis
Adults I
0.5
0.5 ..U
0.0
I
0.0
I
Tz w
0.5 -
-0.5 1 W
-
. ...?
1
0.5
.G 0.0 g
1
-1
o-o.5 2 W -1
.
-1 1
I
1
lmmaturar
-
1
-1
1
.r”o.o .g
I
-0.5
1 I
-1 c w
I
I
-0.5
.
1 1
‘i’
I
1
Juveniles
.
0.5
0.5
6
,
0.0 -0.5
,
.
I
-0.5
I
nF
E
,
nDF
0
1
-I*
-1 I
.
0.0
,
I
PDF
nC
-Phytoplankton-
I
&IC
I
PZF
MC+
I
I
R
nF
-Microzooplanktan-
I
E
I
nDF
I
vDF
-Phytoplankton-
I
nC
PC
of M. wooldridgei and ranking and abbrevia-
nificant (Mann-Whitney test, Table 2). Only adults of M. wooldridgei showed icant difference at CI= 0.05. Differences between phyto- and microzooplankton
80
Rhopalophrhalmus
wooldridgei
Adults
-I
PC*
--Microzooplankton-
Fig. 6. Electivity indices calculated from clearance rates for the three size classes R. terranatalis feeding on microplankton. Refer to text (Table 1) for microplankton tion.
Mesopodopsis
I
@F
a signifcarbon
&sranstalis
Adults
-I
lmmaturer
u n
60
Juveniles
1
AN
PNa
PNb
Juveniles
1
AC
PC
AA
AN
PNa
PNb
AC
PC
AA
Fig. 7. Composition of prey during mysid predation experiments. Acartia longipatella: AN = nauplii, AC = copepodids, AA = adults. Pseudodiaptomus hessei: PNa = nauplii N2-N4, PNb = nauplii N5-N6, PC = copepodids. Prey ranked according to size. *, Not present in feeding containers.
7
R
254
H.J. Jerling, T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
ingested by immatures and juveniles of this species and adults of R. terranatalis were marginally significant at a = 0.10. For immatures and juveniles of R. terranatulis differences were not significant (R = 0.20 and 0.15, respectively). Electivity indices Ei* (Fig. 6) (Vanderploeg & Scavia, 1979b) calculated from the clearance rates, clearly indicate selection for the largest microzooplankton category for all classes of both mysid species. For all instars there is also a trend suggesting a preference for increasing prey sizes. None of the mysid instar groups selected for the phytoplankton species. 3.2. Predation on nauplii and copepodids No predator mortality occurred during the feeding experiments. Prey abundance during the experimental runs did not change in control chambers. The most abundant i
25
-0
1
Mesopodopsis
wooldridgei
25
50
Prey -
25
-
i9 i
CR 20
75
cont.
100
125
150
(pgC.I-‘I
Rhopalophthalmus terranatafis
Y = 0.15% - 0.317
-
6
0
25
50
75
Prey cont.
100
125
150
IpgC.I-‘I
Fig. 8. Weight specific predation rate in terms of carbon ingestion for M. wooldridgei and R. ferranntnlis size classes. Adults (O), immatures (H), Juveniles (A). For R. ferranatali.r juveniles, experiments were run at Only two prey COnCCntratiOnS. VCrtiCd h?S = 1 SD; n = 3.
H.J.
Jerling,
T.H.
Mesopodopsis
-1
Mar. Biol. Ecol. 188 (1995)
wooldridgei
'1
r
Wooldridge / J. Exp.
'1
Adults
J
I
1 1
r w
t.............. *
I
* I
-1. j) AN
.
.I .
I
~
i
1
I
1 1
*
.
Juveniles
0.5 ._............
I
I
I
-1
Juveniles
.! ,..,,..,_..,.! I
-0.5
Lo.5 0 w
1
.
lmmatursr
1
0.5
E 0.0 2
L .... ........ .. ’
1
._
terranatalis
Adults
-1 J
I
lmmaturss
ET 0.5
Rhopalophthalmus
255
243-259
f
,
0.0 .
#
#
.
,
PNa
PNb
AC
PC
I
I
.
*
*
.
AC
PC
I
-0.5 ( AA
.
-1 AN
PNa
PNC
a
I AA
Fig. 9. Electivity indices calculated for size classes of M. wooldridgei and R. terranatalis feeding on copepod instars. Acartia longipatella: AN = nauplii, AC = copepodids, AA = adults. Pseudodiaptomus hessei: PNa = nauplii N2-N4, PNb = nauplii NS-N6, PC = copepodids.
category present was P. hessei nauplius stages N2-N4 (Fig. 7). Acartia longipatella nauplii and copepodid stages were not represented in feeding chambers when experiments using adult R. terranatalis were undertaken. Weight specific predation rate increased with increasing prey concentration (Fig. 8). The rate of increase was linear for all mysid instars and did not taper off at the highest prey concentrations investigated. The trend towards higher weight specific carbon ingestion rates by smaller predator size classes was more pronounced for M. wooldridgei than for R. terranatalis. The carbon ingestion rate by juvenile and immature classes of the latter species did not differ significantly. Adult mysids showed a decreasing trend in prey selection with increasing prey size (Fig. 9), suggesting preference for smaller prey (nauplii). As the preferred prey were also the most abundant (Fig. 7), this observation may also reflect an opportunistic feeding strategy. Immatures and juveniles, particularly of M. wooldridgei, showed a large scatter in the calculated electivity indices with no persistent selection for any prey group.
4. Discussion The use of natural prey assemblages in feeding experiments using cell counts may pose several difficulties with respect to methodology (Peters, 1984) and interpretation of results. However, the method is more representative of events in the field compared to monospecific food cultures or artificially composed food assemblages and can provide valuable insight into selective feeding on different phyto-and microzooplankton components (e.g. Gifford & Dagg, 1988).
