Journal of Plankton Research Vol.12 no.3 pp.483-495, 1990 Instar-specific mortalities of coexisting Daphnia species in relation to food and invertebrate predation Wouter Hovenkamp LimnologicalInstitute, Rijksstraatweg 6, 3631 AC Nieuwersluis, The Netherlands Abstract. Instar-specific mortalities of Daphnia hyalina and D.cucullala were studied from May 19 to September 29, 1988 in combination with invertebrate predator and phytoplankton abundance. Simultaneous life-table experiments were conducted under semi-natural conditions in the laboratory to estimate juvenile mortality in a predator-free environment. Juvenile mortality by predation was calculated as the difference between juvenile mortality in the field and in the experiments and was the most important factor for the differences in abundance of the two species. For D.hyalina juvenile mortality was higher in early summer and probably caused by selective predation by Chaoborus flavicans. Predation by Leptodora kindtii was probably more important during the rest of the summer. Estimated mortality by predation adequately explained juvenile mortality, except for a 3- week period in August. Decreasing flagellate densities in July were accompanied by increased juvenile mortalities of D.hyalina and D.cucullata in the life-table experiments in August and coincided with a Daphnia population decrease. Introduction The present study is part of an investigation on the coexistence of Daphnia species in relation to food and predation in Lake Vechten, The Netherlands. A detailed analysis of the instar-specific mortality rates of D.hyalina and D.cucullata in this lake in 1986 showed that juvenile mortality was the main cause for the replacement of D.hyalina (dominant in spring) by D.cucullata (Hovenkamp, 1989). Relatively small differences in juvenile mortality led to small differences in the rates of increase. Nevertheless, these small differences were sufficient to cause large differences in densities of the two species during the summer. Juvenile mortality can be caused by food conditions and by predation, mainly by invertebrates (Neill, 1975; Goulden and Hornig, 1980; DeMott, 1983). Phytoplankton species composition and densities, and size-related fecundities of daphnids indicate food conditions. However, experimental work is needed to quantify juvenile mortality caused by food conditions only. If total juvenile mortality in the lake and in a predator-free environment on natural food can be estimated, the difference between the two will be an estimate of mortality by predation. Mortality by predation is discussed with regard to the observed densities of invertebrate predators and literature data on invertebrate predation rates. Absolute and relative densities of coexisting species can differ greatly from year to year. Nevertheless, similar patterns can often be detected among years (Jacobs, 1977; Seitz, 1980). Therefore it is expected that the same underlying mechanisms are responsible for these patterns. If juvenile mortality was the most important mechanism determining the relative densities of the two species in 1986, one would expect that also in 1988 this pattern of coexistence was mainly determined by differences in juvenile mortalities. The differences in the 483 at McGill University Libraries on October 2, 2012 http://plankt.oxfordjournals.org/ Downloaded from
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Journal of Plankton Research Vol.12 no.3 pp.483-495, 1990
Instar-specific mortalities of coexisting Daphnia species in relationto food and invertebrate predation
Wouter HovenkampLimnologicalInstitute, Rijksstraatweg 6, 3631 AC Nieuwersluis, The Netherlands
Abstract. Instar-specific mortalities of Daphnia hyalina and D.cucullala were studied from May 19 toSeptember 29, 1988 in combination with invertebrate predator and phytoplankton abundance.Simultaneous life-table experiments were conducted under semi-natural conditions in the laboratoryto estimate juvenile mortality in a predator-free environment. Juvenile mortality by predation wascalculated as the difference between juvenile mortality in the field and in the experiments and wasthe most important factor for the differences in abundance of the two species. For D.hyalina juvenilemortality was higher in early summer and probably caused by selective predation by Chaoborusflavicans. Predation by Leptodora kindtii was probably more important during the rest of thesummer. Estimated mortality by predation adequately explained juvenile mortality, except for a 3-week period in August. Decreasing flagellate densities in July were accompanied by increasedjuvenile mortalities of D.hyalina and D.cucullata in the life-table experiments in August andcoincided with a Daphnia population decrease.
