Download The Adaptive Significance of Diel Vertical Migration of Zooplankton

Functional
Ecology 1989,
3, 21-27
ESSAY REVIEW
The adaptive significanceof diel vertical
migrationof zooplankton
downwards. The movement of the population
reflectsonly the net effect.The distance between
times
the mean depths of a population at different
equals the distance travelledby an individual only
if all animals migratesynchronously.Otherwise,
the movement of an individual can be considerably underestimated.As it is not possible to track
adapZooplankton,diel verticalmigration,
Key-words:
trade- small individual zoo'lankton in situ,this problem
visualpredation,
tivevalue,metabolicadvantage,
consequences,photo-protection
offs,demographic
is still not solved.
In the sixties,the main concern of investigators
of vertical migrationwas the neurophysiological
The phenomenon
basis of the rhythmic behaviour. Behavioural
Many taxa of both marine and freshwaterzoophysiology tried to identifythe stimuli for initiplankton perform diel vertical migrations with
ation and direction of the migration.The relative
amplitudes froma fewto 100 metres(Hutchinson,
change of lightintensityhas been found to be the
1967). The 'normal' patternis an evening ascent
proximate cue that controls the upwards and
and a morning descent, though several cases of
downwards movements.At least in Daphnia, the
'reversed' migrations have been described
reactiondepends on the level oflightadaptation of
(Ohman, Frost & Cohen, 1983; Bayly, 1986).
the animal's eye (Siebeck, 1960; Ringelberg,1964;
Migratinganimals spend the day in deep waters
McNaught & Hasler, 1964; Ringelberg,Van Kasteel
but staynear the surfaceat night.The amplitude of
& Servaas, 1967). Today the focus ofmostresearch
the movements and the shape of the vertical
on verticalmigrationhas shiftedfromthe environdistributionof the population may be very differ- mental control towards the search for ultimate
ent between species and between ontogenetic reasons.
stages of the same species and may be influenced
by factors like turbitiy and food abundance
(Bohrer, 1980; George, 1983). Zooplankton may
The problem
eithermigrateup and down togetherin a narrow
The presence ofverticalmigrationin so manytaxa
band or may be sharply stratifiedin deep waters
suggeststhatithas some adaptive value. Although
during the day but spread throughoutthe entire
thereis no reason to believe thatthe same ultimate
water column at night.
factordrives migrationin all taxa, it is interesting
However, what we observe are only changes in
that all migrating filter-feedingzooplankton
the population density at differentdepths of the
experience similar disadvantageous environwater column. When taking plankton samples
mental conditions. This effectis principallysimifromdifferentwater layers, we obtain a vertical
lar in freshwaterand in the sea but may be more
profile of animal abundances. Shifts in these
pronounced in stratifiedlakes. Migratinganimals
vertical distributionsare usually interpretedas
movementsofthe population and day-nightdiffer- spend the nightin warm food-richsurfacewaters
ences between means or medians of the distri- but they leave this advantageous environment
during the day to stay in the cold hypolimnion
butions serve as measures of the verticalrange of
where quantityand quality offood are low. Thus,
migration.However, such population responses
several costs are associated with migration.
may be seriously misleading in terms of the
Reduced food availabilityresultsin slower growth
behaviour of constituent individuals (Pearre,
and lower fecundity.The developmental time of
1979a). Individuals may vary speed and direction
the eggs carried by females is prolonged at the
of their movements, so that at any time some
lower temperatures.Moreover,swimmingup and
animals move upwards while othersrest or move
W. LAMPERT
Departmentof Physiological Ecology,Max
Planck InstituteofLimnology,Postfach 165,
2330 Plin, Federal Republic of Germany
21
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
22
W. Lampert
down the watercolumn needs energy.These costs
mustresultin reduced fitnessofmigratinganimals
compared to those that stay in the surfacewaters
all day long.
However, since theymigrate,it is reasonable to
suppose that there must be a selective force that
favoursmigrationbehaviour. This apparent paradox has puzzled plankton ecologists for several
years. A large variety of competing hypotheses
have been offeredto explain the adaptive value of
vertical migration.The majorityof them can be
grouped in two categoriesaccording to the different components of fitnesstheyemphasize:
(1) Vertical migrationprovides a metabolic or
demographicadvantage.
