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Diel Vertical Migration
Diel Vertical Migration L D Meester, Katholieke Universiteit Leuven, Leuven, Belgium ã 2009 Elsevier Inc. All rights reserved.
Introduction Diel vertical migration (DVM) is a conspicuous and widespread behavior in planktonic organisms in both inland waters and marine environments. The first scientific studies on this behavior date from more than 100 years ago, and DVM has been observed in a wide variety of habitats worldwide. DVM has attracted a lot of attention from researchers because of several reasons: (1) it is a spectacular behavior, (2) its causes have remained enigmatic for a long time, and (3) the behavior has important ecological consequences.
DVM in its Various Forms DVM is often associated with zooplankton, and zooplankton ecologists have indeed devoted most attention to the phenomenon. However, it should be mentioned that other organisms too have been shown to perform DVM, such as fish, aquatic insects, and phytoplankton. Figures 1–3 provide illustrations of DVM in zooplankton, chosen because they reveal several key aspects of the behavior and its variation. Figure 1 illustrates the migration pattern of a calanoid copepod in a subtropical lake. It shows the classical pattern of a ‘standard’ migration: the animals reside higher in the water column during the night than during the day. During the day, they stay in deep water layers, whereas at night, they distribute themselves more evenly in the water column, and move towards the surface water layers just after sunset and before dawn. The migration is over a long distance. Indeed, the animals move 30–40 m twice every day, which is >40 103 times their own body length (to human standards, this would translate into a traveling distance of >60 km a day). This illustrates why DVM is considered a spectacular behavior. Figure 1 also shows that the movement from the upper to the bottom water layers and vice versa is associated with dawn and dusk. Finally, the figure also illustrates another very common feature: there is a clear tendency for more individuals to be caught during the night than during the day. This phenomenon is called the ‘daytime deficit,’ and is often observed in studies on zooplankton populations showing extensive DVM patterns. In the study system shown in Figure 1, it was shown that a fraction of the copepod population actually moves into the sediments during the day. In many systems, the daytime deficit is probably caused
by the fact that the zooplankton is either residing so close to the sediments during the day that it cannot be sampled by traditional sampling gear or is even moving into the surface layers of the sediment. This is striking, as the sediment is a harsh environment for a zooplankton individual to reside in during part of the day. In many systems that show a strong oxycline, during the day the zooplankton resides at depths that are characterized by very low oxygen levels. Figure 2 even shows a population of calanoid copepods that resides part of the day in the anaerobic monimolimnion of a meromictic lake. In this coastal lake, there is no oxygen below 5 m depth. Figure 2 also shows the pattern of changes in vertical distribution around sunset, and illustrates that different life stages may differ in their daytime distribution and migration pattern. Indeed, it is clear from this figure that the youngest life stages tend to be distributed similarly to their food during the day, whereas most (sub)adult animals reside in the monimolimnion during the night, and rapidly ascend to the mixolimnion after sunset. Figure 3 illustrates strongly different DVM patterns among two congeneric species in the same habitat. This same study also reported seasonal changes in DVM, with Daphnia hyalina migrating only vertically during the summer season. This pattern has been reported for many deep lakes in temperate regions. Summarizing, DVM involves changes in depth distribution over a diel cycle, can take extreme forms and shows tremendous variation through time as well as among life stages, species, and lakes. All the three examples illustrated by the figures represent the most commonly observed pattern of migration, with the animals residing deeper in the water column during the day than during the night (‘standard migration’). However, it should be mentioned that many natural zooplankton populations exhibit a clear-cut depth distribution that does not change over a diel cycle, and there are also reports on ‘reverse migration,’ where populations reside higher in the water column during the day than during the night. This reverse pattern of DVM is less common, but is nevertheless observed in several, often small-bodied species, such as rotifers. In the face of this overwhelming diversity in DVM patterns among species and populations, it is important to develop a broad perspective that allows structuring the observed variation. DVM can be considered a habitat selection behavior. More specifically, it is a depth selection behavior that consists of several elements that can vary among habitats,
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0 20 40 Figure 1 Diel vertical migration of adult females of the calanoid copepod Pseudodiaptomus hessei in Lake Sibaya (March 1972). The broken line indicates a light intensity isocline (1 lux). X-axis: time of day; Y-axis: depth (m); thickness of bars indicates number of animals (see scale bar). Reproduced from Hart RC (1976) The substrate bin – A new sampling device for studying diel vertical migratory movements on to and off lake sediments. Freshwater Biology 6: 155–159, with permission from Blackwell Publishing.
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Figure 2 Vertical distribution of calanoid copepods in meromictic coastal Lake Nagada (Papua New Guinea); the lake has a brackish mixolimnion and has no oxygen below 4.5 m (cf. accumulation of hydrogen sulfide by anaerobic metabolism). (a) vertical distribution of algae in a mid-lake station, June 4, 1992. Filled circles: diatoms and flagellates; filled squares: cyanobacteria (Oscillatoria); shaded area: bacterial plate. (b) vertical distribution of different ontogenetic stages (small nauplii: N1-3; larger nauplii: N4-6; young copepodites: C1-3; larger copepodites: C4-6) of Acartia tonsa 1 h before sunset (17.00; small empty symbols), at sunset (18.00; larger empty symbols) and 1 h after sunset (19.00; filled symbols) at a mid lake station, May 30, 1992. Reproduced from De Meester L and Vyverman W (1997) Diurnal residence of the larger stages of the calanoid copepod Acartia tonsa in the anoxic monimolimnion of a tropical meromictic lake in New Guinea. Journal of Plankton Research 19: 425–434, with permission from Oxford University Press.
species, and populations: the depth at which the animals reside during the day, the depth at which they reside during the night, and the timing and speed of the migration from one depth to the other. This view has proved productive in structuring the observed variation in DVM patterns. For instance, it allows the viewing of the many observations of strong but constant depth preference during day and night as a DVM phenotype that may be selected for if the optimal depth is the same during the day and night, e.g., because it is only determined by the distribution of food. The ubiquity of standard migration would then reflect the fact that under a wide variety of circumstances it is adaptive to stay deeper in the water column during the day than during the night. It is revealing that DVM, viewed as a habitat selection behavior, is essentially very similar to twilight activity as reported for many small mammals, or the migration of aquatic macroinvertebrates in rivers to the underside of stones during the day. Viewed as a
habitat selection behavior, DVM can also be seen as an alternative to diel horizontal migration (DHM). DHM has been observed in many zooplankton species in shallow lakes with a well-developed littoral zone. In a typical DHM migration, the zooplankton resides between the macrophyte vegetation in the littoral zone during the day, and moves into the open water during the night. DHM shows many parallels to DVM: it shows similar diel dynamics, with the main movements being associated with dawn and dusk, and in both cases, the zooplankton moves to rather marginal habitats during the day.
Causes of DVM What causes zooplankton to migrate vertically in a diel cycle? It is important to make a distinction between the proximate and ultimate factors leading to DVM in nature.