Introduction
The present study is part of an investigation on the coexistence of Daphniaspecies in relation to food and predation in Lake Vechten, The Netherlands. Adetailed analysis of the instar-specific mortality rates of D.hyalina andD.cucullata in this lake in 1986 showed that juvenile mortality was the maincause for the replacement of D.hyalina (dominant in spring) by D.cucullata(Hovenkamp, 1989). Relatively small differences in juvenile mortality led tosmall differences in the rates of increase. Nevertheless, these small differenceswere sufficient to cause large differences in densities of the two species duringthe summer.
Juvenile mortality can be caused by food conditions and by predation, mainlyby invertebrates (Neill, 1975; Goulden and Hornig, 1980; DeMott, 1983).Phytoplankton species composition and densities, and size-related fecundities ofdaphnids indicate food conditions. However, experimental work is needed toquantify juvenile mortality caused by food conditions only. If total juvenilemortality in the lake and in a predator-free environment on natural food can beestimated, the difference between the two will be an estimate of mortality bypredation. Mortality by predation is discussed with regard to the observeddensities of invertebrate predators and literature data on invertebrate predationrates.
Absolute and relative densities of coexisting species can differ greatly fromyear to year. Nevertheless, similar patterns can often be detected among years(Jacobs, 1977; Seitz, 1980). Therefore it is expected that the same underlyingmechanisms are responsible for these patterns. If juvenile mortality was themost important mechanism determining the relative densities of the two speciesin 1986, one would expect that also in 1988 this pattern of coexistence wasmainly determined by differences in juvenile mortalities. The differences in the
rates of increase of D.hyalina and D.cucullata should have higher correlationswith differences in juvenile mortalities than with differences in adult mortalities.Instar-specific mortalities were calculated in 1988 and the results will becompared with those obtained in 1986 to test this hypothesis.
Materials and methods
During 1988 zooplankton was sampled from May 19 to September 29 in LakeVechten, a small, mesotrophic lake (surface area 4.7 ha; maximum depth 12 m;mean depth 6 m) near Bunnik, The Netherlands, containing three Daphniaspecies: D.hyalina, D.galeata and D.cucullata. For this study D.hyalina andD.galeata were lumped and denoted as D.hyalina. Samples were taken at threedifferent depths and 12 different sites. All samples of the same depth werepooled and subsampled. Subsamples were counted until at least 100 daphnidswere recorded. The methods for estimating zooplankton population densities,rates of increase [r = (In N2 - In Ni)l(t2 - h)] and birth [b = ln(£ + l)D, whereE is the average number of eggs per animal and D is egg development time indays] and death rates (d = b — r), instar mortalities and their relativeimportances were reported in detail by Hovenkamp (1989), except for someminor modifications, described below.
In 1986 temperatures at 6 and 3 m depth were used to estimate eggdevelopment times of D.hyalina and D.cucullata, because they preferreddifferent water layers. Owing to low summer temperatures, the temperaturedifferences in the epilimnion were less than in 1986 and ovigerous females ofboth species did not show the marked preferences for different depths.Therefore, contrary to 1986, only water temperature at 3 m depth was used toestimate egg development times of both the species. Size frequency distributionswere converted into instar frequency distributions as in 1986 (see Hovenkamp,1989). Results of different growth experiments were used to construct thegrowth curve. Four cohorts of D.hyalina and three cohorts of D.cucullata werecultured at 18°C in 60 u,m filtered lake water from newborn to 3 or 4 week oldbetween June and September. Individual daphnids were cultured in 100 ml testtubes in thermostatically controlled waterbaths at a 16 h light, 8 h dark cycle.Two fluorescent tubes were used for illumination (~3 W m~2). All animals wererecorded for length, eggs or ephippial eggs twice a week when the newbornswere removed and the medium was refreshed. The growth curves of thesecohorts were similar in shape and an average growth curve was used to estimateinstar boundaries.
To assess the importance of the differences in instar mortalities for thedifferences between the rates of increase of the two species, correlations werecalculated between inter-species differences in rates of increase and inter-speciesdifferences in instar mortalities. As in 1986, successive pairs of instars werepooled into instar-classes to facilitate interpretation. Instar classes 4 and 5 werenegligible in numbers during 1988 and calculations include only three instarclasses, of which the first is juvenile.