(2) Avoidance of surfacewaters duringthe day
reduces the light-dependentmortalityrisk.
A thirdgroup is not directlyrelated to individual
fitness,but proposes optimum exploitation strategies offood resources.
Adaptive value
Metabolic and demographic advantage
The idea that migratingzooplankton may have a
ones was
metabolic advantage over non-migrating
proposed by McLaren (1963). He estimated an
energeticbonus forcopepods feeding at nightin
the warm,food-richwaters and restingin the cold
during the day. However, besides the energetic
bonus, thereis a retardationofdevelopmentat low
temperatures. So McLaren (1974) modified the
original hypothesis by constructing a possible
demographic advantage. Copepods growing at
lower temperaturesmay reach largeradult body
size. Provided there are non-limitingfood conditions and fecundityof large specimens is higher
than that of smaller ones, this may result in a
demographicadvantage. McLaren himselfpointed
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 thatcopepods
raised under fluctuatingtemperatureconditions
did not grow to larger sizes than those kept at a
constant average temperature. Kerfoot (1985)
criticized the demographic advantage hypothesis
rigorouslyby clearly pointing out that increased
fecundity cannot compensate for the negative
effectof decreased temperature on the rate of
population growth(r).
All attemptsto test McLaren's hypothesishave
failed to demonstratea reproductiveadvantage of
migrating zooplankton. Larvae of Chooborus
Loew gained no energeticbenefitunder
trivittatus
simulated verticalmigrationconditions in laboratory experiments of Swift (1976). More information is available forvarious Daphnia species.
Good luck provided Stich & Lampert(1981) with a
fieldtest.They foundtwo Daphnia species in Lake
Constance that,albeit being morphologicallyvery
similar, showed pronounced differencesin their
migrationbehaviour. Daphnia galeata Sars and
Daphnia hyalina Leydig are so closely relatedthat
theyeven formhybrids(Wolf& Mort,1986), but D.
hyalina performsdiel migrationsof more than 40
metersamplitude, while D. galeata migratesvery
little and stays in the epilimnion all day long. If
diel vertical migrationhas 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
fewereggsthan D. galeata and, moreover,the eggs
develop much more slowly than those of D.
galeata.
Laboratory experiments have confirmedthese
field observations. Orcutt & Porter (1983) and
Manca, DeBernardi & Savia (1986) constructedlife
tables forDaphnia under several fluctuatingand
constanttemperatureconditions. Althoughreproductive patterns differed between treatments,
there was no indication that fluctuating temperaturesincreased r. Daphnids grown under the
highestconstanttemperaturealways had the highest reproductive output. Orcutt & Porter (1983)
clearly point out that'the differencebetween a
migrationand non-migrationstrategyis not fluctuating versus average constant temperaturebut
fluctuatingversus maximum temperaturein the
cycle. The differencesbetween the two strategies
were even morepronounced in the only studythat
varied temperatureand food simultaneouslyin a
diel cycle (Stich & Lampert,1984). Althoughthere
-were slight differencesbetween the two species
that performdifferentmigrationpatternsin Lake
Constance, both of them grew faster and had
considerably higher reproductive output under
non-migrationconditions. These results corroborate the field observations and suggest that, at
least in daphnids, vertical migration is energeticallydisadvantageous.
Energyconservation
However, additional assumptions revivedthe idea
ofa metabolic advantage,Geller (1986) proposed a
'starvationavoidance hypothesis', based on data
on the Lake Constance Daphnia populations.
Though it is difficultto understand how natural
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
23
Diel vertical
migration
selection can favour a seasonally-stable, high
population density in a parthenogeneticspecies,
his basic idea is that migratingdaphnids use a
'conservation' strategyto avoid population fluctuations. During spring,when food is very abundant, both Daphnia
species utilize an
'exploitative' strategyto 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
thatperiods ofstarvationmay occur. Energylosses
during starvationin 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 migrationarises from the need to gain
energythat is not available in the deep water. To
enforcethe energygain, Geller (1986) assumed a
mechanism of temperatureacclimation as found
in marine littoral snails (Somero & Hochachka,
1976). Feeding and respirationof cold acclimated
animals are supposed to respond differentlyto
variations in temperature. If the feeding rate
increases steeply with raising temperaturein the
epilimnion,while the respiratoryrateresponds to
a lesser extent,migratinganimals will achieve a
net gain ofenergyto partlycompensate the starvation losses. However, to date this effecthas not
been demonstratedin any zooplankton.
