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Egg production of Eurytemora affinis—Effect of k-strategy
Estuarine, Coastal and Shelf Science (1992) 35, 395-407
Egg Production of Eurytemora affinis-Effect of k-Strategy
H.-J. Hirche Alfred-Wegener-Institute for Polar and Marine Research, Columbusstr. I, D-2850 Bremerhaven, Germany Received 17July 1991 and in revised form 5 February 1992
Keywords: Eurytemora; egg production; reproductive strategy The number of eggs found in egg sacs of Eurytemora affinis in the Schlei, a mesohaline fjord in the Western Baltic, was determined between January and August, and female prosome length measured. Prosome length at 25 °C was only half that at 0 °C and was significantly correlated with mean temperature during development. Clutch size increased from lower winter values to a maximum in April and thereafter sharply decreased to a minimum at the end of July. The correlation between clutch size and body size was stronger than that between clutch size and temperature at collection. From calculations using regressions of body size and clutch size with temperature, a curve was derived for female fecundity at satiating food levels with a minimum at 12 °C and increased values at both lower and higher temperatures. Depending on the length-weight conversion applied, P/B for egg production was 0.01 to 0.02 day- ~in winter and 0.43 to 0-51 day -~ at the temperature maximum in summer. Reproductive production is similar to somatic production of larval stages at low temperatures, but increases faster with increasing temperatures. The considerably smaller fecundity and weight specific egg production rate ofE. affinis may be the reason why it is outnumbered by Acartia tonsa in the summer in many locations. Seasonal partitioning of the biotope by the two species is maintained by k-strategy at lower temperatures with E. affinis carrying few large eggs, and r-strategy in summer with A. tonsa depositing many small eggs.
Introduction Eurytemora affinis is a key c o m p o n e n t o f the m e s o h a l i n e p l a n k t o n c o m m u n i t y in the coastal a n d b r a c k i s h waters a r o u n d the N o r t h A t l a n t i c . D u e to its c a p a b i l i t y o f filtering small size particles ( H e e r k l o s s , 1979) it can c o n v e r t b a c t e r i a ( G y l l e n b e r g , 1980) a n d d e t r i t u s ( H e i n l e et al., 1977) into f o o d for h i g h e r t r o p h i c levels. T h u s it is a n i m p o r t a n t food source for c o m m e r c i a l l y i m p o r t a n t larval a n d a d u l t fish ( S c h n a c k & B6ttger, 1981), a n d for o t h e r p r e d a t o r s such as s h r i m p s ( H e i n l e & F l e m e r , 1975). M a x i m u m a b u n d a n c e o f Eurytemora affinis is often o b s e r v e d in s p r i n g at relatively low w a t e r t e m p e r a t u r e s ( C r o n i n et al., 1962; H i r c h e , 1974; Baretta, 1980; S o l t a n p o u r G a r g h a r i & W e l l e r s h a u s , 1985). I n s u m m e r , w i t h t e m p e r a t u r e s e x c e e d i n g 15 °C, E. affinis decreases in a b u n d a n c e a n d is o f t e n s u c c e e d e d b y Acartia tonsa ( D e e v e y , 1948; H i r c h e , 1974; C h r i s t i a n s e n , 1988). T e m p e r a t u r e was n o t c o n s i d e r e d r e s p o n s i b l e for this c h a n g e in 0272-7714/92/100395 + 13 $03.00/0
© 1992 Academic Press Limited
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H.-J. Hirche
dominance, as E. aJ3inis has been reared successfully in the laboratory at temperatures up to 25 °C (Katona, 1970; Heinle & Flemer, 1975) and even tolerated temperatures up to 30 °C for some time (Bradley, 1975); instead, selective predation or seasonal changes in food quality (Christiansen, 1988) have been considered to favour A. tonsa. Due to large seasonal variations of water temperature in the habitat of Eurytemora aj~inis, understanding of its population dynamics in summer and modelling of its productivity in trophic studies of estuaries (G/idge, 1988) requires detailed knowledge of the relationship between temperature, body size and reproductive parameters. T h e measurement of egg production provides useful information such as female production and recruitment. As egg production in many species is closely related to ingestion, it may also be used as an indicator of the nutritional condition (Runge, 1985). In cases where a close relationship exists between somatic and reproductive growth, egg production may serve as an estimate of secondary production (Hirche et al., 1991). E. affinis carries the eggs in paired egg sacs which facilitates studies of its reproductive biology. I n this study, a set of field data collected for another study (Hirche, 1974) has been evaluated to investigate the relationship between temperature, body size and clutch size of E. affinis. Using existing data on hatching time of eggs and developmental times at different temperatures, individual as well as weight specific (P/B) egg production rates were estimated for various temperatures under conditions of food satiation. Specific egg production rate was then compared to productivity of growing stages. Reproductive strategy of E. aJ~nis was compared with that of Acartia tonsa and the effect on seasonal distribution patterns was discussed.
Material and methods Copepods were collected on 19 occasions between 22 January 1972 and 1 January 1973 with an Apstein net (50 and 100 ~tm mesh) in tows from close to the bottom to the surface. Mostly three fixed stations were visited, but at five occasions samples were taken only at station 4 (Figure 1). Water depth at the four stations varied between 2-0 and 2.2 m. Samples were preserved in buffered formalin. From water casts taken at the bottom and the surface, temperature was measured with a thermometer, and salinity was determined by the Microchloride method (Grasshoff, 1976). T h e largest difference between bottom and surface temperature was 1.8 °C on one occasion; usually the whole water column was well mixed. Female prosome length was measured with a micrometer (at 50 × ; to the nearest 0-02 mm) between the tip of the forehead and the lateral end of the last thoracic segment. T h e number of eggs per egg sac was only counted when the egg sac looked complete, i.e. when no empty shells were present and no ripe eggs were in the oviducts.
Results
Hydrography T h e Schlei Fjord is a narrow inlet of Kiel Bight of 30 km length (Figure 1). Salinity decreases from 12 to 20 at the mouth of the Schlei to < 5 in Schleswig (Nellen & Rheinheimer, 1970). It is therefore a mesohaline system. At the sampling sites, salinity varied between 5-1 and 9.4. Seasonal variability of temperature at station 4 is shown in Figure 2(a) (data from Schiemann, 1974). From mid-January to beginning of March the Schlei was partly ice covered.
Egg production of Eurytemora affmis
397
K°p~eJnr~ BalSen tic Schles~ 54030 , N I
I0 km
I
Figure 1. Sampling locations in the Schlei Fjord, Western Baltic.
Body size Seasonal variation of body size was considerable [Figure 2(b)]. Data showed a change in mean prosome length from 0.45 to 1.05 ram. A population of females with similar size present in the first three months was replaced by a population including the largest specimens found during this study. I n M a y these females had all disappeared. Body size was decreasing exponentially until the smallest size group was found in the beginning of July. Thereafter size increased again, and in D e c e m b e r specimens intermediate in size between the J a n u a r y - M a r c h group and the April group were found. Between 11 September and 18 N o v e m b e r , adult E. affinis were only present in very small numbers. Comparison of female prosome length with the seasonal cycle of temperature indicated an inverse relationship [Figure 2(a,b)], which was corroborated when body size was directly related to temperature (Figure 3). But clearly, lengths at low temperatures do not fit into the general relationship. As adult body size is probably the result of the temperature conditions during larval development (Hart & M c L a r e n , 1978), an attempt was made to calculate mean temperatures per generation ofE. affinis. Using the relationship between temperature (T) and developmental time (D) from egg to first egg sac by Heinle & Flemer (1975, calculated from their T a b l e 1) log D = 2.017 - 0.0428 * T
(Equation 1)
the mean temperature (Tmc~) during larval development was obtained from Tmean =
~ T d / t , where
T d =
mean daily temperature,
by stepwise back calculation with t = (1, 2 . . . . , days) and comparison with D at Tmea~, until D/t~ 1 This procedure was not applied to females found between January and M a r c h since, for their development, temperatures between 6 °C and 9 °C were required according to the temperature--length regression (Figure 3). This would imply life times of 100 and more days for the winter females. Such life times were indeed reported by Katona (1970). H e found generation times for E. aftinis of > 70 days and average survival times of ca. 80 days for females at 2 °C. Therefore no mean temperature was estimated for samples from
398
H.-J. Hirche
25
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IIIII
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30
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90
,
120 150 180 210 240 270 3 0 0 330 560 dulian day
Figure 2. Surface temperature and chlorophyll a concentrations at station 4 (a). Seasonal variation of prosome length (b) and clutch size (c) of female Eurytemora a.~inis. Error bars indicate standard deviation. , temperature; . . . . , Chl a.
