migration of zooplankton

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1 Functional Ecology 1989, ESSAY REVIEW 3, The adaptive significance of die1 vertical migration of zooplankton W. LAMPERT Department of Physiological Ecology, Max Planck Institute of Limnology, Postfach 165, 2330 Plon, Federal Republic of Germany Key-words: Zooplankton, diel vertical migration, adaptive value, metabolic advantage, visual predation, tradeoffs, demographic consequences, photo-protection The phenomenon Many taxa of both marine and freshwater zooplankton perform diel vertical migrations with amplitudes from a few to 100 metres (Hutchinson, 1967). The 'normal' pattern is an evening ascent and a morning descent, though several cases of 'reversed' migrations have been described (Ohman, Frost & Cohen, 1983; Bayly, 1986). Migrating animals spend the day in deep waters but stay near the surface at night. The amplitude of the movements and the shape of the vertical distribution of the population may be very different between species and between ontogenetic stages of the same species and may be influenced by factors like turbitiy and food abundance (Bohrer, 1980; George, 1983). Zooplankton may either migrate up and down together in a narrow band or may be sharply stratified in deep waters during the day but spread throughout the entire water column at night. However, what we observe are only changes in the population density at different depths of the water column. When taking plankton samples from different water layers, we obtain a vertical profile of animal abundances. Shifts in these vertical distributions are usually interpreted as movements of the population and day-night differences between means or medians of the distributions serve as measures of the vertical range of migration. However, such population responses may be seriously misleading in terms of the behaviour of constituent individuals (Pearre, 1979a). Individuals may vary speed and direction of their movements, so that at any time some animals move upwards while others rest or move downwards. The movement of the population reflects only the net effect. The distance between the mean depths of a population at different times equals the distance travelled by an individual only if all animals migrate synchronously. Otherwise, the movement of an individual can be considerably underestimated. As it is not possible to track small individual zooplankton in situ, this problem is still not solved. In the sixties, the main concern of investigators of vertical migration was the neurophysiological basis of the rhythmic behaviour. Behavioural physiology tried to identify the stimuli for initiation and direction of the migration. The relative change of light intensity has been found to be the proximate cue that controls the upwards and downwards movements. At least in Daphnia, the reaction depends on the level of light adaptation of the animal's eye (Siebeck, 1960; Ringelberg, 1964; McNaught & Hasler, 1964; Ringelberg, Van Kasteel & Servaas, 1967). Today the focus of most research on vertical migration has shifted from the environmental control towards the search for ultimate reasons. The problem The presence of vertical migration in so many taxa suggests that it has some adaptive value. Although there is no reason to believe that the same ultimate factor drives migration in all taxa, it is interesting that all migrating filter-feeding zooplankton experience similar disadvantageous environmental conditions. This effect is principally similar in freshwater and in the sea but may be more pronounced in stratified lakes. Migrating animals spend the night in warm food-rich surface waters but they leave this advantageous environment during the day to stay in the cold hypolimnion where quantity and quality of food are low. Thus, several costs are associated with migration. Reduced food availability results in slower growth and lower fecundity. The developmental time of the eggs carried by females is prolonged at the lower temperatures. Moreover, swimming up and

2 22 down the water column needs energy. These costs W.Lampert must result in reduced fitness of migrating animals compared to those that stay in the surface waters all day long. However, since they migrate, it is reasonable to suppose that there must be a selective force that favours migration behaviour. This apparent paradox has puzzled plankton ecologists for several years. A large variety of competing hypotheses have been offered to explain the adaptive value of vertical migration. The majority of them can be grouped in two categories according to the different components of fitness they emphasize: (1)Vertical migration provides a metabolic or demographic advantage. (2) Avoidance of surface waters during the day reduces the light-dependent mortality risk. A third group is not directly related to individual fitness, but proposes optimum exploitation strategies of food resources. Adaptive value Metabolic and demographic advantage The idea that migrating zooplankton may have a metabolic advantage over non-migrating ones was proposed by McLaren (1963). He estimated an energetic bonus for copepods feeding at night in the warm, food-rich waters and resting in the cold during the day. However, besides the energetic bonus, there is a retardation of development at low temperatures. So McLaren (1974) modified the original hypothesis by constructing a possible demographic advantage. Copepods growing at lower temperatures may reach larger adult body size. Provided there are non-limiting food conditions and fecundity of large specimens is higher than that of smaller ones, this may result in a demographic advantage. McLaren himself pointed out that his model required some restrictive assumptions. For example, he had to assume that adult stages stayed in the epilimnion, which is not in accordance with most field observations. Also, Lock & McLaren (1970) had shown that copepods raised under fluctuating temperature conditions did not grow to larger sizes than those kept at a constant average temperature. Kerfoot (1985) criticized the demographic advantage hypothesis rigorously by clearly pointing out that increased fecundity cannot compensate for the negative effect of decreased temperature on the rate of population growth (r). All attempts to test McLaren's hypothesis have failed to demonstrate a reproductive advantage of migrating zooplankton. Larvae of Chaoborus trivittatus Loew gained no energetic benefit under simulated vertical migration conditions in laboratory experiments of Swift (1976). More information is available for various Daphnia species. Good luck provided Stich & Lampert (1981) with a field test. They found two Daphnia species in Lake Constance that, albeit being morphologically very similar, showed pronounced differences in their migration behaviour. Daphnia galeata Sars and Daphnia hyalina Leydig are so closely related that they even form hybrids (Wolf & Mort, 1986), but D. hyalina performs diel migrations of more than 40 meters amplitude, while D. galeata migrates very little and stays in the epilimnion all day long. If diel vertical migration has a metabolic or demographic advantage, this must be reflected in a higher reproductive output of D. hyalina. However, just the opposite was found: D. hyalina has fewer eggs than D. galeata and, moreover, the eggs develop much more slowly than those of D. galeata. Laboratory experiments have confirmed these field observations. Orcutt & Porter (1983) and Manca, DeBernardi & Savia (1986) constructed life tables for Daphnia under several fluctuating and constant temperature conditions. Although reproductive patterns differed between treatments, there was no indication that fluctuating temperatures increased r. Daphnids grown under the highest constant temperature always had the highest reproductive output. Orcutt & Porter (1983) clearly point out that the difference between a migration and non-migration strategy is not fluctuating versus average constant temperature but fluctuating versus maximum temperature in the cycle. The differences between the two strategies were even more pronounced in the only study that varied temperature and food simultaneously in a diel cycle (Stich & Lampert, 1984). Although there were slight differences between the two species that perform different migration patterns in Lake Constance, both of them grew faster and had considerably higher reproductive output under non-migration conditions. These results corroborate the field observations and suggest that, at least in daphnids, vertical migration is energetically disadvantageous. Energy conservation However, additional assumptions revived the idea of a metabolic advantage, Geller (1986) proposed a 'starvation avoidance hypothesis', based on data on the Lake Constance Daphnia populations. Though it is difficult to understand how natural

3 23 selection can favour a seasonally-stable, high Die1 vertical population density in a parthenogenetic species, migration his basic idea is that migrating daphnids use a 'conservation' strategy to avoid population fluctuations. During spring, when food is very abundant, both Daphnia species utilize an 'exploitative' strategy to build up a high population density and do not migrate. D. hyalina switches to the 'conservation' strategy when, during summer, food supply is unpredictable, so that periods of starvation may occur. Energy losses during starvation in the warm epilimnion would be higher than in the cold hypolimnion, causing elevated mortality of juveniles of the surfacedwelling animals and severe population fluctuations. In the cold, daphnids can retain energy, survive longer and show dampened fluctuations. Vertical migration arises from the need to gain energy that is not available in the deep water. To enforce the energy gain, Geller (1986) assumed a mechanism of temperature acclimation as found in marine littoral snails (Somero & Hochachka, 1976). Feeding and respiration of cold acclimated animals are supposed to respond differently to variations in temperature. If the feeding rate increases steeply with raising temperature in the epilimnion, while the respiratory rate responds to a lesser extent, migrating animals will achieve a net gain of energy to partly compensate the starvation losses. However, to date this effect has not been demonstrated in any zooplankton. Resource related hypotheses Enright (1977) was the first to incorporate feedbacks between filter-feeding zooplankton and their algal prey into a metabolic model. His model differed from McLaren's (1963) in two additional assumptions: (1)Since photosynthesis takes place during the day, but only losses (respiration, grazing) occur at night, algal biomass must be greater in the evening than in the morning. Algal quality must also be different as the cells will be filled with reserves at dusk. (2) Animals returning to the surface after several hours of starvation will feed at enhanced rates. They may compensate for the day-time starvation by feeding in the evening at elevated rates on algae of higher abundance and quality. As respiratory losses are low during the starvation period in the cold hypolimnion, migrating animals may, thus, gain an energetic profit. Contrary to the other metabolic-advantage hypotheses that cannot explain why the animals migrate at certain times of the day, Enright's model incorporates the timing of migration. It predicts that zooplankton should not arrive at the surface in complete darkness but before dusk. This prediction has been tested by three series of detailed sampling of the marine copepod Calanus (Enright & Honegger, 1977). The predicted pattern was found in only one series, so the authors concluded that other factors were modifying the migration behaviour. The new hypothesis