Resource related hypotheses
Enright(1977) was the firstto incorporate feedbacks between filter-feedingzooplankton and
theiralgal preyinto a metabolic model. His model
differedfromMcLaren's (1963) in two additional
assumptions: (1) Since photosynthesistakes place
duringthe day, but only losses (respiration,grazing) occur at night,algal biomass mustbe greaterin
the evening than in the morning. Algal quality
must also be differentas the cells will be filled
with reservesat dusk. (2) Animals returningto the
surfaceafterseveral hours ofstarvationwill feed at
enhanced rates. They may compensate for the
day-timestarvationby feeding in the evening at
elevated rates on algae of higher abundance and
quality. As respiratorylosses are low during the
starvationperiod in the cold hypolimnion,migrating animals may, thus, gain an energeticprofit.
Contrary to the other metabolic-advantage hypotheses that cannot explain why the animals
migrateat certaintimesofthe day, Enright'smodel
incorporates the timing of migration.It predicts
thatzooplanktonshould not arriveat the surfacein
complete darkness but before dusk. This prediction has been tested by three series of detailed
sampling ofthe marine copepod Calanus (Enright
& Honegger, 1977). The predicted pattern was
foundin only one series,so the authorsconcluded
that other factorswere modifyingthe 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 thathe had predictedan unexpected phenomenon, and that this phenomenon had been
observed later - at least sometimes. Thus his
hypothesiscould not be refuted.However, Pearre
(1979b) raised the question if copepods that
ascend before sunset also feed before sunset A recent
which is basic to Enright'sinterpretation.
study (M.J. Dagg, unpublished), using the gutfluorescence method (Mackas & Bohrer, 1976),
confirmedthe early ascent of Calanus but found
theirguts to be emptybeforesunset.
The Enrightmodel 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 effectoccurs at low
food concentrationsand also lasts forsome hours.
Some laboratory experiments supported both
assumptions (Runge, 1980) or at least one ofthem
(Ringelberg& Royackers, 1985; Mackas & Burns,
1986). Othersdid not findthe enhancementat low
concentrations(McMahon & Rigler, 1965; Frost,
1972; Lampert,Schmitt& Muck, 1988), but a rapid
decline of the hungerresponse 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 betteradapted to changing
food conditions than cladocerans or ctenophores,
intermittentfeeding may not have a metabolic
advantage forany zooplankton (Kremer& Kremer,
1988). Thus, thereis littleevidence to supportthe
idea of a metabolic advantage in migratingzooplankton.Even ifthe energybalance 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-feedersand their
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
24
W. Lampert
resources. Hardy (1936) already interpretedvertical migration as a mechanism to prevent overexploitation of the resources. McAllister (1969)
proposed the idea thatharvestingofthe 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 duringthe lightphase. Mathematical
models (McAllister, 1969; Petipa & Makarova,
1969; Lampert, 1987) predicted, in fact, higher
algal net production forsituationswhen the total
grazingwas concentratedat night.An explanation
ofverticalmigrationas a strategyto increase algal
production, i.e. more food for the zooplankton,
would require group selection. There is no doubt
thatverticalmigrationsoffilter-feeders,
especially
of the very efficientdaphnids, can result in considerable fluctuationsof grazing pressure in the
epilimnion (Lampert& Taylor,1985). The effectof
rhythmicharvestingcannot be tested in the field
due to the lack of appropriate controls.However,
laboratory simulations in chemostats failed to
demonstratethe enhancement of algal growthby
nocturnal grazing when nutrientswere limiting,
because the positive effectwas compensated forby
restrictednutrientregenerationby zooplankton
(Lampert et al., 1988). Vertical migrationof the
grazers has important indirect effectson algal
biomass and species composition (Lampert,1987).