22 January, 19 February and 17 March. T h e regression with Tmean gave a much better fit (r 2= 0"951) than the one with temperature at collection (r 2= 0.821) for samples (Figure 3), when values for both temperature at collection and mean temperature were available. Thus the equation used below is log L = 0.00139--0-0134 * T
(Equation 2)
Clutch size T h e content of the egg sacs (clutch size) of E. affinis showed extreme seasonal variability [Figure 2(c)]. T h e largest clutch had 79 eggs. In the beginning of February few egg sacs were found, but ovaries looked well developed and ready to spawn. F r o m low egg numbers in January clutch size increased dramatically to maximum size in April. Thereafter it decreased abruptly until a minimum was reached at the end of July. At this time very few
Egg production o f Eurytemora a~nis
399
TABLE 1. Comparison of female dry weight (~tg), fecundity (eggs female-J day-~), daily dry weight (B) specific egg production (EP) and somatic production (P) per dry weight of Eurytemora a O~nis and Acartia tonsa. Field observations or experiments, where females grew up at experimental temperatures (Heinle & Flemer, 1975) T °C
Dry weight
Eurytemora a_Oinis 0--25 2.16-7.35 5 6.24-8.25 10 4.80-5-40 15 3-14-3-24 20 2.14-2.33 25 1.54-1-68 5.5 8. I0 10 5.40 15 3.24 20 2.33 25 1.68 5-8-14-9 0-23 ? Acartia tonsa 15
8.50
20 25 12 15 20 26 15 20 14-23 20 20 20
6.00 4.50 7.00 7-00 5-30 5-7.25
Fecundity
EP/B
0.6-15-7 5"78 5-5 5-85 6.24 7.31
0.01-0.45 0.09--0.12 0.13-0.15 0'23 0.35-0.38 0.57-0.62
22 59 54
This study* 0"07 0"10 0"16 0.23 0.34 0.06 0.13 0-25 0-28 0.36 0-03-0.13 0.08--0.23 0.18-0.21
0.28 0.67 1"06
0.29 0.42-0.82
64 85 166
This study, model data ~
Heinle & Flemer, 1975 Burkill & Kendall, 1982 Christiansen, 1988 Amdt, 1985 Ambler, 1985b
0-23 0-41 0.58 0.58-0.87 50 70
Source
P/B
Miller et al., 1977 Dagg, 1977, mod. by Ambler, 1985 Beckman & Peterson, 1986 Christiansen, 1988 Durbin et al., 1983' Sullivan & Ritacco a Sullivan & Ritacco'
°See text. Female biomass calculated from length-weight conversion of Heinle & Flemer, 1975. bAssuming a factor of 2.5 for carbon to dry weight conversion. 'Enriched seawater. ~Tank experiment control. ~Tank experiment nutrient enriched. females w e r e c a r r y i n g egg sacs, a n d the eggs a p p e a r e d n o n - v i a b l e . E g g size varied b e t w e e n 7 8 - 9 0 lam ( m e a n 84 lam). T h e r e was no i n d i c a t i o n o f a relationship b e t w e e n egg size and b o d y size. T h e p o r t i o n o f female d r y w e i g h t d e p o s i t e d in each egg sac was calculated f r o m egg d r y w e i g h t (0" 13 lag e g g - t , H e i n l e & F l e m e r , 1975) a n d b o d y d r y weight. P r o s o m e l e n g t h was c o n v e r t e d into dry w e i g h t u s i n g existing l e n g t h - w e i g h t relationships for u n p r e s e r v e d E . affinis :
log W = 1'821 * L - 0 ' 6 5 4 , H e i n l e and F l e m e r (1975, P a t u x e n t R i v e r ) log W = 2-11 * L - 1"069, B 6 t t g e r (1979, Schlei) log W = 2.088 * L - 0 - 8 5 9 , Burkill and K e n d a l l (1982, Bristol C h a n n e l ) w h e r e W is dry w e i g h t (lag) a n d L is p r o s o m e l e n g t h (ram). All t h r e e e q u a t i o n s give c o m p a r a b l e results in the smaller size g r o u p , b u t d i v e r g e at p r o s o m e lengths > 0.75 m m
400
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0.9
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Ternperoture
Figure 3. Eurytemora a~inis. Pros•me length related to temperature at collection and mean temperature during development. For the regression curves numbered data (1: 22 January; 2:19 February; 3:17 March) were excluded. 0 , mean temperature; [], collection temperature.
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i
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length
r
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p I 1.0
(mm)
Figure 4. Eurytemora affinis. Dry weights calculated from length-dry weight conversions from El, B6ttger (1979) for the Schlei Fjord, I , Heinle and Flemer (1975) for the Patuxent River estuary, and • , Burkill and Kendall (1982) for the Bristol Channel.
considerably, with the largest discrepancies between the relationship of B6ttger on one side and the other two relationships on the other (Figure 4). Depending on the dry weight conversion used, egg sacs have been estimated to contain 63.4+24.21 (B6ttger, 1979), 58.2 + 17.48 (Burkill & Kendall, 1982) or 56-3_ 16.6 (Heinle & Flemer, 1975) percent body dry weight. The seasonal variability of clutch size showed strong similarities to changes in body size [Figure 2(c)]. Comparison of the correlation coefficients (without the two January values) showed a much stronger relationship between clutch size (C) and body size (L) [r 2 = 0"872; Figure 5(b)] than between clutch size and temperature at collection [r2 = 0.56; Figure 5(a)]: log C = 1'9809 * L - 0.1229
(Equation 3)
Egg production of E u r y t e m o r a ~ i s
401
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0.9
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Figure 5. Eurytemora affinis. Relationship between clutch size and temperature at collection (a) and prosome length (b). Values in circles were excluded from regression.
With respect to relatively fast egg developmental times, temperature at collection was assumed to be a sufficiently accurate measure of temperature during egg formation. T h e importance of body size was most evident in late winter, when the largest discrepancies occurred between body size and temperature at collection [Figure 5(b)]. It is thus concluded that clutch size is not directly related to temperature, but indirectly via body size, which is a function of temperature during larval development.
Fecundity and weight specific egg production Individual egg production rate (F, fecundity) was estimated from clutch size (C) and hatching time (H) by: F = C * 1/H
(Equation 4)
Hatching times were derived from an exponential fit to data from M c L a r e n (1969) and Heinle and Flemer (1975) from experiments at different temperatures (T). log H = 1.001 - 0.05578 * T
(Equation 5)
Hatching times of eggs at each station were calculated from this regression, using the temperatures at the time of sampling. D r y weight specific productivities (P) of mature females were calculated from egg numbers (this study), egg dry weights (0.13 lag, Heinle & Flemer, 1975), female weights (from length-weight relationships), and hatching time (H) by P = egg biomass/female biomass * I / H .
(Equation 6)
Fecundity showed a pronounced peak in the middle of April, coinciding with the maxima of female size and clutch size. A second, smaller peak occurred at the beginning of July [Figure 6(a)]. For the plot of dry weight specific egg production rate (P/B), the length-weight conversion of Burkill and Kendall (1982) was used, which is the intermediate of the three available conversions. Weight specific egg production reflected
402
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~D D
(b)
I~D
0.31 "0
p (m o.[ NlllJll
"'
o
lallll
llilli
JIII
ii Illl
i l I I I ~l'-I
30 6 0 9 0 120 150 lEE) 210 240270300330360 Day
Figure 6. Eurytemora a Ofnis. Individual egg production rate (a) and weight specific egg production rate (b).
strongly the temperature dependence of productivity, with a P/B ratio of 0.01-0.02 d a y - ] (depending on length-weight conversion) in winter and 0.43-0-51 day -1 around the temperature m a x i m u m in s u m m e r [Figure 6(b)].
Model of temperature dependent fecundity and specific production T h e regressions of egg production with body size and temperature obtained from field samples make it possible to model general relationships between temperature and the before mentioned parameters. T h e effect of temperature on fecundity was estimated using relationships of hatching time (equation 5), body size (equation 2), and clutch size (equation 3) with temperature (T). As a result, fecundity (F) followed the quadratic equation F = 6"6072 - 0"206 * T + 0"00938 * T z
(Equation 7)
T h e m i n i m u m of this equation fell at 12 °C, while egg production rate at 0 °C was equal to that at 20 °C (Figure 8). For modelling of weight specific egg production (Figure 7), body size at different temperatures was calculated from equation (2). Clutch size was then derived from body size (equation 3) and hatching time was taken from equation (5). O f special interest was the comparison of specific egg production with somatic production of growing individuals at different temperatures. Somatic production (SP) was calculated using egg weight (0.13 lag) and adult weight (W) vs. time to reach adulthood (G), presuming exponential growth (Heinle & Flemer, 1975): SP = In W
-
In 0-13/G
(Equation 8)
T i m e to reach adulthood (G) at different temperatures (T) was calculated from a regression using an exponential fit to experimental data presented in Heinle and Flemer (1975): log G = 1"9636 - 0.04333 * T
(Equation 9)
Egg production o f E u r y t e m o r a affmis
07! 0.6
o "o
T
0-5
E o 25
0.4
403
[ ] EP/B B5 y = 0,03107 * T - 1.079 • EP/B HF y = 0.04141 * T - I . 2 5 0 0 P/B B5 y= 0"03493" T - 1"337 • P/B HF y= 0 . 0 3 1 8 7 " T - 1 - : > 8 9
art a[] in u•
at]
.=_o 0 . 5
0.2
--DD
°°°e°°e°egeO° G• nanm~fS~D
[]
#_
•
0.1 I
I
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t
0
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a
5
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I
t
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I
I
I
I
15
|
[
I
I
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20
I
25
Temperature (°C)
Figure 7. Eurytemora a~inis. Comparison of weight specific production rates for egg production (EP/B) and somatic production (P/B) for different length-dry weight conversions (B6: B6ttger, 1979; HF: Heinle & Flemer, 1975; see text for equations).
