cryptic predation and the demographic strategy of two

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JENS PETTER NILSSEN. Zoological Institute, University of ... (Berg and Grimaldi,. 1966; Jacobsen, 1974). ... Accordingly, Berg and. Grimaldi (1966) found that ...
Memorie dell'Zstituto Ztaliano di Zdrobiologia

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J E N S P E T T E R NILSSEN Zoological Institute, University of Oslo, P.O. Box 1050, Blindern, Oslo 3, Norway.

CRYPTIC PREDATION AND THE DEMOGRAPHIC STRATEGY OF TWO LIMNETIC CYCLOPOID COPEPODS Abetract

Fish predation on cyclopoid copepods, although of little energetic importance to fish and restricted to a short period of time, probably determines the demographic strategies of cyclopoid copepods in a n~imber of lakes.

INTRODGCTION. Cyclopoid copepods often overwinter in distinct developmental stages (Elgmork, 1967; Elgnlork and Nilssen, 1977). I n most cases, a part of the popula,tion consists of nauplii and early copepodids (fraction A), and the other part consists of advanced copepodids (fraction B; Lindstrom, 1952, 1958; Axelson, 1961; Lotmarker, 1964 ; Halvorsen and Elgmork, 1976), which frequently undergo diapause in the bottom sediments( Elgmork, 1967; Elgmork and Nilssen, 1977; Smyly, 1973). The adaptive significance of the separation of the population into fractions has not yet been adequately discussed. An attempt is made here to explain the phenomenon in terms of fish predation. T H E IMPACT O F F I S H PREDATJON ON CYCLOPOID COPEPODS. Cyclopoid copepods generalIy are not considerod susceptible to fish predation (Allan, 1976). They are, however, eaten during winter and early spring by ~Yalmotrutta (Klementsen, 1967/68), Salvelinus alpinus (Nilsson, 1960; Matzow, Huru, Jonsson, Kvammen, Nilssen, Sandlund and Ostli, 1976) and Coregonus spp. (Berg and Grimaldi, 1966; Jacobsen, 1974). This may be due to the copepods' strong pigmentation, contagious distribution, and reduced locomotory activity during winter (see Confer and Blades, 1975; Strickler, 1975; Nilssen, unpubl. data). Fig. 1 shows fish predation on Cyclops abyssorurn (adult fema.le length 1.6 mm) and C. scutifer (adult femde length 1.3-1.4 mm)

Mem. Isl. Ital. Idrobiol., 34: 187-196. 1977.

J. P. Nilssen

M J J A S O N D J F M A M J J 1972 1973 Fig. 1 - Fish predation interest in Cyclops abyssorum -( ) and C. sculifer (- - - -) during May 1972-July 1973 in Lenavatn lake, western Norway (Matzow and Nilssen, unpubl. data). Fish predation interest is defined as the ratio (X100) between the numbers of cyclopoid copepods and the cladoceran Bosmina longispina in the stomachs of char, Salvelinus alpinus. During winter char mostly eat bottom organisms. The period of dlapause in C. abyssorum is indicated with a thick black line (Nilssen and Elgmork, 1977).

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over a period of 14 month. I t should be added that fish selected the advanced copepodids and adults within each species. Nauplii and copepodids 1-111 were never recorded in the stomachs of fish (Ma-tzow and Nilssen, unpubl. data). Predation on the larger species C . abyssorum is restricted to the periods of initiation and termination of the diapause (Nilssen, 1975); the smaller species C . scutifer is eaten all over the w-inter (see Klementsen, 1967!68). Another observation concerned with fish predation on two cyclopoid copepods of different size was made in lake Haugatjern (Jacobsen, 1974). Dining winter and early spring both the larger species Megacyclops gigas and the smaller species C . scutifer were present a t the samo time in the open water. C. scutifeer was eaten only when M. yigas migrated from the pelagid towards the benthic region, which provided a refuge from predation. This demonstrates that planktivorous fish could select C . ab?jssorum if it should co-occur with C . scutifer in a non-diapaiise phase in the limnetic zone of lake Lsnavatn during winter. Accordingly, Berg and Grimaldi (1966) found that plankton-eating fish strongly selected pelagic C. abysswum during winter and early spring in Lago Maggiore. The ratio between the size-refuge fraction A and the predationvulnerable fraction B in plankton during winter may be assumed to reflect the degree of fish predation in the lake. Generally in lakes with heavy predation pressure the A!B ratio is high; in lakes with less predation i t is lower (Fig. 2). This suggestion may seem sweeping if based only on the 19 investigated lakes from Norway and Sweden, but the resiilts from previous studies on 13 lakes by Lotmarker (1964) are in agreement, even though winter samples were not taken. The observed spring reproduction of C. scutif~rwith increasing predation pressure by fish is negligible compared with the autumn reproduction. The strength of predation not only depends on the fish species present, hut also on their numbers and feeding habits. Non-uniform data for mixed trout and char populations probably reflect the numbers of char present (cf. Nilsson, 1972). The addition of Coregonus spp. does not modify the A/B ratio, indicating that the plankton community is already considerably exploited by char (cf. Nilsson, 1972). The A!B ratio increases in a population when trout is mainly planktivorous (Fig. 2, M). SEAqONAL VARIATION I N FECUNDITY. Fig. 3 illustrates ~easonalvariation in fecundity in some selected populations of C. abyssorurn and C . scutifm. It is clear that fecundity is highest in spring and early summer. The fecundity of populations not splitted into fractions, as in lake Lsnavatn (Nilssen and Elgmork, 1977), appears to bo stable throughout the breeding season (Fig. 3). Thus, because of fecundity alone, i t would probably be of