But these effectsare probablya consequence ofthe
migrationand cannot be used to propose a higher
fitnessof a migratinganimal compared to a nonmigratingone.
Light-relatedmortality
The second group of hypotheses is based on the
assumption that animals should avoid the epilimnion duringthe day because it is dangerous to
staytherein the light.In thiscase, fitnesswould be
gained by reduced mortalityinstead of increased
fecundity.A strikingadvantage ofthis approach is
that it can easily explain why the animals must
avoid the epilimnion duringdaytime.
Light may have a direct deleterious effecton
zooplankton, especially UV near the surface
(Siebeck, 1978). However, protection from UVlight damage would not require deep migrations,
as UV is absorbed in the uppermostwatercolumn.
Effectsof blue light may be more importantas it
penetratesmuch deeper. Pigmentedcopepods are
less sensitive to visible light than unpigmented
ones, indicatingthat visible lightmay be a source
of mortality(Hairston, 1980). However, it is difficult to separate the harmfuleffectsof short-wave
radiation from visual predation effects (Byron,
1982).
The concept of vertical migrationas a predator
of the various
evasion is the most straightforward
hypotheses. Although mentioned earlier, it has
been explicitely formulatedby Zaret & Suffern
(1976). As the pelagial is a relativelyhomogeneous
environment,zooplankton have no shelterto hide
from visual predators (mainly fish). Their only
refugeis the darkhypolimnion.Since the pioneering work of Hrbf6ek(1962) and Brooks & Dodson
(1965) on the effectof fish predation on zooplankton communities, there is a large body of
literaturedealing with the mechanisms of detection,capture and selection ofzooplankton preyby
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' patternfound in the field.
Even reverse migrationscan sometimes be logically explained. Ohman et al. (1983), forexample,
interpretedthe reverse migration of the small
Pseudocalanus as an escape of the 'normally'
migratinglargeinvertebratepredatorCalan us, that
in turnis affectedby fishpredation.
2 Vertical migrationbehaviour 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 strongertendency to migrate and older
stages and gravid females migrate deeper than
juveniles (Wright,O'Brien & Vinyard,1980).
3 The amplitude of migrationshould vary with
abundance and activityof planktivorousfish.
The seasonal patternof migrationof D. hyalina
in Lake Constance (Stich & Lampert,1981) can be
interpretedas a response to the occurrence offish
fry in the pelagial and to increasing feeding
activityof fishin summer. Interannualvariations
in migrationpatternof Calanus in Dabob Bay can
be related to year class strengthin fish (Frost,
1988). Probably the strongestargumentin favour
of the predation-avoidance hypothesis has
recentlybeen provided by Gliwicz (1986). Comparingthe migrationpatternofCyclops 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 ofthefishpopulation. The copeods did
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
25
Diel vertical
migration
not migratein fishlesslakes, but migratedstrongly
in lakes that had contained fish for >lOOOy.
Intermediate ranges were observed for younger
fish populations. The latterexample clearly suggests a genotypic response owing to selective
mortalityof non-migratingcopepods.
It is sometimes doubted that fish are abundant
enough to have such a strongimpact. However,
visual predators are extremelyeffectivebecause
they select for the adult egg-bearingfemales, so
theykill many offspring
togetherwith one mother.
Anothercriticismis thatplanktivorousfishdo not
hunt during the day but during twilightand at
night (Bohl, 1980). Although fish can hunt at
extremelylow lightintensities,the probabilityof
being detected is much lower fora zooplankterat
night (Iwasa, 1982). If fish stay in the littoral
duringthe day,this maybe because it does notpay
to take the riskofbeing seen by a largepiscivore at
the low daytimezooplankton densities.
the surfacein orderto obtain enough energy.This
can also explain why marine copepods may stop
migratingwhen they come into contact with a
deep-waterphytoplanktonlayer.Note thatvertical
migrationis viewed here as an ascent fromsafe
deep waters, while the metabolic advantage
hypotheses view it as a descent to favourable
places.