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04
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j8 5
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0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 i i i ~ I i t i p I i J J i I I
0
5
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f
20
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Temper•lure
Figure 8. Comparison of individual egg production rate of Eurytemora aj~nis (filled circles, equation 4) and Acartia tons• (open circles). Data for Eurytemora were derived from a model (see text). Clutch size was calculated from pros•me length at different temperatures (equations 2 and 3) and divided by hatching time (equation 5). 1: Ambler, 1985; 2: Dagg, 1977; 3: Sullivan & Ritacco, 1985; 4: Beckman & Peters•n, 1986; 5: Durbin et al., 1983.
Only at the lower temperatures are reproductive and somatic production similar (Figure 7), regardless of the length-weight conversion applied. Towards higher temperatures regressions for the two productive modes diverge considerably.
Discussion Highly significant relationships were observed between environmental temperature, body size and clutch size of E. affinis in the field, except for the winter population. These
404
H.-~. Hirche
relationships permit predictions of recruitment and specific production by females at food satiation from water temperature. In-situ egg counts permit estimation of food limitation by comparison with regression-derived m a x i m u m clutch size. This has been suggested by Runge (1985) and applied by Hirche et al. (1991). T h e excellent fit of clutch size with body size from the end of M a r c h onwards strongly indicates satiating food conditions for E. affinis in the Schlei during most of the year and hence m a x i m u m clutch size in our regression. Chlorophyll a concentrations reported by Schiemann [1974, data in Figure 2(a) from his tables in the Appendix for a station very close to station 1 of this study] show superabundant phytoplankton biomass from the beginning of March to September. T h e chlorophyll maxima in M a r c h and M a y were formed by small Chlorophyceae (1-4 ~tm), while in June and August blooms consisted mostly of Cyanophyceae (J/irgens, pers. comm. in Schiemann, 1974). In general, most of the phytoplankton was in the size range < 60 ~tm (Schiemann, 1974). Direct observations orE. affinis suggest that they are capable of feeding on particles within the range 2 to 60 ~tm (Heinle & Flemer, 1975; Heinle et al., 1977). Only in winter during ice cover were chlorophyll concentrations low. T h u s food limitation may at least partly explain the smaller than expected clutches. In addition, the extreme longevity of females of the early spring p o p u lation, which was indicated by the length-temperature relationship, may have contributed to reduced clutch size through senescent ovaries. It is known, that m a x i m u m egg production is only maintained over a short period in small copepods (Sciandra et al., 1990). As the effect of longevity upon the egg production orE. affinis is not yet understood, prediction of clutch size from body size should be handled with caution at low temperatures, where female survival may be considerable. Productivities measured by Heinle and Flemer (1975) in the Patuxent River estuary during February and April were at some of their stations about one half as great as those predicted from the laboratory studies, suggesting that the supply of food was limiting the production of E. affinis. D u e to the different temperature regime in the Patuxent, the period of food limitation covered a m u c h wider temperature range than in the Schlei and may so have disguised the relationships established during this study. Heinle and Flemer (1975) found larger clutches at some of their stations at low temperatures. T h e i r m a x i m u m was 84.4 as compared to 69 eggs clutch- 1in this study. However, this may relate to the size of their females, which were up to 14% larger and hence up to 80% heavier. Wherever the seasonal cycle ofE. affinis was studied, its disappearance with the s u m m e r warming and succession by other copepods, mostly Acartia tonsa, was a common feature, which has puzzled investigators. According to Bradley (1975), the seasonal distribution of E. affinis is contrary to that expected from thermal tolerance-salinity relationships. Explanations offered are predation by or competition with other species. In its habitat, E. affinis is certainly exposed to strong predation pressure, and Heinle and Flemer (1975) related the decline of E. affinis in the Patuxent in the spring to predation by the Opossum shrimp Neomysis americana. I n addition Christiansen (1988) suggested the mortality of E. affinis in the Schlei was mostly caused by the large n u m b e r offish larvae in this area. However, unless there is selective predation, other copepod species should also be affected as m u c h as E. affinis, yet Heinle (1970) found that predation less strongly affected E. affinis than A. tonsa. I n contrast, Baretta and Malschaert (1988) argue that E. affinis is more strongly affected by predation than A . tonsa and they relate this to different strategies of egg deposition of the two species. Egg sacs would slow down E. affinis when trying to avoid predators, while A . tonsa, which spawns the eggs free in the water, would escape faster. In addition, predation on egg-carrying female E. affinis would entail the loss of the current
Egg production of Eurytemora affinis
405
batch of eggs, whereas in A . tonsa the eggs already spawned would still contribute to the propagation of the species. Direct predation o f A . tonsa on nauplii of other species has also to be taken into consideration according to observations by Lonsdale et al. (1979). Heinle (1970) pointed to physiological differences between E. affinis and A . tonsa: while the growth rate and productivity o r E . affinis were equal to that o f A . tonsa at 12 °C, they were only half as great at 25 °C. Baretta and Malschaert (1988) related the virtual disappearance of A. tonsa from the E m s estuary in winter to decreasing egg production at low temperatures combined with reduced survival of the few eggs due to long development times. T h e dominance of E. affinis in winter and spring was explained by these authors by the advantage of carrying egg sacs. T h e results of the present study also indicate, that reproductive strategy may be one of the key factors determining the seasonal distribution patterns of E. affinis. Its k-strategy expressed in carrying few large eggs in sacs seems to yield sufficient recruitment at lower temperatures. T h r o u g h the observed close coupling of clutch size and body size a strong effect of the enormous size decrease on their reproductive success at higher temperatures is expected. T h e difference in size that occurred at the extremes of the temperature range---variation in prosome length from 0.45 to 1.05 m m corresponding to a change in dry weight from 1-2/1-58 to 9-46/21.55 lag, depending on length-weight conversion--is among the greatest reported. As egg size seems to be invariant, at temperatures > 25 °C E. affinis females apparently reach anatomical limits for egg deposition. Decreasing female size counterbalances the effect of shorter hatching times at higher temperatures. Model data showed that different temperature coefficients for hatching times and body size resulted in decreased fecundity at increased temperatures in the 0 to 12 °C range (Figure 8). T h e fecundity m i n i m u m at ca. 12 °C coincides with the temperature [sensu ' mean temperature during ontogenetic development ', see Figure 5(a)], when E. affinis populations often start decreasing in the field. Acartia tonsa is not competing at low temperatures in spring as it mostly overwinters in the m u d as resting eggs (Zillioux & Gonzalez, 1972). It becomes abundant when eggs hatch at temperatures > 10 °C (Zillioux & Gonzalez, 1972; Christiansen, 1988). Comparison of reproductive strategies reveals clearly the differences between both species. A . tonsa is a r-strategist with a fecundity up to one order of magnitude higher than that of E. affinis (Figure 8). This higher fecundity goes along with larger females and smaller eggs, but also with higher weight specific production. Prosomes of A . tonsa females between M a y and October were generally ca. 100 lam longer in the Schlei (Christiansen, 1988). M o r e examples for body weights from field collections are presented in T a b l e 1. Female A . tonsa are often two or three times heavier than E. affinis. A n egg diameter of 73 lam in A . tonsa (Ambler, 1985) compares with 82 lam in E. affinis. Although there are some discrepancies in reports on egg carbon content of A. tonsa (0"028 lag: Heinle, 1966; Miller et al., 1977; 0"031 lag: D u r b i n & Durbin, 1981; Ambler, 1985; 0.046 lag: Kiorboe et al., 1985; 0"05 lag: Landry, 1983), most of the measurements indicate egg weights half that ofE. affinis, when a dry weight content of 40% carbon is assumed. Comparative data for weight specific egg production at different temperatures (Table 1) clearly show the considerably higher rate for A . tonsa at all temperatures where both species usually co-occur. This may lead to disappearance ofE. affinis in summer, when predation pressure is high on both species. As E. affinis reproduces over a wider temperature range with little variability in fecundity, at higher latitudes with lower temperature maxima it may maintain a significant population over the whole year. T h u s , seasonal resource partitioning by the two species is maintained by k-strategy at lower temperatures, with E. affinis carrying few large eggs, and r-strategy