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Temporal and spatial distribution and composition of the phyto- and microzooplankton in the Sundays River estuary changes rapidly. Hilmer & Bate (1990), for example, showed that chlorophyll-u concentration fluctuated over both diurnal and spring-neap cycles. No clear seasonal pattern in phyto- and microzooplankton distribution was evident (Jerling & Wooldridge, 1995). Phyto- and microzooplankton composition in the present study can thus be considered as representative of general phytoand microzooplankton assemblages in the estuary. However, phytoplankton densities were comparatively low and did not represent bloom densities (Hilmer & Bate, 1991; Jerling & Wooldridge, 1995). Detritus was not quantified in the present study, it may however contribute significantly to the organic content of the water column. Although detritus was less significant in the nutrition of the mysid Neomysis mirubilis compared to living algae (Pechen’Finenko & Pavlovskaya, 1975), detritus is known to contribute significantly to the diet of other mysid species (Lasenby & Langford, 1973; Foulds & Mann, 1978; Mauchline, 1980; Johnston & Lasenby, 1982; Webb & Wooldridge, 1989). In the present study only the more abundant prey organisms in the water column were quantified, leading to a possible under-estimation of total carbon ingestion by the species investigated. The increase in maximum clearance rates with increasing size class in M. wooldridgei contrasts with the decrease observed in R. terrunatalis. All M. wooldridgei size classes also had higher maximum clearance rates compared to the corresponding classes of the larger R. terranatalis, indicating that the former species feeds more successfully on phyto- and microzooplankton. Microzooplankton probably constitutes the lower limit of the potential food particle size range consumed by R. terranatulis. Present results indicate that when microzooplankton abundance is relatively high (as was the case in this study), it forms a more important component in the diet of both mysids compared to phytoplankton. Apparent selection for microzooplankton species is probably due to less efficient feeding on the small phytoplankton cells. Extensive feeding of M. wooldridgei on surf zone phytoplankton was reported by Webb et al. (1987). These diatoms were however relatively large (cells 58 pm in length, but larger colonies also formed) and were comparable in size to the larger microzooplankton species in this study. Webb et al. (1987) also mention selection for the larger cell colonies. Siegfried & Kopache (1980) came to the conclusion that the selectivity patterns of mysids ingesting phytoplankton represent capturability based on size rather than true preference. The predation rate when feeding on copepod instars increased linearly with increasing prey concentration and did not taper off at the highest prey concentrations. Similar results were reported in other studies of mysid predation on zooplankton (Fulton, 1982; Wooldridge & Webb, 1988). ‘The highest copepod instar concentrations in the present predation study were more than double that of recorded field densities. A substantial decrease in prey concentration in the containers, after predation, allowed, however, for the calculation of a linear response over the 24 h feeding period even at high prey concentrations. Fulton (1982) noted that the response should in some way be non-linear and Wooldridge & Webb (1988) reported a curvilinear response when clearance rates instead of predation rates were used. Preferential feeding by mysids on nauplii compared to copepodids was probably due
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
251
to the high abundance of the former in the plankton. With a relatively high abundance of copepod nauplii in the water column, larger mysid instars would benefit more by relying on this food source. Copepodids constituted a small percentage of the plankton prey assemblages in the predation experiments, an artefact introduced by collecting prey during day times. Vigor of the escape response by prey species will also limit the feeding efficiency of mysid predators on larger instars (Grossnickle, 1982). Nauplii seem to be more readily available to mysids, by having a less effective escape response when compared to copepodid stages. This finding is in contrast to that of Siegfried & Kopache (1980) who suggested that nauplii are better able to avoid the mysids’ feeding current than copepodid stages. Observations made during this study did not support their postulation. Even though nauplii seem to be readily exploitable prey item for mysids, their relatively small size may limit their availability to the large adults of R. terrunatalis. Adult R. terranatulis do not undergo a general vertical migration into surface waters but remain near the bottom (Wooldridge & Erasmus, 1980). Copepodids, on the other hand, are known to be demersal (Grindley, 1972) and more abundant in bottom waters during day time and will be more readily available as prey to adult R. terrunatalis than nauplii which occupy surface waters in higher densities. Adult R. terranatalis also readily consume juvenile M. wooldridgei (Wooldridge & Webb, 1988) which contribute significantly to its diet.
Acknowledegments Financial assistance by the Department of Environmental Venture Programme and the University of Port Elizabeth
Affairs, the Estuarine Joint is gratefully acknowledged.
References Bottrell, H.H., A. Duncan, Z.M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norw. J. Zool., Vol. 24, pp. 419-456. Bowers, J.A. & N.E. Grossnickle, 1978. The herbivorous habits of Mysis relicta in Lake Michigan. Limnol. Oceanogr., Vol. 23, pp. 161-776. Bowers, J.A. & H.A. Vanderploeg, 1982. In situ predatory behavior of My& relicta in Lake Michigan. Hydrobiologia, Vol. 93, pp. 121-131. Cooper, S.D. & C.R. Goldman, 1980. Opossum shrimp (Mysis relicta) predation on zooplankton. Can. J. Fish. Aquat. Sci., Vol. 37, pp. 909-919. Foulds, J.B. & K.H. Mann, 1978. Cellulose digestion in Mysis stenolepis and its ecological implications. Limnol. Oceanogr., Vol. 23, pp. 760-766. Frost, B.W., 1972. Effects of size and concentration of food particles on the feeding behaviour of the Marine Planktonic Copepod Calanus pa#icus. Limnol. Oceanogr., Vol. 17, pp. 805-815. Fulton, R.S., 1982. Predatory feeding of two marine mysids. Mar. Biol. Vol. 72, pp. 183-191. Gifford, D.J. & M.J. Dagg, 1988. Feeding of the estuarine copepod Acartia tonsa Dana: carnivory vs. herbivory in natural assemblages. Bull. Mar. Sci., Vol. 43, pp. 458-468. Grindley, J.R., 1972. The vertical migration behaviour of estuarine plankton. Zool. Afr., Vol. 7, pp. 13-20.
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Grossnickle, N.E., 1982. Feeding habits ofMysis relicta - an overview. Hydrobiologia, Vol. 93, pp. 101-107. Hilmer, T. & G.C. Bate, 1990. Covariance analysis of chlorophyll distribution in the Sundays River estuary, eastern cape. Sth. Afr. J. Aquat. Sci., Vol. 16, pp. 37-59. Hilmer, T. & G.C. Bate, 1991. Vertical migration of a flagellate-dominated bloom in a shallow South African estuary. Bat. Mar., Vol. 34, pp. 113-121. Hobro, R. & E. Willen, 1977. Phytoplankton countings. Intercalibration results and recommendations for routine work. Int. Rev. Ges. Hydrobiol., Vol. 62, pp. 805-811. Jerling, H.L. & T.H. Wooldridge, 1991. Population dynamics and estimates of production for the calanoid copepod Pseudodiaptomus hessei in a warm temperate estuary. Estuarine Coastal She!f Sci., Vol. 33, pp. 121-135. Jerling, H.L. & T.H. Wooldridge, 1995. Plankton distribution and abundance in the Sundays River estuary, with comments on potential feeding interactions. S. Afr. J. Mar. Sci. (in press). Johnston, N.T. & D.C. Lasenby, 1982. Diet and feeding of Neomysis mercedis Holmes (Crustacea, Mysidacea) from the Fraser River estuary, British Columbia. Can. J. Zooi., Vol. 60, pp. 813-824. Lampert. W., 1984. The measurement of respiration. In, A manual on methods for the assessment ofsecondaryproductivity, edited by J.A. Downing & F.H. Rigler, Blackwell Scientific Publications, Oxford, pp. 413468. Lasenby, D.C. & R.R. Langford, 1973. Feeding and assimilation of Mysis relicta. Limnol. Oceanogr. Vol. 18, pp. 280-285. Layborn, J. & B.J. Finlay, 1976. Respiratory energy losses related to cell weight and temperature in ciliated protozoa. Oecologia, Vol. 24, pp. 349-355. Mackay, H.M. & E.H. Schumann, 