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shown to increase the sensitivity to changes in light intensity, which translates into an increase in DVM amplitude in the presence of fish. A strong temperature gradient may reduce the responsiveness to relative changes in light intensity, and the same holds for hunger. The latter results in a less strong DVM behavior in the absence of food.
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Figure 3 Vertical migration patterns of Daphnia galeata (plain) and D. hyalina (shaded) during summer in Lake Constance. The right panel shows depth profiles of temperature (solid line) and particulate carbon (broken line) (particles <35 mm, i.e., potential food for Daphnia). Reproduced from Lampert W and Sommer U (1997) Limnoecology: The Ecology of Lakes and Streams. New York, Oxford University Press; figure based on Stich HB and Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293: 396–398, with permission from Nature Publishing.
Proximate Causes
Proximate causes are the stimuli from the immediate environment of the individual organism that trigger the animal to move downwards or upwards. These stimuli–response processes relate to the physiology of the organism, and translate into a specific day- or nighttime depth as well as into a particular timing and speed of migration. It has been convincingly shown that zooplankton DVM is a response to relative changes in light intensity. Elegant laboratory experiments have revealed that a decrease in light intensity that surpasses a specific threshold elicits an upward movement, whereas an increase in light intensity above a specific threshold elicits a downward movement. These responses have been called ‘secondary phototaxis’ – in contrast to ‘primary phototaxis’ that involves a response to a constant light intensity. Most detailed experiments have been carried out with the water-flea Daphnia, and have shown that changes in light intensity result in eye rotations, which then translate in a change in body orientation and an upward or downward swimming. These simple secondary phototaxis responses may allow predicting the day and night time depth as well as the timing and speed of migration. Moreover, several modifying factors have been identified. For instance, the presence of fish kairomones (which have not been chemically identified yet, but characterized as nonvolatile, lowmolecular-weight, lipophylic compounds of medium polarity and high thermal and pH stability) has been
To the question why the zooplankton engages in DVM, one can also answer with reference to the ultimate factors causing DVM, i.e., its adaptive significance. For a long time, the adaptive significance of DVM has remained enigmatic, as researchers were puzzled by the fact that the zooplankton remained in deep and cold water layers that are characterized by low food concentrations during a large part of the diel cycle. Initially, many authors were convinced that DVM was a side-product of the visual system. Others believed that there were metabolic advantages associated with residing part of the time at a lower temperature. These hypotheses were, however, at odds with model predictions and are unsatisfactory with respect to the synchronized timing of DVM. The currently most widely accepted explanation for DVM in zooplankton is that it acts as a predator-avoidance mechanism. The animals move into the deeper and darker water layers during the day to avoid predation by fish. There are many lines of evidence pointing to the importance of predator-avoidance in DVM, most of them being related to the observation that variation in DVM can often be explained by variation in predator risk: . First, the hypothesis is logical: fish need light to detect their prey efficiently, and by hiding in the darker water layers, the zooplankton can reduce mortality by visually hunting fishes. During the night, the zooplankton moves to the upper water layers to feed on algae that remain in the epilimnion because they need sufficient light for photosynthesis. Thus, the hypothesis can explain both the daytime and nighttime depth distribution, as well as the timing of the upward and downward migration. . Overall, there is a tendency for larger zooplankton species to migrate more or with more amplitude than smaller species. For instance, large Daphnia species migrate to deeper water layers than smaller crustacean zooplankton, whereas rotifers often do not migrate at all. . Smaller life stages often migrate with less amplitude or do not migrate at all (e.g., Figure 2). . Individuals that are more conspicuous, such as eggbearing females, often migrate with more amplitude.
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Figure 4 Impact of fish on DVM: field data from Tuesday and Paul Lake, two kettle lakes at the University of Notre Dame Environmental Research Center. Shown are night (solid symbols) and day (empty symbols) average depth of the Daphnia assemblage in the two lakes as determined from vertical profiles taken during several sampling campaigns across four summers. In 1985 and 1986, Tuesday lake was biomanipulated, resulting in a strong reduction in fish predation pressure; in 1987, fish were reintroduced to the lake, resulting in quite high minnow densities. DVM amplitude of the Daphnia assemblage is associated with the presence of planktivores. Paul Lake was not biomanipulated, and harbored planktivorous fish during the whole period. Reproduced from Dini ML and Carpenter SR (1991) The effect of whole-lake fish community manipulations on Daphnia migratory behavior. Limnology & Oceanography 36: 370–377, with permission from American Society of Limnology and Oceanography.
. It has been reported repeatedly that also within a population there is a tendency for a correlation between body size and daytime residence depth within a given lake. . Among-population variation in DVM amplitude can sometimes be related to differences in predation risk by fish (Figure 4). This is illustrated by the absence of migration in many fishless lakes. . Many populations show seasonal variation in DVM amplitude that can be explained by seasonal variation in predation risk by fish (highest in summer when the young-of-the-year are roaming through the pelagial; e.g., Figure 5). . Very direct evidence for the predator-avoidance hypothesis is provided by the many experimental studies that have shown that DVM behavior can be induced by the presence of fish-specific chemicals (kairomones; Figure 6). . Finally, several mathematical models have shown that DVM behavior can indeed be adaptive as a predator-avoidance strategy, i.e., that the benefits outweigh the costs of staying at low food and temperature during part of the diel cycle. The evidence for the predator-avoidance hypothesis is overwhelming. Yet, predator avoidance need not be
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Figure 5 The changes in day (left) and night (right) depth of adult Daphnia hyalina x galeata hybrids in Lake Maarsseveen during the course of the growing season (April 18 – September 14 1989). The dip in the bundle of lines indicates the period of strong DVM. This period corresponds with the massive appearance of juvenile perch in the pelagial of the lake. Reproduced from Ringelberg J, Flik BJG, Lindenaar D, and Royackers K (1991) Diel vertical migration of Daphnia hyalina (sensu latiori) in Lake Maarsseveen: Part 1. Aspects of seasonal and daily timing. Archiv fu¨r Hydrobiologie 121: 129–145, with permission from E. Schweizerbart’sche Verlagsbuchhandlung.
the sole adaptive value of DVM. Indeed, some cases of day depth distribution or DVM cannot be satisfactorily explained by the predator avoidance hypothesis. For instance, zooplankton has been shown to migrate vertically in fishless alpine lakes, and in some studies the amplitude of the migration has been shown to be unrelated to fish predation risk. Recently, evidence has accumulated that an important adaptive value of DVM may lie in the avoidance of damage caused by UV-radiation, or more generally, by high light intensity. Especially in transparent highaltitude lakes, the presence of fish may not be the only or even the main reason for DVM behavior to develop. UV-avoidance can also explain the pattern and timing of typical normal DVM behavior. Moreover, there is an intrinsic interaction between UV- and predator-avoidance, as animals have two mechanisms to avoid photodamage: they may accumulate protective pigments or they may migrate vertically. In the absence of predators, protective pigments may be the more beneficial option, but in the presence of predators, pigmentation bears a high cost of increased risk of predation, and DVM may be the better alternative. It is often observed in alpine lakes that copepods are pigmented whereas cladoceran zooplankton are not and migrate vertically. What drives this difference is insufficiently understood, but it might be related to the fact that most copepods are relatively small and better swimmers than water fleas. Alternatively, it may be that copepods have better capacity to accumulate photoprotective pigments from their food.