406
H.-J. Hirche
in s u m m e r , w i t h A . tonsa d e p o s i t i n g m a n y small eggs. S i n k i n g s p e e d a n d d e v e l o p m e n t a l t i m e o f eggs m a y be critical p a r a m e t e r s d e t e r m i n i n g the success o f free egg d e p o s i t i o n in shallow waters, w h e r e they often m a y b e eaten b y p r e d a t o r s o r d e t e r i o r a t e u n d e r anoxic conditions. F o r Acartia clausi, A . tonsa a n d Eurytemora herdmani, r e a r e d in a b u n d a n t food c o n ditions, eggs are p r o d u c e d at the same i n s t a n t a n e o u s rate as p r e v i o u s somatic p r o d u c t i o n ( S e k i g u c h i et al., 1980; M c L a r e n & C o r k e t t , 1981; B e r g r e e n et al., 1988). T h i s w o u l d p e r m i t p r e d i c t i o n o f somatic p r o d u c t i o n f r o m c l u t c h size counts in E. affinis. H o w ever, w i t h t h e values c h o s e n h e r e , P/B for s o m a t i c p r o d u c t i o n has a s m a l l e r t e m p e r a t u r e coefficient t h a n egg p r o d u c t i o n ; o n l y at lower t e m p e r a t u r e s are values similar. T h e r e is g o o d a g r e e m e n t b e t w e e n P/B calculation b a s e d on results o f this s t u d y a n d field estimates f r o m c o h o r t analysis ( A r n d t , 1985; C h r i s t i a n s e n , 1988, T a b l e 1) a n d w i t h l a b o r a t o r y e x p e r i m e n t s w i t h females r e a r e d at different t e m p e r a t u r e s ( H e i n l e & F l e m e r , 1975). T h e d a t a in T a b l e 1 s h o w that in a d d i t i o n to r e p r o d u c t i o n also s o m a t i c p r o d u c t i o n is g r e a t e r in A . tonsa t h a n in E. affinis at h i g h e r t e m p e r a t u r e s . F o r calculations o f various expressions o f p r o d u c t i v i t y in this s t u d y , d e v e l o p m e n t a l times o f eggs a n d larvae have b e e n t a k e n f r o m the literature. O f t e n these values were d e r i v e d after e x p o s i n g eggs a n d n a u p l i i f r o m females raised at one t e m p e r a t u r e to various o t h e r t e m p e r a t u r e regimes. T e m p e r a t u r e a c c l i m a t i o n o f these rates has r a r e l y b e e n s t u d i e d , a l t h o u g h it is c o m m o n sense t h a t it affects m a n y m e t a b o l i c activities. T h e n e e d o f such i n f o r m a t i o n for p r e d i c t i n g g r o w t h a n d p r o d u c t i o n s h o u l d s t i m u l a t e r e s e a r c h in this field.
Acknowledgements T h e h e l p o f T . B r e y in m a t h e m a t i c a l questions is greatly a c k n o w l e d g e d . T h i s is p u b l i c a t i o n no. 195 o f the A l f r e d - W e g e n e r - I n s t i t u t e for P o l a r a n d M a r i n e R e s e a r c h .
References Ambler, j'. W. 1985 Seasonal factors affecting egg production and viabilityof eggs ofAcartia tonsa Dana from East Lagoon, Galveston, Texas. EstuaHne, Coastal and Shelf Science 20, 743-760. Arndt, H. 1985 Untersuchungen zur Populations6kologie der Zooplankter eines irmeren Kfistengewfissers der Ostsee. Ph.D. University Rostock, 170 pp. Baretta, J. W. 1980 Het zooplankton van het Eems-Dollard estuarium, soorten, aantallen, biomassa en seizoensfluctuaties. BOEDE Publicaties en Verslagen 5, 40 pp. Baretta, J. W. & Malschaert, J. F. P. 1988 Distribution and abundance of the zooplankton of the Eros estuary (North Sea). NetherlandsJournal of Sea Research 22, 69-81. Berggreen, U., Hansen, B. & Kiorboe, T. 1988 Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Marine Biology 99, 341-352. B6ttger, R. 1979 Untersuchungen fiber das Zooplankton der Schlei, im Hinblick auf das Nahrungsangebot fiir Heringslarven im Frfihjahr. Dipl. Thesis, University Hamburg, 109 pp. Bradley, B. P. 1975 The anomalous influence of salinity on temperature tolerances of summer and winter populations of the copepod Eurytemora a~inis. BiologicalBulletin 148, 26-34. Burkill, P. H. & Kendall, T. F. 1982 Production of the copepod Eurytemora a~nis in the Bristol Channel. Marine Ecology ProgressSeries 7, 21-31. Christiansen, B. 1988 Vergleichende Untersuchungen zur Populations-dynamik yon Eurytemora a~inis Poppe und Acartia tonsa Dana, Copepoda, in der Schlei. Ph.D. Thesis, University Hamburg, 141 pp. Cronin, L. E., Daiber, J. C. & Hulbert, E. M. 1962 Quantitative seasonal aspects of zooplankton in the Delaware River estuary. Chesapeake Science 3, 63-93. Dagg, M. 1977 Some effects of patchy food environments on copepods. Limnology and Oceanography 22, 99-107. Deevey, G. B. 1948 The zooplankton of Tisbury Great Pond. Bulletin Bingham Oceanographic Collection 12, 1-44.
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Durbin, E. G., Durbin, A. G., Smayda, T. J. & Verity, P. G. 1983 Food limitation of production by adult Acartia tonsa in Narragansett Bay. Rhode Island. Limnology and Oceanography 28, 1199-1213. Gfidge, U. 1988 Analyse experimenteller Daten und Simulationsrechnungen zur Populationsdynamik und Koexistenz von calanoiden Copepoden im Ems-Dollart-•stuar. Ph.D. Thesis, University Oldenburg, 88 pp. Grasshof, K. 1976 Methods of seawater analysis. Verlag Chemic, Weinheim, New York, 317 pp. Gyllenberg, G. 1980 Feeding of the copepod Eurytemora hirundoides (Crustacea) on the different algal cultures. Annales ZoologiciFennici 17, 181-184. Hart, R. C. & McLaren, I. A. 1978 Temperature acclimation and other influences on embryonic duration in the copepod Pseudocalanus. Marine Biology 45, 23-30. Heerkloss, R. 1979 Selektivitiit der Nahrungsaufnahme, Ingestionsrate und Faecesabgabe bei Eurytemora affinis (Poppe) (Calanoida, Copepoda). Wissenschaftliche Zeitschrift der Universitiit Rostock, Mathematisch-naturzoissenschaftliche Reihe 28, 525-529. Heinle, D. R. 1966 Production of a calanoid copepod, Acartia tonsa, in the Patuxent River estuary. Chesapeake Science 7, 59-74. Heinle, D. R. 1969 Temperature and zooplankton. Chesapeake Science 10, 186-209. Heinle, D. R. 1970 Population dynamics of exploited cultures of calanoid copepods. Helgoliinder wissenschaftliche Meeresuntersuchungen 20, 360-372. Heinle, D. R. & Flemer, D. A. 1975 Carbon requirements of a population of the estuarine copepod Eurytemora affinis. Marine Biology 31,235-247. Heinle, D. R., Harris, R. P., Ustach, J. F. & Flemer, D. A. 1977 Detritus as food for estuarine copepods. Marine Biology 40, 341-353. Hirche, H.-J. 1974 Die Copepoden Eurytemora affinis Poppe und Acartia tonsa Dana und ihre Besiedelung dutch Myoschiston centropagidarum Precht (Peritricha) in der Schlei. Kieler Meeresforschungen 30, 43-64. Hirche, H.-J., Baumann, M. E. M., Katmer, G. & Gradinger, R. 1991 Plankton distribution and the impact of copepod grazing on primary production in Fram Strait, Greenland Sea. Journal of Maline Systems 2, 477-494. Katona, S. K. 1970 Growth characteristics of the copepods Eurytemora affinis and E. herdmani in laboratory cultures. Helgol~nder wissenschaftlicheMeeresuntersuchungen 20, 373-384. Kiorboe, T., Mohlenberg, F. & Hamburger, K. 1985 Bioenergetics of the planktonic copepod Acartia tonsa: relation between feeding, egg production and respiration, and composition of specific dynamic action. Marine Ecology Progress Series 26~ 85-97. Landry, M. R. 1983 The development of marine calanoid copepods with comment on the isochronal rule. Limnology and Oceanography 28, 614-624. Lonsdale, D. J., Heinle, D. R. & Siegfried, C. 1979 Carnivorous feeding behavior of the adult calanoid copepod Acartia tonsa Dana. Journal of experimental marine Biology and Ecology 36, 235-248. McLaren, I. A., Corkett, C. J. & Zillioux, E. J. 1969 Temperature adaptations of copepod eggs from the Arctic to the tropics. Biological Bulletin 137, 486-493. McLaren, I. A. & Corkett, C. J. 1981 Temperature-dependent growth and production by a marine copepod. Canadian Journal of Fisheries and Aquatic Sciences 38, 77-83. Miller, C. B., Johnson, J. K. & Heinle, D. R. 1977 Growth rules in the marine copepod genus Acartia. Limnology and Oceanography 22, 326-334. Nellen, W. & Rheinheimer, G. 1970 Einleitung und Literaturzusammenstellung frfiherer Arbeiten fiber die Schlei. In Chemische, mikrobiologische und planktologische Untersuchungen in der Schlei im Hinblick auf deren Abwasserbelastung(Rheinheimer, G., ed.). Kieler Meeresforschungen26, 105-109. Runge, J. A. 1985 Egg production rates of Calanus finmarchicus in the sea off Nova Scotia. Archly fiir Hydrobiotogie ( Beihefte Ergebnisseder Limnologie) 21, 33-40. Schiemann, S. 1974 Die Primfirproduktion des Phytoplanktons der Schlei und des Windebyer Noors im Jahre 1972 (Ein Vergleich yon Methoden und Biotopen). Ph.D. Thesis, University Kiel, 173 pp. Schnack, D. & B6ttger, R. 1981 Interrelation between invertebrate plankton and larval fish development in the Schlei fjord, Western Baltic. Kieler Meeresforschungen, Sonderheft 5,202-210. Sciandra, A., Gouze, J.