1990. Mixing and circulation in the Sundays River estuary, South Africa. Estuarine Coustal. Shelf: Sci., Vol. 3 1, pp. 203-216. Mauchline, J., 1980. The biology of Mysids and Euphausiids. In, Advances in marine biology, Vol. 18, edited by J.H.S. Blaxter, F.S. Russel & M. Yonge, Academic Press, London. Parsons, T.R., Y. Maita & C.M. Lalli, 1984. A manual ofchemical and biological methodsfbr seawater analysis. Pergamon Press, Oxford. Pechen’-Finenko, G.A. & T.V. Pavlovskaya, 1975. Comparative importance of detritus and algae in the food of Neomysis mirabilis. Hydrobiol. J., Vol. 11, pp. 28-33. Peters, R.H., 1984. Methods for the study of feeding, grazing and assimilation by zooplankton. In, A manual on methods jbr the assessment of secondary productivity, edited by J.A. Downing & F.H. Rigler, Blackwell Scientific Publications, Oxford, pp. 336-412. Robertson, J.R., 1983. Predation by estuarinc zooplankton on tintinnid ciliates. Estuarine Coastul Shelf: Sci., Vol. 16, pp. 27-36. Schoener, T.W., 1974, Resource partitioning in ecological communities. Science, Vol. 185, pp. 27-39. Sieburth, J. McN., V. Smetacek &J. Lenz, 1978. Pelagic ecosystem structure: Hetcrotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr., Vol. 23, pp. 12561263. Siegfried, C.A. & M.E. Kopache, 1980. Feeding of Neomysis mercedis (Holmes). Biol. Bull., Vol. 159, pp. 193-205. Strathmann, R.R., 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceunogr. Vol. 12, pp. 411-418. Talbolt, M.M.B., G.C. Bate & E.E. Campbell. 1990. A review of the ecology of surf-zone diatoms, with special reference to Anaulus australis. Oceanogr. Mar. Biol. Annu. Rev., Vol. 28, pp. 155-175. Vanderploeg, H.A. & D. Scavia, 1979a. Calculation and use of selectivity coefficients of feeding: zooplankton grazing. Ecol. Model., Vol. 7, pp. 135-149. Vanderploeg, H.A. & D. Scavia, 1979b. Two electivity indices for feeding with special reference to zooplankton grazing. J. Fish. Res. Board Cum Vol. 36, pp. 362-365. Webb, P. & T.H. Wooldridge, 1989. Diet elucidation: Supplementary inferences from mysid feeding appendage morphology. S. ,4fr. J. Zool., Vol. 24, pp. 106-109. Webb, P., R. Pcrissinotto & T.H. Wooldridge, 1987. Feeding of Mesopodopsis slabberi (Crustacca, Mysidatea) on naturally occurring phytoplankton. Mar. Ecol. Prog. Ser., Vol. 38, pp. 115- 123. Wittmann, K.J., 1992. Morphogeographic variations in the genus Mesopodopsis Czerniavsky with descriptions of three new species (Crustacea, Mysidacea). Hydrobiologia, Vol. 241, pp. 71-89.
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Wooldridge, T. & C. Bailey, 1982. Euryhaline zooplankton of the Sundays estuary and notes on trophic relationships. S. Afr. J. Zool. Vol. 17, pp. 151-163. Wooldridge, T. & T. Erasmus, 1980. Utilization of tidal currents by estuarine zooplankton. Estuarine Coastal Mar. Sci., Vol. 11, pp. 107-114. Wooldridge, T.H. & P. Webb, 1988. Predator-prey interactions between two species of estuarine mysid shrimps. Mar. Ecol. Prog. Ser., Vol. 50, pp. 21-28.
ELSEVIER
of Experimental Marine Biology and Ecology 188 (1995) 243-259
Feeding of two mysid species on plankton South African estuary
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
in a temperate
H. L. Jerling”, T. H. Wooldridge Department of Zoology and Institute for Coastal Research, University of Port Elizabeth. P.O. Box 1600, Port Elizabeth 6000, South Africa Received
23 June 1994; revision received 5 December 1995; accepted 19 December
Abstract sympatric mysid species, Mesopodopsis wooldridgei and Rhopalophthalmus terranatalis, dominate mesozooplankton biomass in the Sundays River estuary, South Africa. This study aimed to investigate the food and feeding rates of the two mysids on naturally occurring phytoplankton and microzooplankton assemblages, and on copepod instars, using laboratory based feeding and predation experiments. Maximum clearance rates calculated for different size classes of M. wooldridgei on microplankton were on average 34.2, 15.8 and 18.6 ml.ind-i.h-’ for adults, immatures and juveniles respectively. For the same R. terranatalis size classes clearance rates were 8.5, 13.0 and 13.5 ml’ind-‘.h-’ respectively. Thus, all size classes of the smaller M. wooldridgei had higher maximum clearance rates compared to any of the stages of the larger R. terranatalis, indicating that the former species fed more successfully on phyto- and microzooplankton and that these prey assemblages probably constitute the lower limit of the food particle size range consumed by the latter species. R. terranatalis is more successful in preying on larger plankton such as adult copepods and juvenile mysids. Microzooplankton was generally more important in mysid diet than phytoplankton. Apparent selection for microzooplankton species was probably due to an inability to feed efficiently on the smaller phytoplankton cells. Copepod nauplii were readily consumed by all mysid size classes. Predation rates, in terms of weight specific carbon ingestion, increased linearly with copepod instar prey concentration. Two
Keywords:
Estuary;
Feeding;
Mysids;
Plankton;
* Corresponding author. Present address: Department X1001, Kwadlangezwa, 3886, South Africa. Elsevier Science B.V. SSDI 0022-098 1(95)00007-O
South Africa
of Zoology,
University
of Zululand,
Private
Bag
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I88 11995) 243-259
1. Introduction Mysids live in a large variety of aquatic habitats and exploit a diversity of food sources very successfully (Mauchline, 1980). They are generally considered to be omnivorous, although herbivory, in the form of phytoplankton (Bowers & Grossnickle, 1978; Webb et al., 1987) or carnivory (Cooper & Goldman, 1980; Johnston & Lasenby, 1982; Fulton, 1982; Wooldridge & Webb, 1988) have been reported for some species. There is currently a paucity of data on potential feeding of mysids on microzooplankton. Species sharing the same habitat may rely on differences in the utilization of food resources to avoid competition (Schoener, 1974). Two co-existing mysid species, Mesopodopsis wooldridgei (previously M. slabberi, Wittmann, 1992) and Rhopalophthalmus terranatalis, dominate mesozooplankton biomass in the Sundays River estuary, South Africa (Wooldridge & Bailey, 1982). Comprehensive descriptions of this estuary are given in Wooldridge & Bailey (1982), Hilmer & Bate (1990) and Mackay & Schumann (1990). Although Wooldridge & Webb (1988) reported evidence of spatial separation of both species, especially between juvenile M. wooldridgei and adult R. terranatalis, overlap in spatial and temporal distribution occurs in the middle estuarine reaches (Jerling & Wooldridge, 1995) which may lead to resource partitioning. Wooldridge & Bailey (1982) suggested that a major part of the foodweb in the Sundays River estuary was centred in the water column. Due to their relatively large size mysids would be amongst the top predators of the mesozooplankton in this planktonic foodweb with phytoplankton, microzooplankton and copepod instars as potential prey. The feeding of M. wooldridgei on two diatom species which dominate surfzone phytoplankton assemblages along the Sundays River beach (Talbolt et al., 1990) was studied by Webb et al. (1987). These two diatom species do not occur in estuaries. Instead, estuarine phytoplankton was dominated by an entirely different community, mainly composed of flagellates (Jerling & Wooldridge, 1995). Previous studies on R. terranatalis feeding were restricted to predation on juveniles of M. wooldridgei and adults of the copepod Pseudodiaptomus hessei in the Sundays River estuary (Wooldridge & Webb, 1988). However, the abundant phyto- and microzooplankton of the water column in the estuary may also contribute significantly to the diet of R. terranatalis, especially for the smaller size classes. Copepod nauplii formed a significant and consistent food item in the diet of Mysis relicta in Lake Michigan (Bowers & and Vanderploeg, 1982). Since copepod nauplii were highly abundant in the water column of the Sundays (Jerling & Wooldridge, 1991; Jerling & Wooldridge, 1995) they would also be readily available as a food source for mysids. This study aimed to investigate, using laboratory based feeding and predation experiments, whether phytoplankton, microzooplankton and copepod instars (nauplii and copepodid stages) formed significant components in the diet of any of the different developmental stages of M. wooldridgei and R. terranatalis.