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Figure 6 Induction of DVM by fish kairomone in a clonal population of Daphnia galeata x hyalina hybrids in an experiment using the Plankton Towers at the Max Planck Institut for Limnology, Plo¨n. The experiment was started without fish. Then, the upper 3 m of the tank received water that was conditioned by one fish (Leucaspius delineatus, 5 cm body length). After four days of adaptation, the vertical profile was recorded again at night and during the day. Subsequently, the number of fish was doubled, and the same procedure was continued three more times (cf. up to 16 fish). Reproduced from Loose CJ (1993) Daphnia diel vertical migration behavior: Response to vertebrate predator abundance. Archiv fu¨r Hydrobiologie Beihefte Ergebnisse der Limnologie 39: 29–36, with permission from E. Schweizerbart’sche Verlagsbuchhandlung.
A third ultimate reason to exhibit a typical depth distribution or DVM may be avoidance of competition. This has been shown experimentally in rotifers, and is indeed likely in small zooplankton, which may avoid depths at which larger bodied zooplankton accumulate. It should be noted, however, that this mechanism can only operate in a situation where the competitively superior species is restricted to its depth distribution by additional factors. If competitively dominant large bodied water fleas are forced to hide in the deeper water layers by predation risk or UV radiation, then this may open a window for coexistence of smaller species that occupy the upper water layers during the day. During the night, these smaller species may avoid the upper water layers to reduce interference competition with the large bodied species. The result is a reverse migration. A reverse migration may also be associated with the avoidance of invertebrate predation. Indeed, small bodied species are more vulnerable to invertebrate predators, and as these may be forced to hide in deeper waters during the day because of predation risk by fish, the small bodied species may increase their fitness by residing in the upper water layers during the day and then spread over the water column during the night, when the invertebrate predators move up into the open water to search for prey. Costs
Viewing DVM as a habitat selection behavior provides a flexible approach to the overwhelming
variation in DVM patterns, as the observed day and night time depth distribution as well as timing and speed of migration can be considered to be selected because they provide a high benefit to cost ratio. The benefits of DVM are, as mentioned, often related to reduced mortality by predation, but also reduced damage from high light intensities, and in some cases, reduced damage by competition. The costs are largely cast in terms of reduced food intake, reduced food quality, increased competition (when several competing taxa are migrating to the same refuge), and metabolic costs associated with residing at a lower temperature. In addition, there may be costs associated with residing in truly marginal habitats, such as nearanoxic conditions or being buried in sediments. Residing at or near the sediments can also increase the risk of infection by increasing the likelihood of taking up infective parasite spores, as has been shown in the water flea Daphnia. The costs associated with the movement from one depth layer to the other has, however, been shown to be relatively low or even negligible. This is because the animals in general must actively swim to keep their position in the water column anyway, coupled with the observation that the descent is often passive. During the descent, the animals become less active, and they become more active during the ascending phase. In simple wording: if a water flea shows its typical hop–sink–hop–sink swimming behavior to keep its vertical position, descending is accomplished by hop–sink–sink–hop–sink–sink and ascending by hop–hop–hop–sink behavior. One can
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imagine that the energy lost during the ascending phase matches more or less the energy gained during the descending phase.
The previous paragraph pictures a situation in which the most advantageous DVM behavior may strongly differ from lake to lake. The question then arises as to how this is matched with the response to proximate stimuli. How do the physiological responses of the animals lead to the right vertical distribution during the day and night and the right timing and speed of the ascent and descent? There are two possible mechanisms that are not mutually exclusive, and both are supported by experimental evidence. On the one hand, part of the variation in DVM behavior can be accomplished by phenotypic plasticity acting at the physiological responses. It has, for instance, been shown that predator kairomones and hunger influence the sensitivity of zooplankton individuals to relative changes in light intensity, resulting in a modification of DVM behavior. Populations may thus adjust their DVM behavior by showing the appropriate phenotypic plasticity in response to changes in environmental conditions. At the same time, it has been shown that there is ample genetic variation for DVM behavior, both through field studies as well as through laboratory quantitative genetic analyses of the variation in response to a light gradient (Figure 7) and, to a lesser extent, changes in light intensity. Moreover, it has been shown that there is also genetic variation in phenotypic plasticity for DVM, at least in the water flea Daphnia. This sketches a picture of very high flexibility: populations can adjust their DVM behavior by phenotypic plasticity of the individuals as well as by changes in genetic composition with respect to DVM. It has been shown that populations show local genetic adaptation for DVM in relation to predation risk. Moreover, reconstruction of microevolution in DVM behavior on laboratory populations hatched from dormant egg banks that were isolated from a dated sediment core has shown that local populations can genetically track changes in fish predation pressure. Finally, it has also been shown that animals isolated from different depths during the day are often genetically different and that seasonal changes in DVM behavior may also have a genetic component. The picture that emerges is that DVM is an important component of an antipredator strategy in many populations of zooplankton. It should be emphasized that DVM should not be seen in isolation from other antipredator traits. It has, for instance, been shown
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Relative abundance (%) Figure 7 Vertical distribution of three Daphnia hyalina x galeata hybrid clones isolated from the same population (Scho¨hsee, Germany) in the Plankton Towers of the Max Planck Institute for Limnology (Plo¨n), showing genotypic differences in DVM behavior. Top: average vertical distribution of adult females during the day (open symbols) and night (solid symbols) in the absence of fish chemicals or fish; bottom: daytime distribution in the presence of fish chemicals (open symbols) and fish (solid symbols). The dotted line indicates the thermocline. The experiment involved mixed populations of the three clones, and individuals were identified using allozyme markers. Clone 3 has a clearly different vertical distribution from clones 1 and 2. Reproduced from De Meester L, Weider LJ, and Tollrian R (1995) Alternative antipredator defences and genetic polymorphism in a pelagic predator–prey system. Nature 378: 483–485, with permission from Nature Publishing.
that there is often a relationship between size at maturity and day-depth, with larger animals residing in deeper water layers than smaller ones. Different genotypes and species may thus differ in the antipredator strategy they employ. This is nicely illustrated in the differences in migration pattern of D. galeata and D. hyalina in Lake Constance shown in Figure 3. The strategy of D. galeata involves a high predation risk associated with continuous residence at higher temperatures and under good food conditions. This results in high birth and death rates. The strategy of D. hyalina is to reduce mortality rates and bear the cost of having lower birth rates. The fact that both species can co-occur in the lake illustrates that both strategies may have similar fitness. Part of this relationship is also observed at the genotypic level, with larger bodied genotypes showing a stronger
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response to light gradients. Similarly, DVM behavior and pigmentation are both photoprotection strategies, of which the relative importance may be strongly influenced by predation risk. Both pigmentation and DVM have a cost, but the cost of pigmentation is strongly dependent on predator risk.
top–down control, it should be recognized that part of the impact of predators is actually mediated by induced avoidance behavior rather than by direct predation itself.