Besides counting Daphnia in the subsamples, the entire sample was examinedfor Leptodora kindtii. Densities of Chaoborus flavicans were estimatedfortnightly by taking benthic samples at 24 different sites, deeper than 6 m, witha 1 dm2 Ekman bottom grab (Southwood, 1968). The samples were sieved overa 0.5 mm gauze. Prior to the removal of the larvae the debris was pooled forthree bottom zones (6-8, 8-10 and 10 m) and subsampled. From 0 to 6 m thesediment is too sandy to contain any Chaoborus larvae. Subsamples were takenin a 20 1 plastic box which could be divided into two compartments by aremovable part in the middle. The debris was thoroughly mixed and thenhalved. Repeating this procedure once or twice resulted in four or eightsubsamples respectively. Subsamples were counted until at least 60 Chaoboruslarvae were found. The numbers per dm2 of the three zones were multiplied withthe respective surface areas of the three zones to calculate Chaoborus numbers.The length of the head capsule of 25 Chaoborus larvae was measured monthly toassess their stage (Parma, 1969).
Possible predation by Chaoborus and Leptodora was estimated by multiplyingdensities by predation rates. Reported predation rates of fourth instar larvae ofChaoborus are 3.2 prey ind."1 day"1 for Chaoborus flavicans (Dodson, 1970).Predation rates of Leptodora of 4-5 mm length are known to range between 10prey ind."1 day"1 at 10°C and 30 prey ind."1 day"1 at 25-30°C (Mordukhai-Boltovskaya, 1958). A minimal estimate of predation by Leptodora in LakeVechten was made by multiplying Leptodora densities by 10 prey ind."1 day"1.Both Chaoborus and Leptodora prefer prey items in size class <0.75 mm(Mordhukai-Boltovskaya, 1958; Allan, 1973; Cooper and Smith, 1983) soabsolute mortality of Daphnia size class <0.75 mm was compared with theestimated predation. Absolute mortalities of all Daphnia instars <0.75 mm werepooled and compared with estimated loss by predation.
Fortnightly phytoplankton samples were taken at the same depths at whichzooplankton was sampled and fixed with Lugol's solution. The samples werepooled before being counted according to the method of Utermohl (1958) with amagnification of ~300x. The phytoplankton was classified into four groups: (i)flagellates (Chroomonas, Trachelomonas, Cryptomonas ovata); (ii) edible greenalgae and diatoms (Scenedesmus, Ankistrodesmus and mainly centric diatoms);(iii) resistant or inedible algae (Oocystis, Dinobryon, Staurastrum, Tetraedron,Ceratium hirundinella); and (iv) cyanobacteria (Oscillatoria, Lyngbya, Ana-baena).
In the laboratory, life-table experiments were carried out under semi-naturalconditions. The life-table experiments were also used to estimate juvenilemortality in a predator-free environment. Adult daphnids, handled with care,were hardly vulnerable to manipulation for length measurements and eggcounts, but the first instars were easily trapped in the surface layer aftermanipulation. Therefore, survival in the first instar was estimated by comparingegg numbers and the number of juveniles alive at a later measurement. Eggdevelopment time at 18°C is ~3 days and an average egg will develop into anewborn 1.5 days after being observed. The average time between observationswas 3.5 days, and the average age of a newborn was thus estimated to be 2 days.
The instantaneous death rate of the first instar (df) in the absence of predatorswas calculated as
di = (1/2) * [ln(egg no.) - In (no. of juveniles alive)]
Egg and juvenile numbers were summed over 2-week intervals. Egg numbersare difficult to estimate in a full brood pouch and egg counts will be less accuratefor large egg numbers. Therefore egg counts larger than eight and the resultingnewborns were discarded. Degenerate eggs were also excluded. In situinstantaneous mortality during the juvenile period was also calculated forseveral simulated cohorts employing the INSTAR model (Hogeweg andRichter, 1982; Hovenkamp, 1989) in the same periods. Mortality by predation isestimated as the difference between mortality in the field and in the cultures.