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245
2. Methods 2. I. Feeding experiments on phyto- and microzooplankton Mysids and water samples containing natural assemblages of phyto-and microzooplankton were collected at night from the middle reaches of the Sundays estuary (salinity 20-25%,). All samples were transported to the laboratory where they were maintained overnight in 20-l containers at the same temperature from which they were collected (18 ‘C). Experiments commenced the next day. Water samples were filtered through a 90 pm sieve to remove any copepod instars that may have been present. Mysids used as predators were first sorted into three functional groups: adults (secondary sexual characteristics fully developed, R. terranatahs - z 15-18 mm, M. wooldridgei - G 8- 10 mm), immatures (secondary sexual characteristics not fully developed, mm) and juveniles (no sexual R. terranatalis - z S- 10 mm, M. wooldridgei - ~6-7 distinction possible, R. terranatalis - ~4-6 mm, M. wooldridgei - z 2-4 mm) (Mauchline, 1980; Wooldridge & Bailey, 1982). Experimental feeding rates have been shown to be suppressed when conducted in small containers (Peters, 1984). A preliminary experiment, using R. terranatalis adults as predators feeding on rotifers and microciliates, indicated an increase in filtration rate with container volume which tapered off at a container size of 500 ml (Fig. 1). In this experiment predator density was kept constant at 1 mysid per 50 ml and only the volume of estuarine water in the feeding containers increased. The experimental procedure was similar as that described below. Assuming a similar response to container volume in M. wooldridgei, the minimum volume used in the final experiments was 500 ml for both species. Adults of both species as well as immature R. terranatalis (similar in size to adult M. wooldridgei), were placed in buckets containing 1 1 of estuarine water. Containers of 500 ml capacity were used for all other mysid size classes. Five adults (males and females mixed, gravid females were not used), or 10 individuals representing smaller mysid classes were introduced as predators into experi16 ,:... '."'.....,.,,,' ,:' ,:' . ,:' ,:' ,:' ,:' ,:' . .... . :' ,.: .:' . ..~'~"".......,.. ,,,,
14 12 i 2
lo-
i v
a-
5 E ii
6-
...-~~,,r,,..._....~~'~"~ , .:. ,.: ..' ,..'
4'X. 2 A' ......
0 , 25
.... ,_..,......:~.~.;::“:~~” I I 50
Feeding
100
container
I
I
500
volume
.
1000
(ml)
Fig. 1. The effect of container size on clearance rates for adult R. terrunatalis feeding on rotifers microciliates (m). Dotted lines connect the average values of duplicate runs.
(A) and
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mental buckets. This represented mysid densities up to twice that of the maximum densities recorded in the field (Wooldridge & Bailey, 1982; Wooldridge & Webb, 1988). Containers were not sealed and rotated since prey species were motile (rotifers, ciliates and the various flagellates). Three to five replicates were run for each mysid size class. Three sub-samples (30 ml each) of the estuarine water used in experiments were preserved with 1 y0 acid Lugols (Parsons et al., 1984) at the start of each experimental run in order to establish initial phyto- and microzooplankton concentrations. Mysids were allowed to feed overnight for 13 h. In addition, three control containers from which mysids were excluded were treated in the same manner as experimental containers. At the end of the feeding period live mysids were counted. The concentration of phyto- and microzooplankton present at the beginning and after the 13 h feeding period was established with the aid of an inverted microscope, using the Utermiihl technique according to the recommendations by Hobro & Willen (1977). Flagellates, dinoflagellates and ciliates were divided into separate size groups based on morphology and size (Table l), using the terminology suggested by Sieburth et al. (1978): These groups were nanoplankton (2-20 pm) and microplankton (20-200 pm), All dinoflagellates were classified as phytoplankton and all ciliates were assumed to belong to the microzooplankton. Two categories within the microciliate group were recognized: microciliates and large microciliates (Table 1). Prey size (length and width) within each category was measured using an eyepiece micrometer. At least 10 individuals representing each prey category were measured. These measurements were used to construct scale models from clay enabling average volume of each prey category to be calculated. Flagellate and dinoflagellate carbon content was estimated from Log C= - 0.460 + 0.866(log V) (Strathmann, 1967), where C is the carbon content (pg) and V the cell volume (pm3). Rotifer dry mass was considered to be 10% of wet mass (assuming a density of 1.0) (Bottrell et al., 1976). Ciliate volumes were converted to dry mass using the factor 0.17 pg.prn-” (Laybourn & Finlay, 1976). Carbon content of rotifers and ciliates was assumed to be 40% of dry
Table 1 Length (pm) and estimated in the feeding experiments Prey
volume (pm3) of phyto- and microzooplankton
Abbreviation
Length
WI (E)
8.7 17.4 17.4 29.0
(1.7) (2.8) (2.7) (2.5)
215 567 1664 8715
11.6 26.1 33.1 54.0 59.9
(5.1) (8.1) (3.4) (3.8) (7.5)
798 7534 3098 42956 103236
WV
(PDF) W)
(PC) WV (PC*) (R) SD = one standard
deviation,
present as prey species for mysids
II = 10, P = phytoplankton,
M = microzooplankton
(SD)
Volume
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
241
mass, a conversion factor generally used for zooplankton (e.g. Robertson, 1983; Lampert, 1984; Gifford & Dagg, 1988). Mysids were measured along the dorsal midline from the anterior margin of the carapace to the tip of the telson, excluding spines. Measurements were done using a stereo dissecting microscope fitted with an eyepiece micrometer. Dry mass was calculated using length to dry mass relationships (Wooldridge & Bailey, 1982). Carbon content was assumed to be 40% of dry mass (Wooldridge, unpubl. data). The term clearance rate, indicating the volume of ambient medium from which cells are completely removed by mysids, will be used in this study. Clearance rate is synonymous with volume swept clear, filtering, filtration or grazing rates (Frost, 1972; Peters, 1984). Clearance rates, F (mleind-‘.h-‘) and ingestion rates, I (cells.ind-‘.h-‘) were calculated using the equations of Frost (1972). These equations incorporate changes in prey abundance in the control containers due to cell growth. Using the carbon estimates described above, carbon ingestion rates CI (ngeind-‘.h-‘) could be calculated. Care should be taken when estimating feeding rates, not to work over the incipient limiting level of food particle concentration (Peters, 1984), where animals pass from a concentration where ingestion rate is constant to one where clearance rate is constant. From the literature this concentration seems to lie between 1 and 10 ppm (v/v) (Peters, 1984). In this study the concentrations of individual prey groups were all below 1 ppm, with the highest concentration attributed to rotifers (Z 0.3 ppm v/v). 