-L. & Nival, P. 1990 Modelling the reproduction of Centropages typicus (Copepoda: Calanoida) in a fluctuating food supply: effect of adaptation. Journal of Plankton Research 12, 549-573. Sekiguchi, H., McLaren, I. A. & Corkett, C. J. 1980 Relationship between growth rate and egg production in the copepod Acartia elausi hudsonia. Marine Biology 58, 133-138. Soltanpour-Gargari, A. & Wellerhaus, S. 1985 Eurytemora affinis--one year study of abundance and environmental factors. Ver6ffentlichungenaus dem Institut fiir Meeresforschung, Bremerhaven 20, 183-198. Sullivan, B. K. & Ritacco, P. J. 1985 T h e response of dominant copepod species to food limitation in a coastal marine ecosystem. Archiv fiir Hydrobiologie (Beihefte Ergebnisseder Limnologie) 21,407-418. Zillioux, E. J. & Gonzalez, J. G. 1972 Egg dormancy in a neritic calanoid copepod and its implications to overwintering in boreal waters. In 5th European Maline Biology Symposium (Battaglia, B., ed.). Piccin Editore, Padua & London, pp. 217-230.
Egg Production of Eurytemora affinis-Effect of k-Strategy
H.-J. Hirche Alfred-Wegener-Institute for Polar and Marine Research, Columbusstr. I, D-2850 Bremerhaven, Germany Received 17July 1991 and in revised form 5 February 1992
Keywords: Eurytemora; egg production; reproductive strategy The number of eggs found in egg sacs of Eurytemora affinis in the Schlei, a mesohaline fjord in the Western Baltic, was determined between January and August, and female prosome length measured. Prosome length at 25 °C was only half that at 0 °C and was significantly correlated with mean temperature during development. Clutch size increased from lower winter values to a maximum in April and thereafter sharply decreased to a minimum at the end of July. The correlation between clutch size and body size was stronger than that between clutch size and temperature at collection. From calculations using regressions of body size and clutch size with temperature, a curve was derived for female fecundity at satiating food levels with a minimum at 12 °C and increased values at both lower and higher temperatures. Depending on the length-weight conversion applied, P/B for egg production was 0.01 to 0.02 day- ~in winter and 0.43 to 0-51 day -~ at the temperature maximum in summer. Reproductive production is similar to somatic production of larval stages at low temperatures, but increases faster with increasing temperatures. The considerably smaller fecundity and weight specific egg production rate ofE. affinis may be the reason why it is outnumbered by Acartia tonsa in the summer in many locations. Seasonal partitioning of the biotope by the two species is maintained by k-strategy at lower temperatures with E. affinis carrying few large eggs, and r-strategy in summer with A. tonsa depositing many small eggs.
Introduction Eurytemora affinis is a key c o m p o n e n t o f the m e s o h a l i n e p l a n k t o n c o m m u n i t y in the coastal a n d b r a c k i s h waters a r o u n d the N o r t h A t l a n t i c . D u e to its c a p a b i l i t y o f filtering small size particles ( H e e r k l o s s , 1979) it can c o n v e r t b a c t e r i a ( G y l l e n b e r g , 1980) a n d d e t r i t u s ( H e i n l e et al., 1977) into f o o d for h i g h e r t r o p h i c levels. T h u s it is a n i m p o r t a n t food source for c o m m e r c i a l l y i m p o r t a n t larval a n d a d u l t fish ( S c h n a c k & B6ttger, 1981), a n d for o t h e r p r e d a t o r s such as s h r i m p s ( H e i n l e & F l e m e r , 1975). M a x i m u m a b u n d a n c e o f Eurytemora affinis is often o b s e r v e d in s p r i n g at relatively low w a t e r t e m p e r a t u r e s ( C r o n i n et al., 1962; H i r c h e , 1974; Baretta, 1980; S o l t a n p o u r G a r g h a r i & W e l l e r s h a u s , 1985). I n s u m m e r , w i t h t e m p e r a t u r e s e x c e e d i n g 15 °C, E. affinis decreases in a b u n d a n c e a n d is o f t e n s u c c e e d e d b y Acartia tonsa ( D e e v e y , 1948; H i r c h e , 1974; C h r i s t i a n s e n , 1988). T e m p e r a t u r e was n o t c o n s i d e r e d r e s p o n s i b l e for this c h a n g e in 0272-7714/92/100395 + 13 $03.00/0
© 1992 Academic Press Limited
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dominance, as E. aJ3inis has been reared successfully in the laboratory at temperatures up to 25 °C (Katona, 1970; Heinle & Flemer, 1975) and even tolerated temperatures up to 30 °C for some time (Bradley, 1975); instead, selective predation or seasonal changes in food quality (Christiansen, 1988) have been considered to favour A. tonsa. Due to large seasonal variations of water temperature in the habitat of Eurytemora aj~inis, understanding of its population dynamics in summer and modelling of its productivity in trophic studies of estuaries (G/idge, 1988) requires detailed knowledge of the relationship between temperature, body size and reproductive parameters. T h e measurement of egg production provides useful information such as female production and recruitment. As egg production in many species is closely related to ingestion, it may also be used as an indicator of the nutritional condition (Runge, 1985). In cases where a close relationship exists between somatic and reproductive growth, egg production may serve as an estimate of secondary production (Hirche et al., 1991). E. affinis carries the eggs in paired egg sacs which facilitates studies of its reproductive biology. I n this study, a set of field data collected for another study (Hirche, 1974) has been evaluated to investigate the relationship between temperature, body size and clutch size of E. affinis. Using existing data on hatching time of eggs and developmental times at different temperatures, individual as well as weight specific (P/B) egg production rates were estimated for various temperatures under conditions of food satiation. Specific egg production rate was then compared to productivity of growing stages. Reproductive strategy of E. aJ~nis was compared with that of Acartia tonsa and the effect on seasonal distribution patterns was discussed.
Material and methods Copepods were collected on 19 occasions between 22 January 1972 and 1 January 1973 with an Apstein net (50 and 100 ~tm mesh) in tows from close to the bottom to the surface. Mostly three fixed stations were visited, but at five occasions samples were taken only at station 4 (Figure 1). Water depth at the four stations varied between 2-0 and 2.2 m. Samples were preserved in buffered formalin. From water casts taken at the bottom and the surface, temperature was measured with a thermometer, and salinity was determined by the Microchloride method (Grasshoff, 1976). T h e largest difference between bottom and surface temperature was 1.8 °C on one occasion; usually the whole water column was well mixed. Female prosome length was measured with a micrometer (at 50 × ; to the nearest 0-02 mm) between the tip of the forehead and the lateral end of the last thoracic segment. T h e number of eggs per egg sac was only counted when the egg sac looked complete, i.e. when no empty shells were present and no ripe eggs were in the oviducts.
Results
Hydrography T h e Schlei Fjord is a narrow inlet of Kiel Bight of 30 km length (Figure 1). Salinity decreases from 12 to 20 at the mouth of the Schlei to < 5 in Schleswig (Nellen & Rheinheimer, 1970). It is therefore a mesohaline system. At the sampling sites, salinity varied between 5-1 and 9.4. Seasonal variability of temperature at station 4 is shown in Figure 2(a) (data from Schiemann, 1974). From mid-January to beginning of March the Schlei was partly ice covered.