3 Under more oligotrophic conditions, food
availabilityin deep waters may be so poor thatthe
energybalance cannot be maintainedby feedingat
the surface for a restrictedperiod of time. The
animals musttake the riskofbeing eaten and must
stay near the surface. This has recently been
demonstratedexperimentallyforDaphnia longispina O.F. Muller in a Norwegian lake (Johnsen&
Jacobsen,1987). Daphnids did not migratein deep
enclosures when the food was depleted but started
migratingwhen the enclosures were enrichedwith
food particles.
Conclusions
Trade-offs
If vertical migrationimplies energeticand demographic costs, there must be a trade-offbetween
maximumenergyinput and maximumprotection.
Thus, the migrationpatternmay be a compromise
(Vuorinen, 1987), following the principle 'better
hungry than dead' (Kremer & Kremer, 1988).
Althoughit has been observed thatthe presence of
food can modifythe vertical migrationbehaviour
(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-offtheory predicts that in the
presence of predation pressure food availability
and thermalgradientshould determinethe pattern
ofverticalmigration,viz:
1 If the costs of stayingin deep water are low, as
the thermal gradient is not steep and the food
availabilityis high,animals should not migratebut
stay in deep waters all day. This patternhas 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 duringthe day and spread over
the watercolumn at nightas observed forDaphnia
in some Holstein lakes (S. Kruse, unpublished). In
deep, mesotrophic lakes, it may be necessary to
migrateover longer distances and come closer to
Further studies will probably concentrate on
quantifyingthe interactionsof predation pressure
and the verticalgradientsof food availability and
temperature(Gliwicz & Pijanowska, 1988). This
may help to explain why the observed patternsof
vertical migrationare so variable (Bayly, 1986).
Mathematicalmodels 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 whetherwe will be able to
find a unifyingtheorythat explains the different
patterns in all taxa. The problem is difficult
because the falsificationof a hypothesis for one
species stillleaves the possibilitythatit applies to
others (cf. discussion afterLampert et al., 1988).
The only unifyingconcept we have at the moment
is that vertical migrationmay not evolve without
light-dependentmortality(presumablyvisual predation) in the surfacewaters. There is no supporting evidence for a metabolic advantage. The
proposed models of metabolic and demographic
profitmay at best partly compensate the deleterious consequences of migrationas a predator
avoidance.
References
Bayly,I.A.E. (1986) Aspects of diel verticalmigrationin
zooplankton, and its enigma variations.In Limnology
in Australia (ed. P. DeDeckker & W.D. Williams), pp.
349-368. Commonwealth Scientific and Industrial
Research Organisation,Melbourne.
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
26
W. Lampert
Bohl, E. (1980) Diel patternof pelagic distributionand
feedingin planktivorousfish.Oecologia, 44, 368-3 75.
Bohrer,R. (1980) Experimental studies on diel vertical
migration.In Ecology and Evolution of Zooplankton
Communities(ed. W.C. Kerfoot),pp. 111-121. UniversityPress ofNew England, Hanover, New Hampshire.
Brooks, J.L.& Dodson, S.I. (1965) Predation,body size,
and composition ofplankton. Science, 150, 28-35.
Byron,E.R. (1982) The adaptive significanceof calanoid
copepod pigmentation: a comparative and experimental analysis. Ecology, 63, 1871-1886.
Enright,J.T. (1977) Diurnal verticalmigration:adaptive
significanceand timing.Part 1. Selective advantage: a
metabolic model. Limnologyand Oceanography, 22,
856-872.
Enright,J.T.(1979) The why and when ofup and down.
Limnologyand Oceanography,24, 788-791.
Enright,J.T. & Honegger, H.W. (1977) Diurnal vertical
migration:adaptive significance and timing. Part 2.
Test of the model. Limnologyand Oceanography, 22,
873-886.
Frost, B.W. (1972) Effectsof size and concentrationof
food particles on the feedingbehavior of the marine
planktonic copepod Calanus pacificus. Limnology
and Oceanography, 17, 805-815.
Frost, B.W. (1988) Variability and possible adaptive
significance of diel vertical migration in Calanus
pacificus, a planktonic marine copepod. Bulletin of
Marine Science, 43, in press.
Gabriel W. & Thomas, B. (1988) Vertical migrationof
zooplankton as an evolutionarily stable strategy.
American Naturalist,32, 199-216.