2.2. Predation on copepod nauplii and copepodid stages Predation on natural assemblages of nauplii and copepodids was determined for juvenile, immature and adult R. terranatalis and M. wooldridgei. Prey groups were collected in the estuary using a modified WP2 net fitted with 90 pm mesh during daylight hours. Due to the demersal behaviour of the adult copepods (Grindley, 1972) samples collected in the water column contained predominantly nauplii and copepodids of the calanoid copepods Acartia longipatella and P. hessei. The samples collected with the plankton net were carefully introduced into a container holding 20 1 of estuarine water. This provided a relatively concentrated mixture of copepod nauplii and copepodids for experimental purposes. Two to five subsamples were removed from this concentration with a 5 ml wide-bore (8 mm diameter) pipette and a 20 ml Perspex tube (after gentle mixing). Samples were introduced into 5 1 experimental feeding buckets containing 2 1 estuarine water to provide prey assemblages at various concentrations for mysid predators. On average, copepod nauplii and copepodid stages contributed between 5 and 60 pg*l-’ to the zooplankton carbon during the year in the estuary (calculated from unpublished data). Experimental prey carbon concentrations spanned this range, in most cases, and maximum concentrations were in some cases more than double the average field concentrations. Water volumes in the feeding buckets corresponded to those used by Wooldridge & Webb (1988). All experiments were conducted at ambient summer temperatures ranging between 20 and 25 o C. Five adult, 10 immature or 15 juvenile M. wooldridgei were added to experimental containers. Corresponding numbers for the R. terranatalis size classes were 3, 5 and
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H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. I88 (1995) 243-259
10, respectively. Adult and immature densities were similar to those used by Wooldridge & Webb (1988). Predators were allowed to feed for 24 h before termination of experiments. Ambient light was dimmed by covering experimental buckets with opaque plastic lids. Three replicate experiments were conducted at each prey concentration. Three subsamples representing each experimental prey concentration were preserved before the start of each experimental run to determine initial concentrations. Two control buckets without predators were treated in a similar way at each experimental concentration. At the end of each 24 h experimental run, predators were checked for condition and any dead mysids were ignored for calculation purposes. Formalin was added (Z 10% final concentration) to experimental containers, preserving remaining prey animals. Prey preserved in this manner were carefully sieved out and counted. Nauplii and copepodids of A. longipatella were counted separately. Adults of this species were sometimes present and these were also counted separately. Nauplii of P. hessei were divided into two groups representing developmental stages N2-N4 and N5-N6, respectively. Copepodids of P. hessei consisted entirely of stages Cl-C3 since the prey were collected during daylight hours in near-surface waters. Predator length was measured using an eyepiece micrometer of a dissecting microscope. Animals were measured from the anterior margin of the carapace to the end of the telson, excluding spines. Mysid dry mass was determined using length-mass equations (Wooldridge & Bailey, 1982). The dry mass of nauplii and copepodids was estimated from published as well as from unpublished data (Wooldridge & Bailey, 1982; Jerling & Wooldridge, 1991). Carbon content of prey was assumed to be 40% of dry mass. Predation rate was calculated as the number of prey consumed per predator per day. Using predation rate and predator dry mass the mass specific carbon ingestion rate was expressed as FgC ingested.(mg predator dry mass))‘.day -‘. Electivity indices Ei* (Vanderploeg & Scavia, 1979b) were calculated from predation rates [ = feeding rate (Gi), Vanderploeg & Scavia, 1979a] to determine possible selection for nauplii or copepodid prey.
3. Results 3.1. Feeding on phyto- and microzooplankton Composition of phyto- and microzooplankton in the estuarine water used in the feeding experiments is indicated in Fig. 2. Potential prey organisms ranged from = 9 pm (nanoflagellates) to 60 pm (rotifers) in length (Table 1). Nanoflagellates were the most abundant of all groups present in the water; microdinoflagellates contributed most to total phyto- and microzooplankton carbon (Fig. 2). Other important contributors to phyto- and microzooplankton carbon were nanoflagellates, microciliates and rotifers. No predator mortality occurred during the feeding experiments. Although nanoflagellates were the most abundant prey group, they were not predated upon by M. woold-
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 350
-
300
-
250
-
200
-
249
25
20 L
q
Ei = : -0 sj Q 0
15
: 0
3
150-
10
100
-
50
-
7
5
o-
0 nF
E
-Phytoplankton-
nDF
nC
/JC
/JZF
(AC*
R
--Microzooplankton-
Prey Fig. 2. Abundance (open bars) and carbon contribution (shaded bars) of microplankton in the estuarine water used in feeding experiments. Refer to text (Table 1) for prey abbreviation and ranking.
ridgei (Fig. 3). Most of the other phytoplankton groups present in the estuarine water were consumed by juvenile M. wooldridgei, although at a relatively low rate (generally less than 5 ml.ind-‘.h-‘). Immature and adult M. wooldridgei only consumed microdinoflagellates in the phytoplankton category. All three size classes consumed microzooplankton, with each class showing increasing clearance rates with increasing prey size. Clearance rates were maximal for rotifers, the calculated average values being 34.2, 15.8 and 18.6 ml.ind-‘.h-’ for adults, immatures and juveniles, respectively. Clearance rates for adults were in general double the values calculated for juvenile and immature mysid classes (Fig. 3). Rotifers also contributed most to phyto- and microzooplankton carbon ingested by M. wooldridgei, the calculated averages being 228.7, 45.5 and 47.5 ngind-‘.h-’ for adult, immature and juvenile mysids respectively (Fig. 3). Phytoplankton was not extensively utilized as a food source by adult and immature R. terrunatalis (Fig. 4). Consumption of nanoflagellates by adults was evident, but the calculated clearance rate was low (< 1 ml.ind-‘.h-‘) with a large variation between replicates. Juveniles fed on most of the phytoplankton categories although clearance rates were low (< 5 mlind-‘.h-‘). The microzooplankton component was predated upon by all R. terrunatulis size classes. Rotifers formed the most important component, with clearance rates of (8.5, 13.0 and 13.5 ml*ind-‘.h-’ for adult, immature and juvenile mysids respectively) (Fig. 4). Other microzooplankton prey categories were cleared at rates below 5 ml.ind-‘.h-’ by all mysid classes. Rotifers also formed the most important source of carbon for all R. terrunatalis classes (77.9,71,5 and 42.0 ngC*ind-‘.h-’ for adults, immatures and juveniles respectively) (Fig. 4). Contribution by other microplankters to ingested carbon was below 20 ngeind-‘.h-’ for all R. terranatalis instars. Means of the total phyto- and microzooplankton carbon ingested by the three mysid size classes (Table 2) and mysid biomass were used to calculate the weighted carbon ingestion rate for both prey groups (Fig. 5). Microzooplankton contributed on average
250
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 Mesopodopsis 50 -
40
woofdridgei -
Adults
300
- 250
-
- 200 30 - 150 20 - 100 10 -
- 50
I-0
o-
25 -
52
Immatures
20 = ‘L G ; TI .c
15-
g
lo-
IL cl
5-
0
o-
25 -
52
Juveniles
42
31
21
10
0 nF
E
nDF
-Phytoplankton-
uDF
nC
I
I
PC
jG!F
I
MC’
I
R
--Microzooplankton-
Prey Fig. 3. Clearance rates (open bars) and carbon ingestion rates (shaded bars) calculated for the three M. wooldridgei size classes. Refer to text (Table 1) for prey abbreviation and ranking. Vertical lines = 1 SD; n = 4.