Inverse Migrations Consequences of DVM DVM has important consequences, as it strongly influences the top–down impact in lake food webs. DVM reduces the direct impact of fish predation on zooplankton. A more subtle consequence of DVM is that populations of large bodied zooplankton may survive longer in the lake, which thus extends the time during which this food resource remains available for the fish to feed on. In this sense, DVM can be expected to strongly buffer predator–prey interactions between fish and zooplankton. With respect to the zooplankton–algae interaction, DVM has been shown to strongly affect the grazing impact of zooplankton on algae. Here again, however, this has two aspects to it. On the one hand, grazing impact would indeed be higher in the absence of fish-induced DVM, because DVM reduces the time during which zooplankton resides in the epilimnion to feed on algae. On the other hand, DVM may allow large bodied zooplankton to survive in lakes that harbor fish. Given that large bodied zooplankton are more efficient phytoplankton grazers than small bodied zooplankton, DVM may thus indirectly promote the grazing impact of zooplankton on algae, as it allows large-bodied zooplankton to graze on phytoplankton during at least part of the day. In lakes in which the zooplankton exhibits a strong DVM, the algae are indeed fed on by large and efficiently grazing zooplankton during the night. The impacts of DVM on population dynamics of zooplankton and algae and on predator–prey interactions are thus very pervasive. A nice illustration of the impact of DVM on population dynamics is given by the observation of a lunar cycle in zooplankton densities in Lake Kariba. The population densities of zooplankton species in this lake have been reported to show cyclic changes associated with increased predation success of fish on zooplankton during moonlit nights at full moon. In the tropics, sunset and moonrise occur quite fast, and at full moon, the zooplankton is trapped in the surficial water layers by the suddenly rising full moon, providing a feast for the fish. An interesting avenue of thought in this context is the impact of predator-induced plasticity in DVM on predator–prey interactions and top–down control in lakes. Indeed, as DVM has strong impacts on
We focused on the DVM behavior of herbivorous zooplankton (mainly cladocerans, copepods, and rotifers). Predatory zooplankton may, however, also strongly engage in DVM. The best examples are the extensive migrations carried out by phantom midge larvae (Chaoborus) in fish-inhabited lakes. Chaoborus species that inhabit fishless habitats do not migrate vertically, but in fish lakes, the animals often migrate to the sediments during the day and appear in the water column at night. This is believed to be a strong structuring force on the zooplankton in lakes. During the day, large-bodied zooplankton, including Chaoborus larvae, hide in the deep water layers as a refuge from fish predation. By doing so, they provide enemy-free space to small-bodied zooplankton. The small-bodied zooplankton may, however, move out of the high food upper water layers during the night, as these layers are then invaded by efficiently grazing large-bodied zooplankton and gape-limited invertebrate predators that hunt for the small-bodied zooplankton. The resulting pattern is a strong standard migration for crustacean zooplankton and Chaoborus and a reverse migration for small zooplankton such as rotifers. There is an interesting parallel in large, motile phytoplankton. Algae often perform a ‘reverse’ DVM, residing deeper in the water column during the night than during the day. There is much less literature on DVM in algae, but here too, it is a profitable approach to consider it a habitat selection behavior. There are two main reasons for DVM in algae. First, it may be a strategy to combine efficient photosynthesis during the day with a reduction of mortality by grazing of zooplankton during the night, by spreading out over the water column. Alternatively, DVM of algae may also be a strategy to increase nutrient uptake. By migrating to deeper and nutrient-rich layers during the night, the phytoplankton may increase nutrient availability for photosynthesis during the day, thus reducing the impact of nutrient depletion in the epilimnion.
DVM in Fish Fish have also been reported to migrate vertically. They may do so for two reasons. First, they may
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follow their prey. Even though it is much less efficient to hunt in deeper water layers, it may still be more profitable to follow your food in suboptimal conditions than remaining in a habitat that is devoid of any food. It has been shown that fish may even venture for short dives into the near-anoxic conditions to hunt for zooplankton that use these inhospitable layers as a refuge. This may actually explain why zooplankton often migrate deeper than the border zone of the refuge. A second reason why fish migrate may be to avoid their own predators. By avoiding the surface waters during the day, they may reduce their mortality from fish-eating birds. Many fish populations have been reported to either change their vertical or horizontal distribution. In the latter case, they hide in the littoral zone during the day and invade the pelagial during the night. Given that studies often show that both fish and zooplankton avoid the surficial layers of the pelagial zone during the day, one may wonder why the zooplankton does not simply reinvade the food-rich upper water layers. There are several explanations for this. First, it should be acknowledged that in zooplankton populations that show a very strong DVM behavior, intensive sampling of the superficial water layers often reveals some individuals residing there at very low densities. Secondly, it is easy to imagine that, if densities in the superficial layers would become higher, the fish would also rapidly start exploring this food source. Given that hunting at high light intensities is so efficient, even short excursions of the fish to these water layers would decimate the zooplankton. So one expects densities of larger bodied zooplankton to be very low in the epilimnion in such lakes, which is the pattern that is observed.
See also: Cladocera; Competition and Predation; Copepoda; Light, Biological Receptors; Phytoplankton Population Dynamics: Concepts and Performance Measurement; Regulators of Biotic Processes in Stream and River Ecosystems; Role of Zooplankton in Aquatic Ecosystems; Rotifera; Ultraviolet Light.
Further Reading Bayly IAE (1986) Aspects of diel vertical migration in zooplankton, and its enigma variations. In: De Deckker P and Willams WD (eds.) Limnology in Australia. Dordrecht: Junk. Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, and Volckaert F (2001) Rapid local adaptation of zooplankton behavior to changes in predation pressure in absence of neutral genetic changes. Proceedings of the National Academy of Sciences USA 98: 6256–6260. De Meester L, Weider LJ, and Tollrian R (1995) Alternative antipredator defences and genetic polymorphism in a pelagic predator–prey system. Nature 378: 483–485. Gliwicz ZM (1986) A lunar cycle in zooplankton. Ecology 67: 882–897. Haney JF (1988) Diel patterns of zooplankton behavior. Bulletin of Marine Sciences 43: 583–603. Lampert W and Sommer U (2007) Limnoecology: The Ecology of Lakes and Streams. 2nd edn. Oxford: Oxford University Press. Ohman MD (1990) The demographic benefits of diel vertical migration by zooplankton. Ecological Monographs 60: 257–281. Ringelberg J (ed.) (1993) Diel Vertical Migration of Zooplankton, Archiv fu¨r Hydrobiologie – Advances in Limnology, vol. 39. Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung. Ringelberg J (1999) The photobehaviour of Daphnia spp. As a model to explain diel vertical migration in zooplankton. Biological Reviews 74: 397–423. Stich HB and Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293: 396–398. Tollrian R and Harvell CD (eds.) (1999) The Ecology and Evolution of Inducible Defenses. Princeton: Princeton University Press.