Geller, W. (1986) Diurnal vertical migration of zooplankton in a temperategreat lake (L. Constance): a
starvationavoidance mechanism? Archivfur Hydrobiologie/Supplement,74, 1-60.
George, D.G. (1983) Interrelationsbetween the vertical
migrationof Daphnia and chlorophylla in two large
limneticenclosures. Journalof Plankton Research, 5,
457-475.
Gliwicz, Z.M. (1986) Predation and the evolution of
vertical migrationbehavior in zooplankton. Nature,
320, 746-748.
Gliwicz, Z.M. & Pijanowska, J. (1988) Predation and
resource depth distributionin shaping behaviour of
vertical migrationin zooplankton. Bulletin of Marine
Science, 43, in press.
Hairston, N.G., Jr (1980) The vertical distribution of
diaptomid copepods in relationto body pigmentation.
In Evolution and Ecology of Zooplankton Communities (ed. W.C. Kerfoot),pp. 98-100. UniversityPress of
New England, Hanover, New Hampshire.
Hardy,A.C. (1936) Planktonecology and the hypothesis
of animal exclusion. Proceedings of the Linnean
Society,London, 148, 64-70.
Hardy, A.C. & Gunther,E.R. (1936) The plankton of the
South Georgia whaling ground and adjacent water,
1926-27. 'Discovery'Report,11, 1-456.
Hrba6ek, J. (1962) Species composition and amount of
the zooplankton in relationto the fishstock.Rozpravy
Ceskoslovenske Akademie Ved, Rada matamatychkycha prirodnichved, 72, 1-116.
Huntley,M. & Brooks,E.R. (1982) Effectsofage and food
availability on diel vertical migration of Calanus
pacificus. Marine Biology,71, 23-31.
Hutchinson,G.E. (1967) A Treatiseon Limnology,Vol. II:
Introductionto Lake Biology and the Limnoplankton.
Wiley,New York.
Iwasa, Y. (1982) Vertical migration of zooplankton: a
game between predator and prey. American Naturalist,120, 171-180.
Johnsen,G.H. & Jacobsen,P.J.(1987) The effectof food
limitationon the verticalmigrationin Daphnia longispina. Limnologyand Oceanography, 32, 873-880.
Kerfoot, W.C. (1985) Adaptive value of vertical migration: comments on the predation hypothesis and
some alternatives. In Migration: Mechanisms and
Adaptive Significance (ed. M.A. Rankin),pp. 91-113.
Contributions in Marine Science 27, University of
Texas, PortAransas.
Koslow, J.A. (1979) Vertical migratorssee the light?
Limnologyand Oceanography,24, 783-784.
Kremer, P. & Kremer, J.N. (1988) Energetic and behavioral implications of pulsed food avaiability for
zooplankton. Bulletin ofMarine Science, 43, in press.
Lampert, W. (1987) Vertical migration in freshwater
zooplankton: indirect effectsof vertebratepredators
on algal communities.In Predation: Direct and Indirect Impacts on Aquatic Communities(ed. W.C. Kerfoot & A. Sih), pp. 291-299. UniversityPress of New
England, Hanover, New Hampshire.
Lampert,W., Schmitt,R.-D. & Muck, P. (1988) Vertical
migration of freshwaterzooplankton: test of some
hypothesespredictinga metabolicadvantage. Bulletin
ofMarine Science, 43, in press.
Lampert,W. & Taylor, B.E. (1985) Zooplankton grazing
in a eutrophiclake: implications ofverticalmigration.
Ecology, 66, 68-82.
Lock, A.R. & McLaren, I.A. (1970) The effectsofvarying
and constant temperatureson size of mature copepods. Limnologyand Oceanography, 15, 638-640.
Mackas, D.L. & Bohrer,R.N. (1976) Fluorescence analysis
of zooplankton gut contents and an investigationof
diel feedingpatterns.JournalofExperimentalMarine
Biology and Ecology, 25, 77-85.
Mackas, D.L. & Burns,K.E. (1986) Poststarvationfeeding
and swimming activity in Calanus pacificus and
Metridia pacifica. Limnologyand Oceanography, 31,
383-392.