more than 70% to the total phyto- and microzooplankton carbon ingested by all classes of both mysid species (Fig. 5). Phytoplankton contributed on average ~20% to the
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
251
Rhopalophthalmus terranatalis 12 -
Adults
10 -
a60 640 420 2-
0
o-
20
60
lmmaturer
T 70
q
60
Q
50
s
40
0 g P
30
2
20
-? ,’
10 0
0
50
20
40 15
30 10 20
5 10
0
0 nF
E
nDF
-Phytoplankton-
I
I
I
I
nC
PC
pZF
I
PC+
I
R
-Microzooplankton-
Prey Fig. 4. Clearance rates (open bars) and carbon ingestion rates (shaded bars) calculated for the three R. terranatalis size classes. Refer to text (Table 1) for prey abbreviation and ranking. Vertical lines = 1 SD; n = 3 for adults and 4 for immatures and juveniles.
total carbon ingested by juveniles of both species, 10 to 15% of carbon ingested by immature and adult A4. wooldridgei, and less than 10% of carbon ingested by imma-
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
252
Table 2 Mean (x) phyto- and microzooplankton mysid size classes Mysid
carbon
ingestion
rates (ngC.ind
‘,h
Microrooplankton
Phytoplankton
I) calculated
for the various
Mann-Whitney
,Z
P x
SD
x
SD
M. wooldridgei Adult Immature Juvenile
39.2 13.4 14.1
57.1 22.9 15.9
275.3 78.3 66.3
52.6 25.1 29.6
4 4 4
0.03 0.06 0.06
R. terranatalis Adult Immature Juvenile
10.1 5.9 16.2
14.3 10.2 28.0
98.3 65.7 59.3
6.3 39.1 15.4
3 4 4
0.08 0.12 0.18
SD = one standard deviation. Probability (p) of no difference ingested was determined using the Mann-Whitney test.
between phyto- and microzooplankton
carbon
ture and adult R. terranatalis (Fig. 5). Carbon ingestion rates increased with increasing body size of mysids as expected (Figs. 3 and 4), but weight specific carbon ingestion decreased with increasing developmental stage (Fig. 5). Due to the high variations in the total phyto- and microzooplankton ingestion rates (indicated by the large standard deviations, Table 2) the differences between amounts of phyto- and microzooplankton carbon ingested were generally not statistically sigMesopodopsis 1200
Rhopalophthalmus
wooldridgei Adults
terranatalis
Adults
900 i-
600
4
300
i P
0
0+
1200
I: ? .g
900
;:
300
P
25 i-
rl
0’
-I
el
-
Immature5
lmmaturcs
600
0
Juveniles
I Phytoplankton
Microzooplankton
Phytoplankton
Microzooplankton
Fig. 5. Weight specific phytoplankton and microzooplankton carbon ingested by the three size classes of M. wooldridgei and R. terranatalis. Vertical lines = 1 SD; II = 3 for adult R. terranatalis and 4 for other size classes.
253
H.J. Jerling. T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259 Mesopodopsis
Rhopalophthalmus
wooldridgei
1
Adults
1
-
terranatalis
Adults I
0.5
0.5 ..U
0.0
I
0.0
I
Tz w
0.5 -
-0.5 1 W
-
. ...?
1
0.5
.G 0.0 g
1
-1
o-o.5 2 W -1
.
-1 1
I
1
lmmaturar
-
1
-1
1
.r”o.o .g
I
-0.5
1 I
-1 c w
I
I
-0.5
.
1 1
‘i’
I
1
Juveniles
.
0.5
0.5
6
,
0.0 -0.5
,
.
I
-0.5
I
nF
E
,
nDF
0
1
-I*
-1 I
.
0.0
,
I
nC
-Phytoplankton-
I
&IC
I
PZF
MC+
I
I
R
nF
-Microzooplanktan-
I
E
I
nDF
I
vDF
-Phytoplankton-
I
nC
PC
of M. wooldridgei and ranking and abbrevia-
nificant (Mann-Whitney test, Table 2). Only adults of M. wooldridgei showed icant difference at CI= 0.05. Differences between phyto- and microzooplankton
80
Rhopalophrhalmus
wooldridgei
Adults
-I
PC*
--Microzooplankton-
Fig. 6. Electivity indices calculated from clearance rates for the three size classes R. terranatalis feeding on microplankton. Refer to text (Table 1) for microplankton tion.
Mesopodopsis
I
@F
a signifcarbon
&sranstalis
Adults
-I
lmmaturer
u n
60
Juveniles
1
AN
PNa
PNb
Juveniles
1
AC
PC
AA
AN
PNa
PNb
AC
PC
AA
Fig. 7. Composition of prey during mysid predation experiments. Acartia longipatella: AN = nauplii, AC = copepodids, AA = adults. Pseudodiaptomus hessei: PNa = nauplii N2-N4, PNb = nauplii N5-N6, PC = copepodids. Prey ranked according to size. *, Not present in feeding containers.
7
R
254
H.J. Jerling, T.H. Wooldridge 1 J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
ingested by immatures and juveniles of this species and adults of R. terranatalis were marginally significant at a = 0.10. For immatures and juveniles of R. terranatulis differences were not significant (R = 0.20 and 0.15, respectively). Electivity indices Ei* (Fig. 6) (Vanderploeg & Scavia, 1979b) calculated from the clearance rates, clearly indicate selection for the largest microzooplankton category for all classes of both mysid species. For all instars there is also a trend suggesting a preference for increasing prey sizes. None of the mysid instar groups selected for the phytoplankton species. 3.2. Predation on nauplii and copepodids No predator mortality occurred during the feeding experiments. Prey abundance during the experimental runs did not change in control chambers. The most abundant i
25
-0
1
Mesopodopsis
wooldridgei
25
50
Prey -
25
-
i9 i
CR 20
75
cont.
100
125
150
(pgC.I-‘I
Rhopalophthalmus terranatafis
Y = 0.15% - 0.317
-
6
0
25
50
75
Prey cont.