INCREASING PREDATION PRESSURE Mg. 2 - The ratio between nauplii plus small cope1)odids and advanced copepodids in C. sculi/er (AIR, see text for further explanations) in winter, related t o fish predation pressure. 1: brown trout alone, 2: brown trout and char, 3: brown trout, char and whitefish (from Lindstriim, 1952, 1958: Nilssen, unpubl. data). M: plankton-eating trout, N: char present only in small numbers. Line drawn through mean value for the dinerent classes on the abscissa.

selective advantage for the population not to split into fractions and have reproduction in the spring. These curves are also consistent in the case of females, living from spring to autumn, produce clutches with subsequent smaller numbers of eggs per sac. A closer study of the reproductive strategy of these copepods (Nilssen, in prep.) concludes that females from

Cryptic predalion and the demographic slralegy of two limnelic cyclopoid copepods

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Fig. 3 - Seasonal variation in fecundity of dinerent populations of Cyclops abyssorum and C . sculifer. Fecundity is used equivalent t o clutch slxe. Filled in squares: females originating from the winter B fraction; fllled in dotts: females originating from the winter A fraction; note a certain overlap between t h e two fractions. L : Lake Lnnavatn. (After Walker, 1970; Smyly, 1973; Halvorsen and Elgmork, 1976; Nilssen and Elgmork, 1977; Lie, pers. comm.).

the B fraction reproduce and die after having produced relatircly few clutches. The eggs produced during autumn derive from females originating from the winter A fraction.

FISH PREDATION AND POPULATION STRATEGIES. I n most cases we lack information on fish predation pressure when outlining the life cycles of cyclopoid copepods. Authors studying life cycles have generally tried to correlate them with abiotic factors. Only recently also biological factors have been related to the initiation of diapause in C. saatifer (Strickler and Twombly, 1975). Fourth copepodids of C. soutifer (length about 1 mm and weakly pigmented) are eaten by fish during winter (Fig. 1)..The copepod population remains within the first 5 m above the bottom sediments (Nilssen, unpubl. data), which are also the most suitable habit'at for 8. alpinus in the same period (Matzow, Huru, Jonsson, Kvammen, Nilssen, Sandlund and Ostli, 1976). I n contrast with C. soulifer, C. abyssorurn enters diapause from autumn until spring (Nilssen and Elgmork, 1977). This species [conspicuously coloured by oil droplets full of carotenoids, and with a length of about 1.5 mm a t the stage

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of copepodid V (Nilssen and Elgmork, 1977)], would probably be an attractive prey for 8. alpinus during winter (cf. Berg and Grimaldi, 1966), if i t did not have a refuge in the sediment. Predation pressure in the sediment is little known, but it is probably not so heavy (Elgmork, 1959; Mittelholzer, 1970). Diapause in C. abyssorum stops a t the same time as its most important predator shifts its interest to Chironomidae and then to Cladocera (Matzow, H,uru, Jonsson, Kvammen, Nilssen, Sandlund and Oslti, 1976). I11 this case, the timing probably saves i t from heavy predation a t the time of maturity, when i t might otherwise be strongly selected for (Gliwicz, 1967). Some fishes a t this time had their stomachs filled with copepodids in advanced stages and adult,s: as many 23.000 G. ahys,~orumwere found in a single stomach. I n lakes in castern and southern Norway, where C. abyssorum spend the winter in the hypolimnion mostly as fifth copepodid (Nilssen unpubl. data), i t occurs in very sma.11 numbers (Strem, 1932; Nilssen unpubl. data). This may reflect its vulnerability to fish predation. Another strategy operates in C. scutifer for the protection of itls offspring. Advanced copepodids suffer from fish predation, wliilc nauplii and early copepodids do not, as fish predation is nearly zero in this size group. Adults derived from the winter nauplii and young copepodites (fraction A) are far less fecund that the spring reproductive fraction (see Fig. 3). Therefore i t might be expected that the total biomass of G . scutifer in different lakes would be inversely related to fish predation pressure, and this exactly has been observed (Fig. 4). EVOLUTIONARY CONSEQUENCES. Different strategies operate for cyclopoid copepods in different aquatic environments to ensure reproductive success. As a result of strong predation pressure from plankton-eating fish C. abyssorum, during a potentially vulnerable period, probably uses the bottom sediment as a refuge. (J. scutifer, on the other hand, remains in. the pelagic water in two fractions: one potentially more fertile but subject to predation, the other far less fertile but with a refuge from predation due to its small size. Adults of C . abyssorum (Fryer, 1957; Walker, 1970) and C. scutifer (Paveljeva and Sorokin, 1971) are mainly carnivorous. For this rcason selection would counteract., having one fraction of the population present as adults, which would graze down the biomass of its own nauplii (McQueen, 1969; Anderson, 1970). If planktivorous fish were present, the adults would suffer a considerable predation due to their larger size. I t is often emphasized that cyclopoid copepods are not greatly influenced by fish predation. This study suggests t,hat predation

Cryptic predation and the demographic strategy of two limnetic cyclopoid copepods 193

INCREASING PREDATION PRESSURE Fig. 4 - Numbers of C. scutifer related to flsh predation pressure in different localities (mainly based on Lotmarker, 1964; Nilssen unpubl. data). Line drawn through mean value for the different classes on the abscissa.