Introduction Diel vertical migration (DVM) is a conspicuous and widespread behavior in planktonic organisms in both inland waters and marine environments. The first scientific studies on this behavior date from more than 100 years ago, and DVM has been observed in a wide variety of habitats worldwide. DVM has attracted a lot of attention from researchers because of several reasons: (1) it is a spectacular behavior, (2) its causes have remained enigmatic for a long time, and (3) the behavior has important ecological consequences.
DVM in its Various Forms DVM is often associated with zooplankton, and zooplankton ecologists have indeed devoted most attention to the phenomenon. However, it should be mentioned that other organisms too have been shown to perform DVM, such as fish, aquatic insects, and phytoplankton. Figures 1–3 provide illustrations of DVM in zooplankton, chosen because they reveal several key aspects of the behavior and its variation. Figure 1 illustrates the migration pattern of a calanoid copepod in a subtropical lake. It shows the classical pattern of a ‘standard’ migration: the animals reside higher in the water column during the night than during the day. During the day, they stay in deep water layers, whereas at night, they distribute themselves more evenly in the water column, and move towards the surface water layers just after sunset and before dawn. The migration is over a long distance. Indeed, the animals move 30–40 m twice every day, which is >40 103 times their own body length (to human standards, this would translate into a traveling distance of >60 km a day). This illustrates why DVM is considered a spectacular behavior. Figure 1 also shows that the movement from the upper to the bottom water layers and vice versa is associated with dawn and dusk. Finally, the figure also illustrates another very common feature: there is a clear tendency for more individuals to be caught during the night than during the day. This phenomenon is called the ‘daytime deficit,’ and is often observed in studies on zooplankton populations showing extensive DVM patterns. In the study system shown in Figure 1, it was shown that a fraction of the copepod population actually moves into the sediments during the day. In many systems, the daytime deficit is probably caused
by the fact that the zooplankton is either residing so close to the sediments during the day that it cannot be sampled by traditional sampling gear or is even moving into the surface layers of the sediment. This is striking, as the sediment is a harsh environment for a zooplankton individual to reside in during part of the day. In many systems that show a strong oxycline, during the day the zooplankton resides at depths that are characterized by very low oxygen levels. Figure 2 even shows a population of calanoid copepods that resides part of the day in the anaerobic monimolimnion of a meromictic lake. In this coastal lake, there is no oxygen below 5 m depth. Figure 2 also shows the pattern of changes in vertical distribution around sunset, and illustrates that different life stages may differ in their daytime distribution and migration pattern. Indeed, it is clear from this figure that the youngest life stages tend to be distributed similarly to their food during the day, whereas most (sub)adult animals reside in the monimolimnion during the night, and rapidly ascend to the mixolimnion after sunset. Figure 3 illustrates strongly different DVM patterns among two congeneric species in the same habitat. This same study also reported seasonal changes in DVM, with Daphnia hyalina migrating only vertically during the summer season. This pattern has been reported for many deep lakes in temperate regions. Summarizing, DVM involves changes in depth distribution over a diel cycle, can take extreme forms and shows tremendous variation through time as well as among life stages, species, and lakes. All the three examples illustrated by the figures represent the most commonly observed pattern of migration, with the animals residing deeper in the water column during the day than during the night (‘standard migration’). However, it should be mentioned that many natural zooplankton populations exhibit a clear-cut depth distribution that does not change over a diel cycle, and there are also reports on ‘reverse migration,’ where populations reside higher in the water column during the day than during the night. This reverse pattern of DVM is less common, but is nevertheless observed in several, often small-bodied species, such as rotifers. In the face of this overwhelming diversity in DVM patterns among species and populations, it is important to develop a broad perspective that allows structuring the observed variation. DVM can be considered a habitat selection behavior. More specifically, it is a depth selection behavior that consists of several elements that can vary among habitats,
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Figure 2 Vertical distribution of calanoid copepods in meromictic coastal Lake Nagada (Papua New Guinea); the lake has a brackish mixolimnion and has no oxygen below 4.5 m (cf. accumulation of hydrogen sulfide by anaerobic metabolism). (a) vertical distribution of algae in a mid-lake station, June 4, 1992. Filled circles: diatoms and flagellates; filled squares: cyanobacteria (Oscillatoria); shaded area: bacterial plate. (b) vertical distribution of different ontogenetic stages (small nauplii: N1-3; larger nauplii: N4-6; young copepodites: C1-3; larger copepodites: C4-6) of Acartia tonsa 1 h before sunset (17.00; small empty symbols), at sunset (18.00; larger empty symbols) and 1 h after sunset (19.00; filled symbols) at a mid lake station, May 30, 1992. Reproduced from De Meester L and Vyverman W (1997) Diurnal residence of the larger stages of the calanoid copepod Acartia tonsa in the anoxic monimolimnion of a tropical meromictic lake in New Guinea. Journal of Plankton Research 19: 425–434, with permission from Oxford University Press.
species, and populations: the depth at which the animals reside during the day, the depth at which they reside during the night, and the timing and speed of the migration from one depth to the other. This view has proved productive in structuring the observed variation in DVM patterns. For instance, it allows the viewing of the many observations of strong but constant depth preference during day and night as a DVM phenotype that may be selected for if the optimal depth is the same during the day and night, e.g., because it is only determined by the distribution of food. The ubiquity of standard migration would then reflect the fact that under a wide variety of circumstances it is adaptive to stay deeper in the water column during the day than during the night. It is revealing that DVM, viewed as a habitat selection behavior, is essentially very similar to twilight activity as reported for many small mammals, or the migration of aquatic macroinvertebrates in rivers to the underside of stones during the day. Viewed as a
habitat selection behavior, DVM can also be seen as an alternative to diel horizontal migration (DHM). DHM has been observed in many zooplankton species in shallow lakes with a well-developed littoral zone. In a typical DHM migration, the zooplankton resides between the macrophyte vegetation in the littoral zone during the day, and moves into the open water during the night. DHM shows many parallels to DVM: it shows similar diel dynamics, with the main movements being associated with dawn and dusk, and in both cases, the zooplankton moves to rather marginal habitats during the day.
Causes of DVM What causes zooplankton to migrate vertically in a diel cycle? It is important to make a distinction between the proximate and ultimate factors leading to DVM in nature.
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shown to increase the sensitivity to changes in light intensity, which translates into an increase in DVM amplitude in the presence of fish. A strong temperature gradient may reduce the responsiveness to relative changes in light intensity, and the same holds for hunger. The latter results in a less strong DVM behavior in the absence of food.