100
125
150
IpgC.I-‘I
Fig. 8. Weight specific predation rate in terms of carbon ingestion for M. wooldridgei and R. ferranntnlis size classes. Adults (O), immatures (H), Juveniles (A). For R. ferranatali.r juveniles, experiments were run at Only two prey COnCCntratiOnS. VCrtiCd h?S = 1 SD; n = 3.
H.J.
Jerling,
T.H.
Mesopodopsis
-1
Mar. Biol. Ecol. 188 (1995)
wooldridgei
'1
r
Wooldridge / J. Exp.
'1
Adults
J
I
1 1
r w
t.............. *
I
* I
-1. j) AN
.
.I .
I
~
i
1
I
1 1
*
.
Juveniles
0.5 ._............
I
I
I
-1
Juveniles
.! ,..,,..,_..,.! I
-0.5
Lo.5 0 w
1
.
lmmatursr
1
0.5
E 0.0 2
L .... ........ .. ’
1
._
terranatalis
Adults
-1 J
I
lmmaturss
ET 0.5
Rhopalophthalmus
255
243-259
f
,
0.0 .
#
#
.
,
PNa
PNb
AC
PC
I
I
.
*
*
.
AC
PC
I
-0.5 ( AA
.
-1 AN
PNa
PNC
a
I AA
Fig. 9. Electivity indices calculated for size classes of M. wooldridgei and R. terranatalis feeding on copepod instars. Acartia longipatella: AN = nauplii, AC = copepodids, AA = adults. Pseudodiaptomus hessei: PNa = nauplii N2-N4, PNb = nauplii NS-N6, PC = copepodids.
category present was P. hessei nauplius stages N2-N4 (Fig. 7). Acartia longipatella nauplii and copepodid stages were not represented in feeding chambers when experiments using adult R. terranatalis were undertaken. Weight specific predation rate increased with increasing prey concentration (Fig. 8). The rate of increase was linear for all mysid instars and did not taper off at the highest prey concentrations investigated. The trend towards higher weight specific carbon ingestion rates by smaller predator size classes was more pronounced for M. wooldridgei than for R. terranatalis. The carbon ingestion rate by juvenile and immature classes of the latter species did not differ significantly. Adult mysids showed a decreasing trend in prey selection with increasing prey size (Fig. 9), suggesting preference for smaller prey (nauplii). As the preferred prey were also the most abundant (Fig. 7), this observation may also reflect an opportunistic feeding strategy. Immatures and juveniles, particularly of M. wooldridgei, showed a large scatter in the calculated electivity indices with no persistent selection for any prey group.
4. Discussion The use of natural prey assemblages in feeding experiments using cell counts may pose several difficulties with respect to methodology (Peters, 1984) and interpretation of results. However, the method is more representative of events in the field compared to monospecific food cultures or artificially composed food assemblages and can provide valuable insight into selective feeding on different phyto-and microzooplankton components (e.g. Gifford & Dagg, 1988).
256
H.J. Jerling, T.H. Wooldridge / J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
Temporal and spatial distribution and composition of the phyto- and microzooplankton in the Sundays River estuary changes rapidly. Hilmer & Bate (1990), for example, showed that chlorophyll-u concentration fluctuated over both diurnal and spring-neap cycles. No clear seasonal pattern in phyto- and microzooplankton distribution was evident (Jerling & Wooldridge, 1995). Phyto- and microzooplankton composition in the present study can thus be considered as representative of general phytoand microzooplankton assemblages in the estuary. However, phytoplankton densities were comparatively low and did not represent bloom densities (Hilmer & Bate, 1991; Jerling & Wooldridge, 1995). Detritus was not quantified in the present study, it may however contribute significantly to the organic content of the water column. Although detritus was less significant in the nutrition of the mysid Neomysis mirubilis compared to living algae (Pechen’Finenko & Pavlovskaya, 1975), detritus is known to contribute significantly to the diet of other mysid species (Lasenby & Langford, 1973; Foulds & Mann, 1978; Mauchline, 1980; Johnston & Lasenby, 1982; Webb & Wooldridge, 1989). In the present study only the more abundant prey organisms in the water column were quantified, leading to a possible under-estimation of total carbon ingestion by the species investigated. The increase in maximum clearance rates with increasing size class in M. wooldridgei contrasts with the decrease observed in R. terrunatalis. All M. wooldridgei size classes also had higher maximum clearance rates compared to the corresponding classes of the larger R. terranatalis, indicating that the former species feeds more successfully on phyto- and microzooplankton. Microzooplankton probably constitutes the lower limit of the potential food particle size range consumed by R. terranatulis. Present results indicate that when microzooplankton abundance is relatively high (as was the case in this study), it forms a more important component in the diet of both mysids compared to phytoplankton. Apparent selection for microzooplankton species is probably due to less efficient feeding on the small phytoplankton cells. Extensive feeding of M. wooldridgei on surf zone phytoplankton was reported by Webb et al. (1987). These diatoms were however relatively large (cells 58 pm in length, but larger colonies also formed) and were comparable in size to the larger microzooplankton species in this study. Webb et al. (1987) also mention selection for the larger cell colonies. Siegfried & Kopache (1980) came to the conclusion that the selectivity patterns of mysids ingesting phytoplankton represent capturability based on size rather than true preference. The predation rate when feeding on copepod instars increased linearly with increasing prey concentration and did not taper off at the highest prey concentrations. Similar results were reported in other studies of mysid predation on zooplankton (Fulton, 1982; Wooldridge & Webb, 1988). ‘The highest copepod instar concentrations in the present predation study were more than double that of recorded field densities. A substantial decrease in prey concentration in the containers, after predation, allowed, however, for the calculation of a linear response over the 24 h feeding period even at high prey concentrations. Fulton (1982) noted that the response should in some way be non-linear and Wooldridge & Webb (1988) reported a curvilinear response when clearance rates instead of predation rates were used. Preferential feeding by mysids on nauplii compared to copepodids was probably due
H.J. Jerling, T.H. Wooldridge /J. Exp. Mar. Biol. Ecol. 188 (1995) 243-259
251
to the high abundance of the former in the plankton. With a relatively high abundance of copepod nauplii in the water column, larger mysid instars would benefit more by relying on this food source. Copepodids constituted a small percentage of the plankton prey assemblages in the predation experiments, an artefact introduced by collecting prey during day times. Vigor of the escape response by prey species will also limit the feeding efficiency of mysid predators on larger instars (Grossnickle, 1982). Nauplii seem to be more readily available to mysids, by having a less effective escape response when compared to copepodid stages. This finding is in contrast to that of Siegfried & Kopache (1980) who suggested that nauplii are better able to avoid the mysids’ feeding current than copepodid stages. Observations made during this study did not support their postulation. Even though nauplii seem to be readily exploitable prey item for mysids, their relatively small size may limit their availability to the large adults of R. terrunatalis. Adult R. terranatulis do not undergo a general vertical migration into surface waters but remain near the bottom (Wooldridge & Erasmus, 1980). Copepodids, on the other hand, are known to be demersal (Grindley, 1972) and more abundant in bottom waters during day time and will be more readily available as prey to adult R. terrunatalis than nauplii which occupy surface waters in higher densities. Adult R. terranatalis also readily consume juvenile M. wooldridgei (Wooldridge & Webb, 1988) which contribute significantly to its diet.