Egg production of Eurytemora affmis
397
K°p~eJnr~ BalSen tic Schles~ 54030 , N I
I0 km
I
Figure 1. Sampling locations in the Schlei Fjord, Western Baltic.
Body size Seasonal variation of body size was considerable [Figure 2(b)]. Data showed a change in mean prosome length from 0.45 to 1.05 ram. A population of females with similar size present in the first three months was replaced by a population including the largest specimens found during this study. I n M a y these females had all disappeared. Body size was decreasing exponentially until the smallest size group was found in the beginning of July. Thereafter size increased again, and in D e c e m b e r specimens intermediate in size between the J a n u a r y - M a r c h group and the April group were found. Between 11 September and 18 N o v e m b e r , adult E. affinis were only present in very small numbers. Comparison of female prosome length with the seasonal cycle of temperature indicated an inverse relationship [Figure 2(a,b)], which was corroborated when body size was directly related to temperature (Figure 3). But clearly, lengths at low temperatures do not fit into the general relationship. As adult body size is probably the result of the temperature conditions during larval development (Hart & M c L a r e n , 1978), an attempt was made to calculate mean temperatures per generation ofE. affinis. Using the relationship between temperature (T) and developmental time (D) from egg to first egg sac by Heinle & Flemer (1975, calculated from their T a b l e 1) log D = 2.017 - 0.0428 * T
(Equation 1)
the mean temperature (Tmc~) during larval development was obtained from Tmean =
~ T d / t , where
T d =
mean daily temperature,
by stepwise back calculation with t = (1, 2 . . . . , days) and comparison with D at Tmea~, until D/t~ 1 This procedure was not applied to females found between January and M a r c h since, for their development, temperatures between 6 °C and 9 °C were required according to the temperature--length regression (Figure 3). This would imply life times of 100 and more days for the winter females. Such life times were indeed reported by Katona (1970). H e found generation times for E. aftinis of > 70 days and average survival times of ca. 80 days for females at 2 °C. Therefore no mean temperature was estimated for samples from
398
H.-J. Hirche
25
500
2O
400
15
300 . ~
I0
200
5
I00
o E
~
0 1.0 b) 0-9 E
5 0'8 D
-,g
0"7
III
0"6 0.5
i
l
t
i
l
i
l
l
l
l
IIIII
l
80 (c) 6O
4O
'6 zo Z
30
It! 60
90
,
120 150 180 210 240 270 3 0 0 330 560 dulian day
Figure 2. Surface temperature and chlorophyll a concentrations at station 4 (a). Seasonal variation of prosome length (b) and clutch size (c) of female Eurytemora a.~inis. Error bars indicate standard deviation. , temperature; . . . . , Chl a.
22 January, 19 February and 17 March. T h e regression with Tmean gave a much better fit (r 2= 0"951) than the one with temperature at collection (r 2= 0.821) for samples (Figure 3), when values for both temperature at collection and mean temperature were available. Thus the equation used below is log L = 0.00139--0-0134 * T
(Equation 2)
Clutch size T h e content of the egg sacs (clutch size) of E. affinis showed extreme seasonal variability [Figure 2(c)]. T h e largest clutch had 79 eggs. In the beginning of February few egg sacs were found, but ovaries looked well developed and ready to spawn. F r o m low egg numbers in January clutch size increased dramatically to maximum size in April. Thereafter it decreased abruptly until a minimum was reached at the end of July. At this time very few
Egg production o f Eurytemora a~nis
399
TABLE 1. Comparison of female dry weight (~tg), fecundity (eggs female-J day-~), daily dry weight (B) specific egg production (EP) and somatic production (P) per dry weight of Eurytemora a O~nis and Acartia tonsa. Field observations or experiments, where females grew up at experimental temperatures (Heinle & Flemer, 1975) T °C
Dry weight
Eurytemora a_Oinis 0--25 2.16-7.35 5 6.24-8.25 10 4.80-5-40 15 3-14-3-24 20 2.14-2.33 25 1.54-1-68 5.5 8. I0 10 5.40 15 3.24 20 2.33 25 1.68 5-8-14-9 0-23 ? Acartia tonsa 15
8.50
20 25 12 15 20 26 15 20 14-23 20 20 20
6.00 4.50 7.00 7-00 5-30 5-7.25
Fecundity
EP/B
0.6-15-7 5"78 5-5 5-85 6.24 7.31
0.01-0.45 0.09--0.12 0.13-0.15 0'23 0.35-0.38 0.57-0.62
22 59 54
This study* 0"07 0"10 0"16 0.23 0.34 0.06 0.13 0-25 0-28 0.36 0-03-0.13 0.08--0.23 0.18-0.21
0.28 0.67 1"06
0.29 0.42-0.82
64 85 166
This study, model data ~
Heinle & Flemer, 1975 Burkill & Kendall, 1982 Christiansen, 1988 Amdt, 1985 Ambler, 1985b
0-23 0-41 0.58 0.58-0.87 50 70
Source
P/B
Miller et al., 1977 Dagg, 1977, mod. by Ambler, 1985 Beckman & Peterson, 1986 Christiansen, 1988 Durbin et al., 1983' Sullivan & Ritacco a Sullivan & Ritacco'
°See text. Female biomass calculated from length-weight conversion of Heinle & Flemer, 1975. bAssuming a factor of 2.5 for carbon to dry weight conversion. 'Enriched seawater. ~Tank experiment control. ~Tank experiment nutrient enriched. females w e r e c a r r y i n g egg sacs, a n d the eggs a p p e a r e d n o n - v i a b l e . E g g size varied b e t w e e n 7 8 - 9 0 lam ( m e a n 84 lam). T h e r e was no i n d i c a t i o n o f a relationship b e t w e e n egg size and b o d y size. T h e p o r t i o n o f female d r y w e i g h t d e p o s i t e d in each egg sac was calculated f r o m egg d r y w e i g h t (0" 13 lag e g g - t , H e i n l e & F l e m e r , 1975) a n d b o d y d r y weight. P r o s o m e l e n g t h was c o n v e r t e d into dry w e i g h t u s i n g existing l e n g t h - w e i g h t relationships for u n p r e s e r v e d E . affinis :
log W = 1'821 * L - 0 ' 6 5 4 , H e i n l e and F l e m e r (1975, P a t u x e n t R i v e r ) log W = 2-11 * L - 1"069, B 6 t t g e r (1979, Schlei) log W = 2.088 * L - 0 - 8 5 9 , Burkill and K e n d a l l (1982, Bristol C h a n n e l ) w h e r e W is dry w e i g h t (lag) a n d L is p r o s o m e l e n g t h (ram). All t h r e e e q u a t i o n s give c o m p a r a b l e results in the smaller size g r o u p , b u t d i v e r g e at p r o s o m e lengths > 0.75 m m
400
H.-J. Hirche
0.9
I
"~o-
I
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o~ 0.6 °'[i r
0-~
•
• ~
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I
0
i
i
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i
5
I
I
I0
15
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20
25
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Figure 3. Eurytemora a~inis. Pros•me length related to temperature at collection and mean temperature during development. For the regression curves numbered data (1: 22 January; 2:19 February; 3:17 March) were excluded. 0 , mean temperature; [], collection temperature.
20
-&
15
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[]
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C3
i OF i 0.5
i
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i
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I 0.7 Body
i
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length
r
I I 0.8
J
I
I
I I 0.9
J
r
p I 1.0
(mm)
Figure 4. Eurytemora affinis. Dry weights calculated from length-dry weight conversions from El, B6ttger (1979) for the Schlei Fjord, I , Heinle and Flemer (1975) for the Patuxent River estuary, and • , Burkill and Kendall (1982) for the Bristol Channel.
considerably, with the largest discrepancies between the relationship of B6ttger on one side and the other two relationships on the other (Figure 4). Depending on the dry weight conversion used, egg sacs have been estimated to contain 63.4+24.21 (B6ttger, 1979), 58.2 + 17.48 (Burkill & Kendall, 1982) or 56-3_ 16.6 (Heinle & Flemer, 1975) percent body dry weight. The seasonal variability of clutch size showed strong similarities to changes in body size [Figure 2(c)]. Comparison of the correlation coefficients (without the two January values) showed a much stronger relationship between clutch size (C) and body size (L) [r 2 = 0"872; Figure 5(b)] than between clutch size and temperature at collection [r2 = 0.56; Figure 5(a)]: log C = 1'9809 * L - 0.1229
(Equation 3)
Egg production of E u r y t e m o r a ~ i s
401
80
60
(o)
I
~ 2o 8,
0
I0 15 Temperolure
5
8c
(b~
20
:'5 I
Z
4O 2O
0.5
0"6
0-7 0.8 Body lengfh (mm)
0.9
I.O
Figure 5. Eurytemora affinis. Relationship between clutch size and temperature at collection (a) and prosome length (b). Values in circles were excluded from regression.