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Figure 3 Vertical migration patterns of Daphnia galeata (plain) and D. hyalina (shaded) during summer in Lake Constance. The right panel shows depth profiles of temperature (solid line) and particulate carbon (broken line) (particles <35 mm, i.e., potential food for Daphnia). Reproduced from Lampert W and Sommer U (1997) Limnoecology: The Ecology of Lakes and Streams. New York, Oxford University Press; figure based on Stich HB and Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293: 396–398, with permission from Nature Publishing.
Proximate Causes
Proximate causes are the stimuli from the immediate environment of the individual organism that trigger the animal to move downwards or upwards. These stimuli–response processes relate to the physiology of the organism, and translate into a specific day- or nighttime depth as well as into a particular timing and speed of migration. It has been convincingly shown that zooplankton DVM is a response to relative changes in light intensity. Elegant laboratory experiments have revealed that a decrease in light intensity that surpasses a specific threshold elicits an upward movement, whereas an increase in light intensity above a specific threshold elicits a downward movement. These responses have been called ‘secondary phototaxis’ – in contrast to ‘primary phototaxis’ that involves a response to a constant light intensity. Most detailed experiments have been carried out with the water-flea Daphnia, and have shown that changes in light intensity result in eye rotations, which then translate in a change in body orientation and an upward or downward swimming. These simple secondary phototaxis responses may allow predicting the day and night time depth as well as the timing and speed of migration. Moreover, several modifying factors have been identified. For instance, the presence of fish kairomones (which have not been chemically identified yet, but characterized as nonvolatile, lowmolecular-weight, lipophylic compounds of medium polarity and high thermal and pH stability) has been
To the question why the zooplankton engages in DVM, one can also answer with reference to the ultimate factors causing DVM, i.e., its adaptive significance. For a long time, the adaptive significance of DVM has remained enigmatic, as researchers were puzzled by the fact that the zooplankton remained in deep and cold water layers that are characterized by low food concentrations during a large part of the diel cycle. Initially, many authors were convinced that DVM was a side-product of the visual system. Others believed that there were metabolic advantages associated with residing part of the time at a lower temperature. These hypotheses were, however, at odds with model predictions and are unsatisfactory with respect to the synchronized timing of DVM. The currently most widely accepted explanation for DVM in zooplankton is that it acts as a predator-avoidance mechanism. The animals move into the deeper and darker water layers during the day to avoid predation by fish. There are many lines of evidence pointing to the importance of predator-avoidance in DVM, most of them being related to the observation that variation in DVM can often be explained by variation in predator risk: . First, the hypothesis is logical: fish need light to detect their prey efficiently, and by hiding in the darker water layers, the zooplankton can reduce mortality by visually hunting fishes. During the night, the zooplankton moves to the upper water layers to feed on algae that remain in the epilimnion because they need sufficient light for photosynthesis. Thus, the hypothesis can explain both the daytime and nighttime depth distribution, as well as the timing of the upward and downward migration. . Overall, there is a tendency for larger zooplankton species to migrate more or with more amplitude than smaller species. For instance, large Daphnia species migrate to deeper water layers than smaller crustacean zooplankton, whereas rotifers often do not migrate at all. . Smaller life stages often migrate with less amplitude or do not migrate at all (e.g., Figure 2). . Individuals that are more conspicuous, such as eggbearing females, often migrate with more amplitude.
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Figure 4 Impact of fish on DVM: field data from Tuesday and Paul Lake, two kettle lakes at the University of Notre Dame Environmental Research Center. Shown are night (solid symbols) and day (empty symbols) average depth of the Daphnia assemblage in the two lakes as determined from vertical profiles taken during several sampling campaigns across four summers. In 1985 and 1986, Tuesday lake was biomanipulated, resulting in a strong reduction in fish predation pressure; in 1987, fish were reintroduced to the lake, resulting in quite high minnow densities. DVM amplitude of the Daphnia assemblage is associated with the presence of planktivores. Paul Lake was not biomanipulated, and harbored planktivorous fish during the whole period. Reproduced from Dini ML and Carpenter SR (1991) The effect of whole-lake fish community manipulations on Daphnia migratory behavior. Limnology & Oceanography 36: 370–377, with permission from American Society of Limnology and Oceanography.
. It has been reported repeatedly that also within a population there is a tendency for a correlation between body size and daytime residence depth within a given lake. . Among-population variation in DVM amplitude can sometimes be related to differences in predation risk by fish (Figure 4). This is illustrated by the absence of migration in many fishless lakes. . Many populations show seasonal variation in DVM amplitude that can be explained by seasonal variation in predation risk by fish (highest in summer when the young-of-the-year are roaming through the pelagial; e.g., Figure 5). . Very direct evidence for the predator-avoidance hypothesis is provided by the many experimental studies that have shown that DVM behavior can be induced by the presence of fish-specific chemicals (kairomones; Figure 6). . Finally, several mathematical models have shown that DVM behavior can indeed be adaptive as a predator-avoidance strategy, i.e., that the benefits outweigh the costs of staying at low food and temperature during part of the diel cycle. The evidence for the predator-avoidance hypothesis is overwhelming. Yet, predator avoidance need not be
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Figure 5 The changes in day (left) and night (right) depth of adult Daphnia hyalina x galeata hybrids in Lake Maarsseveen during the course of the growing season (April 18 – September 14 1989). The dip in the bundle of lines indicates the period of strong DVM. This period corresponds with the massive appearance of juvenile perch in the pelagial of the lake. Reproduced from Ringelberg J, Flik BJG, Lindenaar D, and Royackers K (1991) Diel vertical migration of Daphnia hyalina (sensu latiori) in Lake Maarsseveen: Part 1. Aspects of seasonal and daily timing. Archiv fu¨r Hydrobiologie 121: 129–145, with permission from E. Schweizerbart’sche Verlagsbuchhandlung.
the sole adaptive value of DVM. Indeed, some cases of day depth distribution or DVM cannot be satisfactorily explained by the predator avoidance hypothesis. For instance, zooplankton has been shown to migrate vertically in fishless alpine lakes, and in some studies the amplitude of the migration has been shown to be unrelated to fish predation risk. Recently, evidence has accumulated that an important adaptive value of DVM may lie in the avoidance of damage caused by UV-radiation, or more generally, by high light intensity. Especially in transparent highaltitude lakes, the presence of fish may not be the only or even the main reason for DVM behavior to develop. UV-avoidance can also explain the pattern and timing of typical normal DVM behavior. Moreover, there is an intrinsic interaction between UV- and predator-avoidance, as animals have two mechanisms to avoid photodamage: they may accumulate protective pigments or they may migrate vertically. In the absence of predators, protective pigments may be the more beneficial option, but in the presence of predators, pigmentation bears a high cost of increased risk of predation, and DVM may be the better alternative. It is often observed in alpine lakes that copepods are pigmented whereas cladoceran zooplankton are not and migrate vertically. What drives this difference is insufficiently understood, but it might be related to the fact that most copepods are relatively small and better swimmers than water fleas. Alternatively, it may be that copepods have better capacity to accumulate photoprotective pigments from their food.