Acknowledegments Financial assistance by the Department of Environmental Venture Programme and the University of Port Elizabeth
Affairs, the Estuarine Joint is gratefully acknowledged.
References Bottrell, H.H., A. Duncan, Z.M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norw. J. Zool., Vol. 24, pp. 419-456. Bowers, J.A. & N.E. Grossnickle, 1978. The herbivorous habits of Mysis relicta in Lake Michigan. Limnol. Oceanogr., Vol. 23, pp. 161-776. Bowers, J.A. & H.A. Vanderploeg, 1982. In situ predatory behavior of My& relicta in Lake Michigan. Hydrobiologia, Vol. 93, pp. 121-131. Cooper, S.D. & C.R. Goldman, 1980. Opossum shrimp (Mysis relicta) predation on zooplankton. Can. J. Fish. Aquat. Sci., Vol. 37, pp. 909-919. Foulds, J.B. & K.H. Mann, 1978. Cellulose digestion in Mysis stenolepis and its ecological implications. Limnol. Oceanogr., Vol. 23, pp. 760-766. Frost, B.W., 1972. Effects of size and concentration of food particles on the feeding behaviour of the Marine Planktonic Copepod Calanus pa#icus. Limnol. Oceanogr., Vol. 17, pp. 805-815. Fulton, R.S., 1982. Predatory feeding of two marine mysids. Mar. Biol. Vol. 72, pp. 183-191. Gifford, D.J. & M.J. Dagg, 1988. Feeding of the estuarine copepod Acartia tonsa Dana: carnivory vs. herbivory in natural assemblages. Bull. Mar. Sci., Vol. 43, pp. 458-468. Grindley, J.R., 1972. The vertical migration behaviour of estuarine plankton. Zool. Afr., Vol. 7, pp. 13-20.
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Grossnickle, N.E., 1982. Feeding habits ofMysis relicta - an overview. Hydrobiologia, Vol. 93, pp. 101-107. Hilmer, T. & G.C. Bate, 1990. Covariance analysis of chlorophyll distribution in the Sundays River estuary, eastern cape. Sth. Afr. J. Aquat. Sci., Vol. 16, pp. 37-59. Hilmer, T. & G.C. Bate, 1991. Vertical migration of a flagellate-dominated bloom in a shallow South African estuary. Bat. Mar., Vol. 34, pp. 113-121. Hobro, R. & E. Willen, 1977. Phytoplankton countings. Intercalibration results and recommendations for routine work. Int. Rev. Ges. Hydrobiol., Vol. 62, pp. 805-811. Jerling, H.L. & T.H. Wooldridge, 1991. Population dynamics and estimates of production for the calanoid copepod Pseudodiaptomus hessei in a warm temperate estuary. Estuarine Coastal She!f Sci., Vol. 33, pp. 121-135. Jerling, H.L. & T.H. Wooldridge, 1995. Plankton distribution and abundance in the Sundays River estuary, with comments on potential feeding interactions. S. Afr. J. Mar. Sci. (in press). Johnston, N.T. & D.C. Lasenby, 1982. Diet and feeding of Neomysis mercedis Holmes (Crustacea, Mysidacea) from the Fraser River estuary, British Columbia. Can. J. Zooi., Vol. 60, pp. 813-824. Lampert. W., 1984. The measurement of respiration. In, A manual on methods for the assessment ofsecondaryproductivity, edited by J.A. Downing & F.H. Rigler, Blackwell Scientific Publications, Oxford, pp. 413468. Lasenby, D.C. & R.R. Langford, 1973. Feeding and assimilation of Mysis relicta. Limnol. Oceanogr. Vol. 18, pp. 280-285. Layborn, J. & B.J. Finlay, 1976. Respiratory energy losses related to cell weight and temperature in ciliated protozoa. Oecologia, Vol. 24, pp. 349-355. Mackay, H.M. & E.H. Schumann, 1990. Mixing and circulation in the Sundays River estuary, South Africa. Estuarine Coustal. Shelf: Sci., Vol. 3 1, pp. 203-216. Mauchline, J., 1980. The biology of Mysids and Euphausiids. In, Advances in marine biology, Vol. 18, edited by J.H.S. Blaxter, F.S. Russel & M. Yonge, Academic Press, London. Parsons, T.R., Y. Maita & C.M. Lalli, 1984. A manual ofchemical and biological methodsfbr seawater analysis. Pergamon Press, Oxford. Pechen’-Finenko, G.A. & T.V. Pavlovskaya, 1975. Comparative importance of detritus and algae in the food of Neomysis mirabilis. Hydrobiol. J., Vol. 11, pp. 28-33. Peters, R.H., 1984. Methods for the study of feeding, grazing and assimilation by zooplankton. In, A manual on methods jbr the assessment of secondary productivity, edited by J.A. Downing & F.H. Rigler, Blackwell Scientific Publications, Oxford, pp. 336-412. Robertson, J.R., 1983. Predation by estuarinc zooplankton on tintinnid ciliates. Estuarine Coastul Shelf: Sci., Vol. 16, pp. 27-36. Schoener, T.W., 1974, Resource partitioning in ecological communities. Science, Vol. 185, pp. 27-39. Sieburth, J. McN., V. Smetacek &J. Lenz, 1978. Pelagic ecosystem structure: Hetcrotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr., Vol. 23, pp. 12561263. Siegfried, C.A. & M.E. Kopache, 1980. Feeding of Neomysis mercedis (Holmes). Biol. Bull., Vol. 159, pp. 193-205. Strathmann, R.R., 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceunogr. Vol. 12, pp. 411-418. Talbolt, M.M.B., G.C. Bate & E.E. Campbell. 1990. A review of the ecology of surf-zone diatoms, with special reference to Anaulus australis. Oceanogr. Mar. Biol. Annu. Rev., Vol. 28, pp. 155-175. Vanderploeg, H.A. & D. Scavia, 1979a. Calculation and use of selectivity coefficients of feeding: zooplankton grazing. Ecol. Model., Vol. 7, pp. 135-149. Vanderploeg, H.A. & D. Scavia, 1979b. Two electivity indices for feeding with special reference to zooplankton grazing. J. Fish. Res. Board Cum Vol. 36, pp. 362-365. Webb, P. & T.H. Wooldridge, 1989. Diet elucidation: Supplementary inferences from mysid feeding appendage morphology. S. ,4fr. J. Zool., Vol. 24, pp. 106-109. Webb, P., R. Pcrissinotto & T.H. Wooldridge, 1987. Feeding of Mesopodopsis slabberi (Crustacca, Mysidatea) on naturally occurring phytoplankton. Mar. Ecol. Prog. Ser., Vol. 38, pp. 115- 123. Wittmann, K.J., 1992. Morphogeographic variations in the genus Mesopodopsis Czerniavsky with descriptions of three new species (Crustacea, Mysidacea). Hydrobiologia, Vol. 241, pp. 71-89.
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