and the associated test initiated considerable debate. A series of comments was published in response (Pearre, 1979b; Koslow, 1979; Miller, 1979; Enright, 1979). In defence of his hypothesis, Enright (1979) pointed out that he had predicted an unexpected phenomenon, and that this phenomenon had been observed later - at least sometimes. Thus his hypothesis could not be refuted. However, Pearre (1979b) raised the question if copepods that ascend before sunset also feed before sunset - which is basic to Enright's interpretation. A recent study (M.J. Dagg, unpublished), using the gutfluorescence method (Mackas & Bohrer, 1976), confirmed the early ascent of Calanus but found their guts to be empty before sunset. The Enright model implies additional physiological assumptions that can be tested. For example, enhancement of the feeding rate by starvation is a critical proposition. The model requires that the starvation effect occurs at low food concentrations and also lasts for some hours. Some laboratory experiments supported both assumptions (Runge, 1980) or at least one of them (Ringelberg & Royackers, 1985; Mackas & Burns, 1986). Others did not find the enhancement at low concentrations (McMahon & Rigler, 1965; Frost, 1972; Lampert, Schmitt & Muck, 1988), but a rapid decline of the hunger response when the animals received food, especially in Daphnia. Therefore, experimental evidence suggests that the Enright model cannot be applied to Daphnia. Although copepods seem to be better adapted to changing food conditions than cladocerans or ctenophores, intermittent feeding may not have a metabolic advantage for any zooplankton (Kremer & Kremer, 1988). Thus, there is little evidence to support the idea of a metabolic advantage in migrating zooplankton. Even if the energy balance is positive in migrators, this must be compensated for by the negative demographic effects caused by lower temperature not considered in Enright's model (Kerfoot, 1985). Enright's hypothesis stressed the relationship between the migrating filter-feeders and their

4 24 resources. Hardy (1936) already interpreted verti- W.Lampert cal migration as a mechanism to prevent overexploitation of the resources. McAllister (1969) proposed the idea that harvesting of the algal crop only at night may result in a higher production compared to continuous harvesting, even if the total daily consumption by zooplankton is identical in both strategies, because all algae can grow unimpeded during the light phase. Mathematical models (McAllister, 1969; Petipa & Makarova, 1969; Lampert, 1987) predicted, in fact, higher algal net production for situations when the total grazing was concentrated at night. An explanation of vertical migration as a strategy to increase algal production, i.e. more food for the zooplankton, would require group selection. There is no doubt that vertical migrations of filter-feeders, especially of the very efficient daphnids, can result in considerable fluctuations of grazing pressure in the epilimnion (Lampert & Taylor, 1985). The effect of rhythmic harvesting cannot be tested in the field due to the lack of appropriate controls. However, laboratory simulations in chemostats failed to demonstrate the enhancement of algal growth by nocturnal grazing when nutrients were limiting, because the positive effect was compensated for by restricted nutrient regeneration by zooplankton (Lampert et al., 1988). Vertical migration of the grazers has important indirect effects on algal biomass and species composition (Lampert, 1987). But these effects are probably a consequence of the migration and cannot be used to propose a higher fitness of a migrating animal compared to a nonmigrating one. Light-related mortality The second group of hypotheses is based on the assumption that animals should avoid the epilimnion during the day because it is dangerous to stay there in the light. In this case, fitness would be gained by reduced mortality instead of increased fecundity. A striking advantage of this approach is that it can easily explain why the animals must avoid the epilimnion during daytime. Light may have a direct deleterious effect on zooplankton, especially UV near the surface (Siebeck, 1978). However, protection from UVlight damage would not require deep migrations, as UV is absorbed in the uppermost water column. Effects of blue light may be more important as it penetrates much deeper. Pigmented copepods are less sensitive to visible light than unpigmented ones, indicating that visible light may be a source of mortality (Hairston, 1980). However, it is difficult to separate the harmful effects of short-wave radiation from visual predation effects (Byron, 1982). The concept of vertical migration as a predator evasion is the most straightforward of the various hypotheses. Although mentioned earlier, it has been explicitely formulated by Zaret & Suffern (1976). As the pelagial is a relatively homogeneous environment, zooplankton have no shelter to hide from visual predators (mainly fish). Their only refuge is the dark hypolimnion. Since the pioneering work of HrbaEek (1962) and Brooks & Dodson (1965) on the effect of fish predation on zooplankton communities, there is a large body of literature dealing with the mechanisms of detection, capture and selection of zooplankton prey by fish (for review see Zaret, 1980; O'Brien, 1987). The predator-avoidance hypothesis generates several predictions: 1 Zooplankton must ascend in the evening and descend at dawn. This is the 'normal' pattern found in the field. Even reverse migrations can sometimes be logically explained. Ohman et al. (1983), for example, interpreted the reverse migration of the small Pseudocalanus as an escape of the 'normally' migrating large invertebrate predator Calanus,that in turn is affected by fish predation. 