With respect to relatively fast egg developmental times, temperature at collection was assumed to be a sufficiently accurate measure of temperature during egg formation. T h e importance of body size was most evident in late winter, when the largest discrepancies occurred between body size and temperature at collection [Figure 5(b)]. It is thus concluded that clutch size is not directly related to temperature, but indirectly via body size, which is a function of temperature during larval development.
Fecundity and weight specific egg production Individual egg production rate (F, fecundity) was estimated from clutch size (C) and hatching time (H) by: F = C * 1/H
(Equation 4)
Hatching times were derived from an exponential fit to data from M c L a r e n (1969) and Heinle and Flemer (1975) from experiments at different temperatures (T). log H = 1.001 - 0.05578 * T
(Equation 5)
Hatching times of eggs at each station were calculated from this regression, using the temperatures at the time of sampling. D r y weight specific productivities (P) of mature females were calculated from egg numbers (this study), egg dry weights (0.13 lag, Heinle & Flemer, 1975), female weights (from length-weight relationships), and hatching time (H) by P = egg biomass/female biomass * I / H .
(Equation 6)
Fecundity showed a pronounced peak in the middle of April, coinciding with the maxima of female size and clutch size. A second, smaller peak occurred at the beginning of July [Figure 6(a)]. For the plot of dry weight specific egg production rate (P/B), the length-weight conversion of Burkill and Kendall (1982) was used, which is the intermediate of the three available conversions. Weight specific egg production reflected
402
H.-J. Hirche
i T
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"'
o
lallll
llilli
JIII
ii Illl
i l I I I ~l'-I
30 6 0 9 0 120 150 lEE) 210 240270300330360 Day
Figure 6. Eurytemora a Ofnis. Individual egg production rate (a) and weight specific egg production rate (b).
strongly the temperature dependence of productivity, with a P/B ratio of 0.01-0.02 d a y - ] (depending on length-weight conversion) in winter and 0.43-0-51 day -1 around the temperature m a x i m u m in s u m m e r [Figure 6(b)].
Model of temperature dependent fecundity and specific production T h e regressions of egg production with body size and temperature obtained from field samples make it possible to model general relationships between temperature and the before mentioned parameters. T h e effect of temperature on fecundity was estimated using relationships of hatching time (equation 5), body size (equation 2), and clutch size (equation 3) with temperature (T). As a result, fecundity (F) followed the quadratic equation F = 6"6072 - 0"206 * T + 0"00938 * T z
(Equation 7)
T h e m i n i m u m of this equation fell at 12 °C, while egg production rate at 0 °C was equal to that at 20 °C (Figure 8). For modelling of weight specific egg production (Figure 7), body size at different temperatures was calculated from equation (2). Clutch size was then derived from body size (equation 3) and hatching time was taken from equation (5). O f special interest was the comparison of specific egg production with somatic production of growing individuals at different temperatures. Somatic production (SP) was calculated using egg weight (0.13 lag) and adult weight (W) vs. time to reach adulthood (G), presuming exponential growth (Heinle & Flemer, 1975): SP = In W
-
In 0-13/G
(Equation 8)
T i m e to reach adulthood (G) at different temperatures (T) was calculated from a regression using an exponential fit to experimental data presented in Heinle and Flemer (1975): log G = 1"9636 - 0.04333 * T
(Equation 9)
Egg production o f E u r y t e m o r a affmis
07! 0.6
o "o
T
0-5
E o 25
0.4
403
[ ] EP/B B5 y = 0,03107 * T - 1.079 • EP/B HF y = 0.04141 * T - I . 2 5 0 0 P/B B5 y= 0"03493" T - 1"337 • P/B HF y= 0 . 0 3 1 8 7 " T - 1 - : > 8 9
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|
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I
I
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20
I
25
Temperature (°C)
Figure 7. Eurytemora a~inis. Comparison of weight specific production rates for egg production (EP/B) and somatic production (P/B) for different length-dry weight conversions (B6: B6ttger, 1979; HF: Heinle & Flemer, 1975; see text for equations).
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0
5
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I
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f
20
i
i
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i
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Temper•lure
Figure 8. Comparison of individual egg production rate of Eurytemora aj~nis (filled circles, equation 4) and Acartia tons• (open circles). Data for Eurytemora were derived from a model (see text). Clutch size was calculated from pros•me length at different temperatures (equations 2 and 3) and divided by hatching time (equation 5). 1: Ambler, 1985; 2: Dagg, 1977; 3: Sullivan & Ritacco, 1985; 4: Beckman & Peters•n, 1986; 5: Durbin et al., 1983.
Only at the lower temperatures are reproductive and somatic production similar (Figure 7), regardless of the length-weight conversion applied. Towards higher temperatures regressions for the two productive modes diverge considerably.
Discussion Highly significant relationships were observed between environmental temperature, body size and clutch size of E. affinis in the field, except for the winter population. These
404
H.-~. Hirche
relationships permit predictions of recruitment and specific production by females at food satiation from water temperature. In-situ egg counts permit estimation of food limitation by comparison with regression-derived m a x i m u m clutch size. This has been suggested by Runge (1985) and applied by Hirche et al. (1991). T h e excellent fit of clutch size with body size from the end of M a r c h onwards strongly indicates satiating food conditions for E. affinis in the Schlei during most of the year and hence m a x i m u m clutch size in our regression. Chlorophyll a concentrations reported by Schiemann [1974, data in Figure 2(a) from his tables in the Appendix for a station very close to station 1 of this study] show superabundant phytoplankton biomass from the beginning of March to September. T h e chlorophyll maxima in M a r c h and M a y were formed by small Chlorophyceae (1-4 ~tm), while in June and August blooms consisted mostly of Cyanophyceae (J/irgens, pers. comm. in Schiemann, 1974). In general, most of the phytoplankton was in the size range < 60 ~tm (Schiemann, 1974). Direct observations orE. affinis suggest that they are capable of feeding on particles within the range 2 to 60 ~tm (Heinle & Flemer, 1975; Heinle et al., 1977). Only in winter during ice cover were chlorophyll concentrations low. T h u s food limitation may at least partly explain the smaller than expected clutches. In addition, the extreme longevity of females of the early spring p o p u lation, which was indicated by the length-temperature relationship, may have contributed to reduced clutch size through senescent ovaries. It is known, that m a x i m u m egg production is only maintained over a short period in small copepods (Sciandra et al., 1990). As the effect of longevity upon the egg production orE. affinis is not yet understood, prediction of clutch size from body size should be handled with caution at low temperatures, where female survival may be considerable. Productivities measured by Heinle and Flemer (1975) in the Patuxent River estuary during February and April were at some of their stations about one half as great as those predicted from the laboratory studies, suggesting that the supply of food was limiting the production of E. affinis. D u e to the different temperature regime in the Patuxent, the period of food limitation covered a m u c h wider temperature range than in the Schlei and may so have disguised the relationships established during this study. Heinle and Flemer (1975) found larger clutches at some of their stations at low temperatures. T h e i r m a x i m u m was 84.4 as compared to 69 eggs clutch- 1in this study. However, this may relate to the size of their females, which were up to 14% larger and hence up to 80% heavier. Wherever the seasonal cycle ofE. affinis was studied, its disappearance with the s u m m e r warming and succession by other copepods, mostly Acartia tonsa, was a common feature, which has puzzled investigators. According to Bradley (1975), the seasonal distribution of E. affinis is contrary to that expected from thermal tolerance-salinity relationships. Explanations offered are predation by or competition with other species. In its habitat, E. affinis is certainly exposed to strong predation pressure, and Heinle and Flemer (1975) related the decline of E. affinis in the Patuxent in the spring to predation by the Opossum shrimp Neomysis americana. I n addition Christiansen (1988) suggested the mortality of E. affinis in the Schlei was mostly caused by the large n u m b e r offish larvae in this area. However, unless there is selective predation, other copepod species should also be affected as m u c h as E. affinis, yet Heinle (1970) found that predation less strongly affected E. affinis than A. tonsa. I n contrast, Baretta and Malschaert (1988) argue that E. affinis is more strongly affected by predation than A . tonsa and they relate this to different strategies of egg deposition of the two species. Egg sacs would slow down E. affinis when trying to avoid predators, while A . tonsa, which spawns the eggs free in the water, would escape faster. In addition, predation on egg-carrying female E. affinis would entail the loss of the current