Food conditions for Daphnia are hard to quantify by phytoplankton countsonly; therefore food quality and quantity is indirectly assessed by using meanbrood size which was calculated for size classes 0.6-0.8, 0.8-1.0 and 1.0-1.2 mm.
Results
Daphnia populations
The daphnids first appeared in mid-May and both species increased slowly untilJuly 7, after which date densities of D.cucullata exceeded those of D.hyalina(Figure 1A). Both species declined in the first week of August, accompanying anincrease in Secchi depth (Figure 2). At that time flagellates and cyanobacteriawere the most important phytoplankton groups. However, cyanobacteria weremainly concentrated in deeper, usually anaerobic water-layers. Daphnids werepresent only in these water-layers when the oxygen isocline descended and thedominance of cyanobacteria coincided with sampling in these water-layers.Phytoplankton densities, excluding cyanobacteria, show flagellates to be themost important group with peaks in early June and mid July (Figure 3).
Rates of increase, and birth and death rates of both species have a similarpattern during most of the season, except the rate of increase of D.cucullatawhich is constantly higher in June and July (Figure IB). Birth and death ratesdiffered the most between species in late May and in June and August, whenD.hyalina had higher birth and death rates than D.cucullata (Figure 1C and D).Especially in June and July mortality of all instar classes of D.cucullata was muchlower than of D.hyalina (Figure 4). Mortality of instar class 1 of D.hyalina madean important contribution to the population death rate from May to September(Figure 5) but mortality of instar class 1 of D.cucullata was relativelyunimportant in June, July and September.
The correlation coefficients between differences in instar mortalities and inrates of increase were not significant, but the highest negative correlation wasfound for instar class 1 (Table I).
Mean brood size of corresponding size classes of the two species were highly
j I j i rFig. 1. Population densities (A), rates of increase (B), and birth (C) and death (D) rates of D.hyalinaand D.cucullata in Lake Vechten from May to September 1988, graphs smoothed by a three-pointrunning mean.
300
260 _
220 _
§ 160 _
140 _
100
Secchi Disk Depth
M I J I j I A I s
Fig. 2. Secchi disk depth in Lake Vechten from May to September 1988.
Fig. 3. Phytoplankton densities (no. of cells ml *) in Lake Vechten from May to September 1988.
0.
0.
0 .
0.
0.
0.
0 .
0.
0.
0.
10 o.
0
0
0
0
0
0
0
0
0
25
20
15
10
05
00
25
20
.15
10
.05
.00
.40
.35
.30
.25
.20
.15
.10
.05
.00
Instar Class 1
H I J I J I A I s
Instar Class 2
M I J I J
Instar Class 3
A I s I
r i s I
Fig. 4. Instar-specific mortalities of D.hyalina and D.cucullata in Lake Vechten from May toSeptember 1988, graphs smoothed by a three-point running mean.
Fig. 5. Relative mortalities of D.hyalina and D.cucullata in Lake Vechten from May to September1988.
TabJe I. Correlation coefficients between differences in the rates of increase and differences in instar-specific mortalities
Correlation coefficient No. of observations Significance level
Instar class 1Instar class 2Instar class 3
-0.3640.0870.007
191919
0.1260.7230.978
similar in August and September, but during June and July D. cucullata hadhigher egg numbers than corresponding size classes of D.hyalina (Figure 6).
Invertebrate predators
Chaoborus density, which was ~0.12 ind. I"1 in May, decreased steadily to~0.01 ind. P 1 (Figure 7). All Chaoborus larvae were of the fourth instar, head
S i z e c l a s s 0 . 6 - 0 . 8 mmD. hyallnaD. cucullats
M I J I J I T
Size c lass 0.8 - 1.0 mm
\
M I J I J I A
Size class 1.0 - 1.2 mm
Fig. 6. Size-dependent mean brood size of D.hyalina and D.cucullata in Lake Vechten from May toSeptember 1988.
u4J
Population DensityChaobonus flavicans A,
—1 Leptodora kindtii / \
Fig. 7. Population densities of Leptodora kindtii and Chaoborus flavicans in Lake Vechten from Mayto September 1988.
capsules having a length of 1-1.3 mm (Parma, 1969). Leptodora densitiesshowed three peaks, one of —0.2 ind. I"1 in June, one of —0.5 ind. I"1 in Julyand one of —0.45 ind. I"1 at the end of August (Figure 7).