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Figure 6 Induction of DVM by fish kairomone in a clonal population of Daphnia galeata x hyalina hybrids in an experiment using the Plankton Towers at the Max Planck Institut for Limnology, Plo¨n. The experiment was started without fish. Then, the upper 3 m of the tank received water that was conditioned by one fish (Leucaspius delineatus, 5 cm body length). After four days of adaptation, the vertical profile was recorded again at night and during the day. Subsequently, the number of fish was doubled, and the same procedure was continued three more times (cf. up to 16 fish). Reproduced from Loose CJ (1993) Daphnia diel vertical migration behavior: Response to vertebrate predator abundance. Archiv fu¨r Hydrobiologie Beihefte Ergebnisse der Limnologie 39: 29–36, with permission from E. Schweizerbart’sche Verlagsbuchhandlung.
A third ultimate reason to exhibit a typical depth distribution or DVM may be avoidance of competition. This has been shown experimentally in rotifers, and is indeed likely in small zooplankton, which may avoid depths at which larger bodied zooplankton accumulate. It should be noted, however, that this mechanism can only operate in a situation where the competitively superior species is restricted to its depth distribution by additional factors. If competitively dominant large bodied water fleas are forced to hide in the deeper water layers by predation risk or UV radiation, then this may open a window for coexistence of smaller species that occupy the upper water layers during the day. During the night, these smaller species may avoid the upper water layers to reduce interference competition with the large bodied species. The result is a reverse migration. A reverse migration may also be associated with the avoidance of invertebrate predation. Indeed, small bodied species are more vulnerable to invertebrate predators, and as these may be forced to hide in deeper waters during the day because of predation risk by fish, the small bodied species may increase their fitness by residing in the upper water layers during the day and then spread over the water column during the night, when the invertebrate predators move up into the open water to search for prey. Costs
Viewing DVM as a habitat selection behavior provides a flexible approach to the overwhelming
variation in DVM patterns, as the observed day and night time depth distribution as well as timing and speed of migration can be considered to be selected because they provide a high benefit to cost ratio. The benefits of DVM are, as mentioned, often related to reduced mortality by predation, but also reduced damage from high light intensities, and in some cases, reduced damage by competition. The costs are largely cast in terms of reduced food intake, reduced food quality, increased competition (when several competing taxa are migrating to the same refuge), and metabolic costs associated with residing at a lower temperature. In addition, there may be costs associated with residing in truly marginal habitats, such as nearanoxic conditions or being buried in sediments. Residing at or near the sediments can also increase the risk of infection by increasing the likelihood of taking up infective parasite spores, as has been shown in the water flea Daphnia. The costs associated with the movement from one depth layer to the other has, however, been shown to be relatively low or even negligible. This is because the animals in general must actively swim to keep their position in the water column anyway, coupled with the observation that the descent is often passive. During the descent, the animals become less active, and they become more active during the ascending phase. In simple wording: if a water flea shows its typical hop–sink–hop–sink swimming behavior to keep its vertical position, descending is accomplished by hop–sink–sink–hop–sink–sink and ascending by hop–hop–hop–sink behavior. One can
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imagine that the energy lost during the ascending phase matches more or less the energy gained during the descending phase.
The previous paragraph pictures a situation in which the most advantageous DVM behavior may strongly differ from lake to lake. The question then arises as to how this is matched with the response to proximate stimuli. How do the physiological responses of the animals lead to the right vertical distribution during the day and night and the right timing and speed of the ascent and descent? There are two possible mechanisms that are not mutually exclusive, and both are supported by experimental evidence. On the one hand, part of the variation in DVM behavior can be accomplished by phenotypic plasticity acting at the physiological responses. It has, for instance, been shown that predator kairomones and hunger influence the sensitivity of zooplankton individuals to relative changes in light intensity, resulting in a modification of DVM behavior. Populations may thus adjust their DVM behavior by showing the appropriate phenotypic plasticity in response to changes in environmental conditions. At the same time, it has been shown that there is ample genetic variation for DVM behavior, both through field studies as well as through laboratory quantitative genetic analyses of the variation in response to a light gradient (Figure 7) and, to a lesser extent, changes in light intensity. Moreover, it has been shown that there is also genetic variation in phenotypic plasticity for DVM, at least in the water flea Daphnia. This sketches a picture of very high flexibility: populations can adjust their DVM behavior by phenotypic plasticity of the individuals as well as by changes in genetic composition with respect to DVM. It has been shown that populations show local genetic adaptation for DVM in relation to predation risk. Moreover, reconstruction of microevolution in DVM behavior on laboratory populations hatched from dormant egg banks that were isolated from a dated sediment core has shown that local populations can genetically track changes in fish predation pressure. Finally, it has also been shown that animals isolated from different depths during the day are often genetically different and that seasonal changes in DVM behavior may also have a genetic component. The picture that emerges is that DVM is an important component of an antipredator strategy in many populations of zooplankton. It should be emphasized that DVM should not be seen in isolation from other antipredator traits. It has, for instance, been shown
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Relative abundance (%) Figure 7 Vertical distribution of three Daphnia hyalina x galeata hybrid clones isolated from the same population (Scho¨hsee, Germany) in the Plankton Towers of the Max Planck Institute for Limnology (Plo¨n), showing genotypic differences in DVM behavior. Top: average vertical distribution of adult females during the day (open symbols) and night (solid symbols) in the absence of fish chemicals or fish; bottom: daytime distribution in the presence of fish chemicals (open symbols) and fish (solid symbols). The dotted line indicates the thermocline. The experiment involved mixed populations of the three clones, and individuals were identified using allozyme markers. Clone 3 has a clearly different vertical distribution from clones 1 and 2. Reproduced from De Meester L, Weider LJ, and Tollrian R (1995) Alternative antipredator defences and genetic polymorphism in a pelagic predator–prey system. Nature 378: 483–485, with permission from Nature Publishing.
that there is often a relationship between size at maturity and day-depth, with larger animals residing in deeper water layers than smaller ones. Different genotypes and species may thus differ in the antipredator strategy they employ. This is nicely illustrated in the differences in migration pattern of D. galeata and D. hyalina in Lake Constance shown in Figure 3. The strategy of D. galeata involves a high predation risk associated with continuous residence at higher temperatures and under good food conditions. This results in high birth and death rates. The strategy of D. hyalina is to reduce mortality rates and bear the cost of having lower birth rates. The fact that both species can co-occur in the lake illustrates that both strategies may have similar fitness. Part of this relationship is also observed at the genotypic level, with larger bodied genotypes showing a stronger
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response to light gradients. Similarly, DVM behavior and pigmentation are both photoprotection strategies, of which the relative importance may be strongly influenced by predation risk. Both pigmentation and DVM have a cost, but the cost of pigmentation is strongly dependent on predator risk.
top–down control, it should be recognized that part of the impact of predators is actually mediated by induced avoidance behavior rather than by direct predation itself.