Egg production of Eurytemora affinis
405
batch of eggs, whereas in A . tonsa the eggs already spawned would still contribute to the propagation of the species. Direct predation o f A . tonsa on nauplii of other species has also to be taken into consideration according to observations by Lonsdale et al. (1979). Heinle (1970) pointed to physiological differences between E. affinis and A . tonsa: while the growth rate and productivity o r E . affinis were equal to that o f A . tonsa at 12 °C, they were only half as great at 25 °C. Baretta and Malschaert (1988) related the virtual disappearance of A. tonsa from the E m s estuary in winter to decreasing egg production at low temperatures combined with reduced survival of the few eggs due to long development times. T h e dominance of E. affinis in winter and spring was explained by these authors by the advantage of carrying egg sacs. T h e results of the present study also indicate, that reproductive strategy may be one of the key factors determining the seasonal distribution patterns of E. affinis. Its k-strategy expressed in carrying few large eggs in sacs seems to yield sufficient recruitment at lower temperatures. T h r o u g h the observed close coupling of clutch size and body size a strong effect of the enormous size decrease on their reproductive success at higher temperatures is expected. T h e difference in size that occurred at the extremes of the temperature range---variation in prosome length from 0.45 to 1.05 m m corresponding to a change in dry weight from 1-2/1-58 to 9-46/21.55 lag, depending on length-weight conversion--is among the greatest reported. As egg size seems to be invariant, at temperatures > 25 °C E. affinis females apparently reach anatomical limits for egg deposition. Decreasing female size counterbalances the effect of shorter hatching times at higher temperatures. Model data showed that different temperature coefficients for hatching times and body size resulted in decreased fecundity at increased temperatures in the 0 to 12 °C range (Figure 8). T h e fecundity m i n i m u m at ca. 12 °C coincides with the temperature [sensu ' mean temperature during ontogenetic development ', see Figure 5(a)], when E. affinis populations often start decreasing in the field. Acartia tonsa is not competing at low temperatures in spring as it mostly overwinters in the m u d as resting eggs (Zillioux & Gonzalez, 1972). It becomes abundant when eggs hatch at temperatures > 10 °C (Zillioux & Gonzalez, 1972; Christiansen, 1988). Comparison of reproductive strategies reveals clearly the differences between both species. A . tonsa is a r-strategist with a fecundity up to one order of magnitude higher than that of E. affinis (Figure 8). This higher fecundity goes along with larger females and smaller eggs, but also with higher weight specific production. Prosomes of A . tonsa females between M a y and October were generally ca. 100 lam longer in the Schlei (Christiansen, 1988). M o r e examples for body weights from field collections are presented in T a b l e 1. Female A . tonsa are often two or three times heavier than E. affinis. A n egg diameter of 73 lam in A . tonsa (Ambler, 1985) compares with 82 lam in E. affinis. Although there are some discrepancies in reports on egg carbon content of A. tonsa (0"028 lag: Heinle, 1966; Miller et al., 1977; 0"031 lag: D u r b i n & Durbin, 1981; Ambler, 1985; 0.046 lag: Kiorboe et al., 1985; 0"05 lag: Landry, 1983), most of the measurements indicate egg weights half that ofE. affinis, when a dry weight content of 40% carbon is assumed. Comparative data for weight specific egg production at different temperatures (Table 1) clearly show the considerably higher rate for A . tonsa at all temperatures where both species usually co-occur. This may lead to disappearance ofE. affinis in summer, when predation pressure is high on both species. As E. affinis reproduces over a wider temperature range with little variability in fecundity, at higher latitudes with lower temperature maxima it may maintain a significant population over the whole year. T h u s , seasonal resource partitioning by the two species is maintained by k-strategy at lower temperatures, with E. affinis carrying few large eggs, and r-strategy
406
H.-J. Hirche
in s u m m e r , w i t h A . tonsa d e p o s i t i n g m a n y small eggs. S i n k i n g s p e e d a n d d e v e l o p m e n t a l t i m e o f eggs m a y be critical p a r a m e t e r s d e t e r m i n i n g the success o f free egg d e p o s i t i o n in shallow waters, w h e r e they often m a y b e eaten b y p r e d a t o r s o r d e t e r i o r a t e u n d e r anoxic conditions. F o r Acartia clausi, A . tonsa a n d Eurytemora herdmani, r e a r e d in a b u n d a n t food c o n ditions, eggs are p r o d u c e d at the same i n s t a n t a n e o u s rate as p r e v i o u s somatic p r o d u c t i o n ( S e k i g u c h i et al., 1980; M c L a r e n & C o r k e t t , 1981; B e r g r e e n et al., 1988). T h i s w o u l d p e r m i t p r e d i c t i o n o f somatic p r o d u c t i o n f r o m c l u t c h size counts in E. affinis. H o w ever, w i t h t h e values c h o s e n h e r e , P/B for s o m a t i c p r o d u c t i o n has a s m a l l e r t e m p e r a t u r e coefficient t h a n egg p r o d u c t i o n ; o n l y at lower t e m p e r a t u r e s are values similar. T h e r e is g o o d a g r e e m e n t b e t w e e n P/B calculation b a s e d on results o f this s t u d y a n d field estimates f r o m c o h o r t analysis ( A r n d t , 1985; C h r i s t i a n s e n , 1988, T a b l e 1) a n d w i t h l a b o r a t o r y e x p e r i m e n t s w i t h females r e a r e d at different t e m p e r a t u r e s ( H e i n l e & F l e m e r , 1975). T h e d a t a in T a b l e 1 s h o w that in a d d i t i o n to r e p r o d u c t i o n also s o m a t i c p r o d u c t i o n is g r e a t e r in A . tonsa t h a n in E. affinis at h i g h e r t e m p e r a t u r e s . F o r calculations o f various expressions o f p r o d u c t i v i t y in this s t u d y , d e v e l o p m e n t a l times o f eggs a n d larvae have b e e n t a k e n f r o m the literature. O f t e n these values were d e r i v e d after e x p o s i n g eggs a n d n a u p l i i f r o m females raised at one t e m p e r a t u r e to various o t h e r t e m p e r a t u r e regimes. T e m p e r a t u r e a c c l i m a t i o n o f these rates has r a r e l y b e e n s t u d i e d , a l t h o u g h it is c o m m o n sense t h a t it affects m a n y m e t a b o l i c activities. T h e n e e d o f such i n f o r m a t i o n for p r e d i c t i n g g r o w t h a n d p r o d u c t i o n s h o u l d s t i m u l a t e r e s e a r c h in this field.
Acknowledgements T h e h e l p o f T . B r e y in m a t h e m a t i c a l questions is greatly a c k n o w l e d g e d . T h i s is p u b l i c a t i o n no. 195 o f the A l f r e d - W e g e n e r - I n s t i t u t e for P o l a r a n d M a r i n e R e s e a r c h .
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Egg production of E u r y t e m o r a affinis
407
Durbin, E. G., Durbin, A. G., Smayda, T. J. & Verity, P. G. 1983 Food limitation of production by adult Acartia tonsa in Narragansett Bay. Rhode Island. Limnology and Oceanography 28, 1199-1213. Gfidge, U. 1988 Analyse experimenteller Daten und Simulationsrechnungen zur Populationsdynamik und Koexistenz von calanoiden Copepoden im Ems-Dollart-•stuar. Ph.D. Thesis, University Oldenburg, 88 pp. Grasshof, K. 1976 Methods of seawater analysis. Verlag Chemic, Weinheim, New York, 317 pp. Gyllenberg, G. 1980 Feeding of the copepod Eurytemora hirundoides (Crustacea) on the different algal cultures. Annales ZoologiciFennici 17, 181-184. Hart, R. C. & McLaren, I. A. 1978 Temperature acclimation and other influences on embryonic duration in the copepod Pseudocalanus. Marine Biology 45, 23-30. Heerkloss, R. 1979 Selektivitiit der Nahrungsaufnahme, Ingestionsrate und Faecesabgabe bei Eurytemora affinis (Poppe) (Calanoida, Copepoda). Wissenschaftliche Zeitschrift der Universitiit Rostock, Mathematisch-naturzoissenschaftliche Reihe 28, 525-529. Heinle, D. R. 1966 Production of a calanoid copepod, Acartia tonsa, in the Patuxent River estuary. Chesapeake Science 7, 59-74. Heinle, D. R. 1969 Temperature and zooplankton. Chesapeake Science 10, 186-209. Heinle, D. R. 1970 Population dynamics of exploited cultures of calanoid copepods. Helgoliinder wissenschaftliche Meeresuntersuchungen 20, 360-372. Heinle, D. R. & Flemer, D. A. 1975 Carbon requirements of a population of the estuarine copepod Eurytemora affinis. Marine Biology 31,235-247. Heinle, D. R., Harris, R. P., Ustach, J. F. & Flemer, D. A. 1977 Detritus as food for estuarine copepods. Marine Biology 40, 341-353. Hirche, H.-J. 1974 Die Copepoden Eurytemora affinis Poppe und Acartia tonsa Dana und ihre Besiedelung dutch Myoschiston centropagidarum Precht (Peritricha) in der Schlei. Kieler Meeresforschungen 30, 43-64. Hirche, H.-J., Baumann, M. E. 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