Estimated predation on the size class <0.75 mm showed that estimatedpredation is higher than mortality of this size class in June, part of August and inSeptember. Leptodora seems to be mainly responsible for this (Figure 8).
IFig. 8. Estimated daily predation by Leptodora kindtii and Chaoborus flavicans and absolute dailymortality of D.hyalina and D.cucullata in Lake Vechten from May to September 1988. Predationrates were based on estimates of Dodson (1970) for Chaoborus and Mordhukay-Boltovskaya (1958)for Leptodora.
•S
0.300.250.200.150.100.050.00
0.300.250.200.150.100.050.00
D. hyalina
• • • Total mortality• Culture nortallty
Mortality by predation
» I J I J I A
D. cucullata
JM I 7 J I A I S I
Fig. 9. Juvenile mortality in the lake population and in the life-table experiments from July toSeptember 1988. Mortality by predation is the difference between both estimates.
Juvenile mortality in the field was higher than in the cultures, especially fromJune 21 to July 8 (Figure 9). There is a distinct peak in mortality of the twoDaphnia species under laboratory conditions and in the field during the lastweeks of August for both Daphnia species. Data for a comparison between
mortality in the cultures and in the simulated cohorts for D.cucullata werescanty, but obviously mortality by predation was much higher for D.cucullatathan for D.hyalina in July and August. Mortality by predation could account forvirtually all the mortality of D.hyalina in July, and of D.cucullata in late July andearly August. Mortality of adults in the life-table experiments was negligible.
.Discussion
During the winter of 1987-1988 Daphnia was absent in the lake; therefore, in1988 populations of both species must have developed from resting eggs.Contrary to 1986, there was no spring peak of D.hyalina in 1988, indicating thatthe spring peak of D.hyalina in 1986 was caused by the presence in the winter of1985-1986 of D.hyalina while D.cucullata was completely absent (Hovenkamp,1989). Because both populations started from resting eggs, death rates duringthe first weeks are likely to be underestimated and thus not reliable. However,since a negative death rate estimate occurred only once, the influence of restingeggs on the rate of increase must have been relatively unimportant comparedwith recruitment from parthenogenetic eggs.
As in 1986, rates of increase and birth and death rates of both species werevery similar and the dominance of D.cucullata from July onwards was caused bya relatively small difference in the rate of increase in June and July. Birth ratesare partly depending on temperature-dependent egg development times, andonly one temperature at 3 m depth was used. It should be noticed that evenwhen an absolute error has been made in estimating birth rates the relative errorbetween D.hyalina and D.cucullata has been small because the two species didnot differ in depth distribution.
During the last weeks of May the population death rate of D.cucullata is lowerthan of D. hyalina but the mortalities of the separate instar classes of D.cucullataare higher. This phenomenon is partly due to the use of running means in thegraphs and partly the fact that the INSTAR model works with discrete numbersof individuals. Because of the extreme low densities in the lake the model startsalso with low numbers and the influence of random events might then be great.At low numbers the model mimicks reality not as realistic as with large numbers.
Mortalities of instar classes 2 and 3 contributed more to the population deathrate than in 1986. Nevertheless, the highest negative correlation betweendifferences in instar-specific mortalities and differences in rates of increase wasfound for instar class 1. This confirms the importance of differences in juvenilemortality as a mechanism determining the relative abundances of the species.Although there were large differences in mortalities of instar class 3, thedifferences in mortalities of this instar class and differences in the rates ofincrease were not significantly correlated.
The birth rate of D.cucullata in June and July is lower than of D.hyalina. Asfertility of comparable size classes of D.cucullata and D.hyalina is higher forD.cucullata in June and July, the lower birth rate is caused by the smaller adultsize of D.cucullata.
A comparison of mortalities observed in the laboratory cultures and the
mortality estimated for the field population showed that in June and Julyvirtually all juvenile mortality of D.hyalina is caused by predation and althoughno laboratory data of June are available for D. cucullata it is likely that predationwas also the most important cause of mortality for D.cucullata in this period.