2 Vertical migration behaviour should predominate in more conspicuous animals that can be better detected by fish. These are large or pigmented animals and those that are carrying a clutch of eggs. In fact, it is often observed that large species have a stronger tendency to migrate and older stages and gravid females migrate deeper than juveniles (Wright, O'Brien & Vinyard, 1980). 3 The amplitude of migration should vary with abundance and activity of planktivorous fish. The seasonal pattern of migration of D. hyalina in Lake Constance (Stich & Lampert, 1981) can be interpreted as a response to the occurrence of fish fry in the pelagial and to increasing feeding activity of fish in summer. Interannual variations in migration pattern of Calanus in Dabob Bay can be related to year class strength in fish (Frost, 1988). Probably the strongest argument in favour of the predation-avoidance hypothesis has recently been provided by Gliwicz (1986). Comparing the migration pattern of Cyclops abyssorum Sars in various lakes of the Tatra mountains that had been stocked with char, he found a clear relationship between the amplitude of migration and the age of the fish population. The copeods did

5 25 not migrate in fishless lakes, but migrated strongly Die1 vertical in lakes that had contained fish for >1000y. migration Intermediate ranges were observed for younger fish populations. The latter example clearly suggests a genotypic response owing to selective mortality of non-migrating copepods. It is sometimes doubted that fish are abundant enough to have such a strong impact. However, visual predators are extremely effective because they select for the adult egg-bearing females, so they kill many offspring together with one mother. Another criticism is that planktivorous fish do not hunt during the day but during twilight and at night (Bohl, 1980). Although fish can hunt at extremely low light intensities, the probability of being detected is much lower for a zooplankter at night (Iwasa, 1982). If fish stay in the littoral during the day, this may be because it does not pay to take the risk of being seen by a large piscivore at the low daytime zooplankton densities. Trade-offs If vertical migration implies energetic and demographic costs, there must be a trade-off between maximum energy input and maximum protection. Thus, the migration pattern may be a compromise (Vuorinen, 1987), following the principle 'better hungry than dead' (Kremer & Kremer, 1988). Although it has been observed that the presence of food can modify the vertical migration behaviour (Hardy & Gunther, 1936; Bohrer, 1980; George, 1983), so that hunger may control the vertical movements (Huntley & Brooks, 1982), the conceptual framework has been developed only recently. Trade-off theory predicts that in the presence of predation pressure food availability and thermal gradient should determine the pattern of vertical migration, viz: 1 If the costs of staying in deep water are low, as the thermal gradient is not steep and the food availability is high, animals should not migrate but stay in deep waters all day. This pattern has been found in very eutrophic Polish lakes (Pijanowska & Dawidowicz, 4987; Gliwicz & Pijanowska, 1988). 2 A gradually higher ascent should occur with increasingly unfavourable conditions in the depth. In eutrophic lakes, animals can assemble near the oxycline during the day and spread over the water column at night as observed for Daphnia in some Holstein lakes (S. Kruse, unpublished). In deep, mesotrophic lakes, it may be necessary to migrate over longer distances and come closer to the surface in order to obtain enough energy. This can also explain why marine copepods may stop migrating when they come into contact with a deep-water phytoplankton layer. Note that vertical migration is viewed here as an ascent from safe deep waters, while the metabolic advantage hypotheses view it as a descent to favourable places. 3 Under more oligotrophic conditions, food availability in deep waters may be so poor that the energy balance cannot be maintained by feeding at the surface for a restricted period of time. The animals must take the risk of being eaten and must stay near the surface. This has recently been demonstrated experimentally for Daphnia longispina O.F. Miiller in a Norwegian lake (Johnsen & Jacobsen, 1987). Daphnids did not migrate in deep enclosures when the food was depleted but started migrating when the enclosures were enriched with food particles. Conclusions Further studies will probably concentrate on quantifying the interactions of predation pressure and the vertical gradients of food availability and temperature (Gliwicz & Pijanowska, 1988). This may help to explain why the observed patterns of vertical migration are so variable (Bayly, 1986). Mathematical models can set the boundary conditions in the way Gabriel & Thomas (1988) demonstrated that diel vertical migration is an evolutionarily stable strategy. The interesting question at present is whether we will be able to find a unifying theory that explains the different patterns in all taxa. The problem is difficult because the falsification of a hypothesis for one species still leaves the possibility that it applies to others (cf. discussion after Lampert et al., 1988). The only unifying concept we have at the moment is that vertical migration may not evolve without light-dependent mortality (presumably visual predation) in the surface waters. There is no supporting evidence for a metabolic advantage. The proposed models of metabolic and demographic profit may at best partly compensate the deleterious consequences of migration as a predator avoidance. References Bayly, I.A.E. (1986) Aspects of diel vertical migration in zooplankton, and its enigma variations. In Limnology in Australia (ed. P. DeDeckker & W.D. Williams), pp Commonwealth Scientific and Industrial Research Organisation, Melbourne.

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