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from fish, although often not heavy and limited in time, largely determines the demographic strategies of cyclopoid copepods in a number of lakes.

I want to thank Dr. R. Stewart Anderson, University of .Calgary, Canada, Dr.philos E r e Elgmork, University of Oslo, Norway for having read and commented this paper, and Dr. Tom Lotmarker, Museum of Natural History, Stockholm for supplying unpublished data on this lakes. Cand. real. Sigmund Lie kindly aJlowed me to include unpublished data from his Thesis in part of Fig. 3. This study was supported in part by Professor R. Collett's endowment and The Norwegian Research Council for Science and Humanities.

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Kltmentsen, A. 1967168. On the feeding habits of the population of brown trout (Salmo trulta L.) in Jelstervann, west Norway, with special reference to the utllization of planktonic crustaceans. Norw. J . Zool., 15: 50-67. Lindstrijm, T. 1952. Sur 1'Bcologie du zooplankton CrustacB. Rep. Znsl. Freshu~al. Zfes. Drollningholm, 33: 70-165.

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Lindstram, T. 1958. Observations sur les cycles annuels des plancton crustacbs. Rep. Znsf. Freshwaf. Res. Droffningholm, 39: 99-145. LtNmarker, T. 1964. Studies on planktonic crustacea in thirteen lakes in northern Sweden. Rep. Znsf. Freshwaf. Res. Droffningholm, 45: 113-189. Matzow. D. led.). H. Hum. B. Jonsson. P. I. Kvammen. J. P. Nilssen. 0. T. Sandlund and T. '0stk 1976. ~krskvannsekolo~iske undersekelser i ~ s n a v a t nog Strandaelva 1972-1974 (Freshwater biological investigations in Lsnavatn lake and . Uniu. Oslo 1: 1-235 Strandaelva river 1972-1974). Rep. V o s s ~ r o j e c l ; ~ o o lZnsf. (mimeogr. in Norwegian, English summary). McQueen, D. J. 1969. Reduction of zooplankton standing stocks by predaceous Cyclops bicuspidafus fhomasi in Marion Lake, British Columbia. J. Fish. Res. Bd Can., 26: 1605-1618. Mittelholzer, E. 1970. Populationsdynamik und Produktion des Zooplanktons im Greifensee und im Vierwaldstiittersee. Schweiz. 2. Hydrol., 32: 90-149. Nilssen, J. P. 1975. Cyclops abyssorum, Sars 1863-en sfudie au dens faxonomi og ekologi (Cyclops abyssorum, Sars 1863-a sfudy of i f s fazonomy and ecology). Unpubl. Thesis Part 11. Univ. Oslo. 129 pp. (mimeogr. in Norwegian). Nilssen, J. P. and K. Elgmork. 1977. Cyclops abyssorum - Life cycle dynamics and habitat selection. Mem. Zsf. Zfal. Zdrobiol., 34: 197-236. Nilsson. N.-A. 1960. Seasonal fluctuations in the food segregation of trout, char and whitefish in 14 North Swedish lakes. Rep. Znsf. Freshluaf. Res. Droffningholm, 41: 185-205. Nilsson, N.-A. 1972. EtTects of introductions of salmonids into barren lakes. J. Fish. Res. Bd Can., 29: 693-697. Pavcljcva, E. B. and Y. I. Sorokin. 1971. The studies of nutrition of zooplankton of Lake Dalnee (Kamchatka). Trans. Znsf. Inland Wafers Acad. Sci. U S S R , 22: 56-63 (in Russian). Smyly, W. J. P. 1973. Bionomics of Cyclops sfrenuus abyssorum (Sars). Oecologia (Berl.), 11: 163-186. Strickler, J. R. 1975. Swimming of planktonic Cyclops species (Copepoda, Crustacea): pattern, movements and their control. In: Wu, T.Y.-T., C. J. Rrokaw and C. Brennen (Eds.), Swimming and flying in nafure. Plenum Press, New York and London: 599-613. Strickler, J. R. and S. Twombly. 1975. Reynolds number, diapause and predatory copepods. Verh. Infernal. Verein. Zmnol,, 19: 2943-2950. Strem, K. M. 1932. Tyrifjord - a limnological study. Skr. VidenskSelsk. Oslo Mat.natwu. Kl.: 1-84. Walker, A. F. 1970. The zooplankton of Loch Leuen. Thesis, Dept. Biol., Univ. Sterling (mimeogr. in English): 123 pp.