All laboratory experiments were conducted at 18°C and ambient temperaturesin the lake ranged between 16.5 and 20cC. It is unlikely that importanttemperature-food interactions occurred within this temperature range. Foodconditions for daphnids are difficult to assess from phytoplankton counts or fromchlorophyll a estimates or particulate carbon estimates. However, insight intothe food conditions can be obtained by determining mean brood size, which canbe used as an indication of food quality and quantity for adults (Slobodkin, 1954;Green, 1956; Hall, 1964; Hebert, 1977; Lampert, 1978). Under good conditionsmean brood size is related to body size; mean brood size will partly depend onthe size structure of the population. For using as an indication of foodconditions, mean brood size should be made independent of the population sizestructure. Hebert (1977) described a method for calculating standard eggproduction, independent of the size structure of the population, in which caselength-brood size regressions were calculated for all sampling dates and used toestimate brood size for a standard sized daphnid. However, if the regressioncoefficients for the different dates are unequal, the results will depend stronglyon the choice of the standard size. To avoid this problem, I calculated meanbrood size separately for different size classes.
High mean brood size in June and July for both species indicates good foodconditions. This is supported by the relatively high densities of flagellates in Juneand July. The high brood size of size class 1.0-1.2 mm of D.cucullata coincideswith high flagellate densities in mid-July, but numbers in this size class were lowand the standard deviations high. Daphnia longispina, a species very similar toD.hyalina, and D.cucullata are both known to graze effectively on particles<25 u-m (Gliwicz, 1977), a size class which contains most flagellates of LakeVechten except Cryptomonas ovata (Blaauboer, 1982). It is therefore unlikelythat in June and July D.cucullata benefits more from food conditions thanD.hyalina.
The comparison of absolute mortality in size class <0.75 mm and estimatedpredation by Chaoborus and Leptodora should be cautiously interpreted. Allan(1973) reported predation rates of Chaoborus punctipennis on Daphnia rangingfrom 1.25 to 3.41 prey ind."1 day"1 and therefore the 3.2 prey ind.""1 day"1
(Dodson, 1970) used in the present study may be too high. This means thatpredation by Chaoborus was less important than predation by Leptodora. Thepredation rate also includes other zooplankton than Daphnia but Leptodora willprobably not capture copepods if sufficient cladocerans are present (Mordhukai-Boltovskaya, 1958). Diaphanosoma brachyurum was the only other cladoceran,present in densities of 5-10 ind. I"1 in July and 10-15 ind. I"1 in August. Thisindicates that potential predation could not account for the mortality of thedaphnids <0.75 mm only in the last weeks of July and August. In this periodthere was also a large drop in flagellate densities and an increase in juvenilemortality in the life-table experiments. Flagellate densities increase again during
August, coinciding with a decrease of culture mortality. The high possibleimpact of Leptodora predation on Daphnia population dynamics is in agreementwith the observations of Hall (1964) and Karabin (1974).
In June and July low Leptodora densities coincided with large differencesbetween juvenile mortalities. In this period predation by Chaoborus, whichprefers non-helmeted species (O'Brien et al., 1979; Havel, 1987), wassufficiently high to explain juvenile mortality of both species.
In conclusion, the importance of juvenile mortality for the relative densities ofD.hyalina and D.cucullata is confirmed. Selective mortality by Chaoborus canexplain the differences in juvenile mortality from mid-June to mid-July butduring the rest of the season predation by Leptodora appeared to be moreimportant than predation by Chaoborus. The decrease of D.hyalina andD.cucullata densities at the end of July is caused by increased juvenile mortality,probably due to low densities of flagellates which were the main food source inLake Vechten during the summer of 1988.
Acknowledgements
I am grateful to H.P.Koelewijn for adapting the INSTAR model to myimmediate needs and I would like to thank J.Ringelberg, R.D.Gulati,J.Vijverberg and O.van Tongeren for discussing and correcting the manuscript.P.Heuts provided valuable assistance in the field and the laboratory.
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Received on May 10, 1989; accepted on January 2, 1990