Inverse Migrations Consequences of DVM DVM has important consequences, as it strongly influences the top–down impact in lake food webs. DVM reduces the direct impact of fish predation on zooplankton. A more subtle consequence of DVM is that populations of large bodied zooplankton may survive longer in the lake, which thus extends the time during which this food resource remains available for the fish to feed on. In this sense, DVM can be expected to strongly buffer predator–prey interactions between fish and zooplankton. With respect to the zooplankton–algae interaction, DVM has been shown to strongly affect the grazing impact of zooplankton on algae. Here again, however, this has two aspects to it. On the one hand, grazing impact would indeed be higher in the absence of fish-induced DVM, because DVM reduces the time during which zooplankton resides in the epilimnion to feed on algae. On the other hand, DVM may allow large bodied zooplankton to survive in lakes that harbor fish. Given that large bodied zooplankton are more efficient phytoplankton grazers than small bodied zooplankton, DVM may thus indirectly promote the grazing impact of zooplankton on algae, as it allows large-bodied zooplankton to graze on phytoplankton during at least part of the day. In lakes in which the zooplankton exhibits a strong DVM, the algae are indeed fed on by large and efficiently grazing zooplankton during the night. The impacts of DVM on population dynamics of zooplankton and algae and on predator–prey interactions are thus very pervasive. A nice illustration of the impact of DVM on population dynamics is given by the observation of a lunar cycle in zooplankton densities in Lake Kariba. The population densities of zooplankton species in this lake have been reported to show cyclic changes associated with increased predation success of fish on zooplankton during moonlit nights at full moon. In the tropics, sunset and moonrise occur quite fast, and at full moon, the zooplankton is trapped in the surficial water layers by the suddenly rising full moon, providing a feast for the fish. An interesting avenue of thought in this context is the impact of predator-induced plasticity in DVM on predator–prey interactions and top–down control in lakes. Indeed, as DVM has strong impacts on
We focused on the DVM behavior of herbivorous zooplankton (mainly cladocerans, copepods, and rotifers). Predatory zooplankton may, however, also strongly engage in DVM. The best examples are the extensive migrations carried out by phantom midge larvae (Chaoborus) in fish-inhabited lakes. Chaoborus species that inhabit fishless habitats do not migrate vertically, but in fish lakes, the animals often migrate to the sediments during the day and appear in the water column at night. This is believed to be a strong structuring force on the zooplankton in lakes. During the day, large-bodied zooplankton, including Chaoborus larvae, hide in the deep water layers as a refuge from fish predation. By doing so, they provide enemy-free space to small-bodied zooplankton. The small-bodied zooplankton may, however, move out of the high food upper water layers during the night, as these layers are then invaded by efficiently grazing large-bodied zooplankton and gape-limited invertebrate predators that hunt for the small-bodied zooplankton. The resulting pattern is a strong standard migration for crustacean zooplankton and Chaoborus and a reverse migration for small zooplankton such as rotifers. There is an interesting parallel in large, motile phytoplankton. Algae often perform a ‘reverse’ DVM, residing deeper in the water column during the night than during the day. There is much less literature on DVM in algae, but here too, it is a profitable approach to consider it a habitat selection behavior. There are two main reasons for DVM in algae. First, it may be a strategy to combine efficient photosynthesis during the day with a reduction of mortality by grazing of zooplankton during the night, by spreading out over the water column. Alternatively, DVM of algae may also be a strategy to increase nutrient uptake. By migrating to deeper and nutrient-rich layers during the night, the phytoplankton may increase nutrient availability for photosynthesis during the day, thus reducing the impact of nutrient depletion in the epilimnion.
DVM in Fish Fish have also been reported to migrate vertically. They may do so for two reasons. First, they may
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follow their prey. Even though it is much less efficient to hunt in deeper water layers, it may still be more profitable to follow your food in suboptimal conditions than remaining in a habitat that is devoid of any food. It has been shown that fish may even venture for short dives into the near-anoxic conditions to hunt for zooplankton that use these inhospitable layers as a refuge. This may actually explain why zooplankton often migrate deeper than the border zone of the refuge. A second reason why fish migrate may be to avoid their own predators. By avoiding the surface waters during the day, they may reduce their mortality from fish-eating birds. Many fish populations have been reported to either change their vertical or horizontal distribution. In the latter case, they hide in the littoral zone during the day and invade the pelagial during the night. Given that studies often show that both fish and zooplankton avoid the surficial layers of the pelagial zone during the day, one may wonder why the zooplankton does not simply reinvade the food-rich upper water layers. There are several explanations for this. First, it should be acknowledged that in zooplankton populations that show a very strong DVM behavior, intensive sampling of the superficial water layers often reveals some individuals residing there at very low densities. Secondly, it is easy to imagine that, if densities in the superficial layers would become higher, the fish would also rapidly start exploring this food source. Given that hunting at high light intensities is so efficient, even short excursions of the fish to these water layers would decimate the zooplankton. So one expects densities of larger bodied zooplankton to be very low in the epilimnion in such lakes, which is the pattern that is observed.
See also: Cladocera; Competition and Predation; Copepoda; Light, Biological Receptors; Phytoplankton Population Dynamics: Concepts and Performance Measurement; Regulators of Biotic Processes in Stream and River Ecosystems; Role of Zooplankton in Aquatic Ecosystems; Rotifera; Ultraviolet Light.
Further Reading Bayly IAE (1986) Aspects of diel vertical migration in zooplankton, and its enigma variations. In: De Deckker P and Willams WD (eds.) Limnology in Australia. Dordrecht: Junk. Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, and Volckaert F (2001) Rapid local adaptation of zooplankton behavior to changes in predation pressure in absence of neutral genetic changes. Proceedings of the National Academy of Sciences USA 98: 6256–6260. De Meester L, Weider LJ, and Tollrian R (1995) Alternative antipredator defences and genetic polymorphism in a pelagic predator–prey system. Nature 378: 483–485. Gliwicz ZM (1986) A lunar cycle in zooplankton. Ecology 67: 882–897. Haney JF (1988) Diel patterns of zooplankton behavior. Bulletin of Marine Sciences 43: 583–603. Lampert W and Sommer U (2007) Limnoecology: The Ecology of Lakes and Streams. 2nd edn. Oxford: Oxford University Press. Ohman MD (1990) The demographic benefits of diel vertical migration by zooplankton. Ecological Monographs 60: 257–281. Ringelberg J (ed.) (1993) Diel Vertical Migration of Zooplankton, Archiv fu¨r Hydrobiologie – Advances in Limnology, vol. 39. Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung. Ringelberg J (1999) The photobehaviour of Daphnia spp. As a model to explain diel vertical migration in zooplankton. Biological Reviews 74: 397–423. Stich HB and Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293: 396–398. Tollrian R and Harvell CD (eds.) (1999) The Ecology and Evolution of Inducible Defenses. Princeton: Princeton University Press.