Manca, M., DeBernardi, R. & Savia, A. (1986) Effectsof
fluctuatingtemperatureand light conditions on the
population dynamics and the life strategiesof migrating and non migratingDaphnia species. Memorie
dell'IstitutoItaliano di Idrobiologia, 44, 177-202.
McAllister,C.D. (1969) Aspects of estimatingzooplankton production fromphytoplanktonproduction.Journal of the Fisheries Research Board of Canada, 26,
199-220.
McLaren, I.A. (1963) Effectof temperatureon growthof
zooplankton and the adaptive value ofverticalmigration. Journal of the Fisheries Research Board of
Canada, 20,685-727.
McLaren, I.A. (1974) Demographic strategyof vertical
migrationby a marine copepod. American Naturalist,
108,91-102.
McMahon, J.W. & Rigler, F.H. (1965) Feeding rate of
foods labelled with
Daphnia magna Straus in different
radioactive phosphorus. Limnology and Oceanography,10, 105-113.
McNaught,D.C. & Hasler, A.D. (1964) Rate ofmovement
of populations of Daphnia in relation to changes in
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions
27
Die] vertical
migration
light intensity. Journal of the Fisheries Research
Board of Canada, 21, 291-318.
Miller,C.B. (1979) Commentsfroma nominaterefereeon
an exchange of notes. Limnologyand Oceanography,
24, 785-787.
O'Brien, W.J. (1987) Planktivory by freshwaterfish:
Thrust and parryin the pelagia. In Predation: Direct
and Indirect Impacts on Aquatic Communities (ed.
W.C. Kerfoot& A. Sih), pp. 3-16. UniversityPress of
New England, Hanover, New Hampshire.
Ohman, M.D., Frost,B.W. & Cohen, E.H. (1983) Reverse
diel verticalmigration- an escape frominvertebrate
predators.Science, 220, 1404-1407.
Orcutt,J.D., Jr& Porter,K.G. (1983) Diel vertical migrationby zooplankton: constantand fluctuatingtemperatureeffectson lifehistoryparametersofDaphnia.
Limnologyand Oceanography, 28, 720-730.
Pearre, S., Jr.(1979a) Problems of detection and interpretation of vertical migration.Journal of Plankton
Research, 1, 29-44.
Pearre, S., Jr(1979b) On the adaptive significance of
verticalmigration.Limnologyand Oceanography,24,
781-782.
Petipa, T.S. & Makarova, N.P. (1969) Dependence of
phytoplankton production on rhythm and rate of
elimination.Marine Biology,3, 191-195.
Pijanowska, J. & Dawidowicz, P. (1987) The lack of
vertical migrationin Daphnia: the effectof homogenously distributedfood. Hydrobiologia, 148, 175181.
Ringelberg,J.(1964) The positivelyphototacticreaction
of Daphnia magna Straus: a contribution to the
understandingof diurnal vertical migration.Netherland Journalof Sea Research, 2, 319-406.
Ringelberg,J.,Van Kasteel, J. & Servaas, H. (1967) The
sensitivityof Daphnia magna Straus to changes in
light intensity of various adaptation levels and its
implications in diurnal verticalmigration.Zeitschrift
fur vergleichendePhysiologie,56, 317-407.
Ringelberg,J. & Royackers, K. (1985) Food uptake in
hungry cladocerans. Archiv far Hydrobiologie,
BeihefteErgebnisse der Limnologie,21, 199-207.
Runge, J.A. (1980) Effectsof hunger and season on the
feedingbehavior of Calanus pacificus, Limnologyand
Oceanography,25, 134-145.
Siebeck, 0. (1960) Untersuchungenfiberdie VertikalwanderungplanktischerCrustaceen unterbesonderer
Berficksichtigungder Strahlungsverhiltnisse.Internationale Revue der gesamten Hydrobiologie, 45,
381-454.
Siebeck, 0. (1978) UV-Toleranz und Photoreaktivierung
bei Daphnien aus Biotopen verschiedener Hohenregionen. Naturwissenschaften,65, 390.
Somero, G.N. & Hochachka, P.W. (1976) Biochemical
adaptations to temperature.In Adaptations to Environment: Essays in the Physiology of Marine
Animals (ed. C.R. Newell), pp. 125-190. Butterworth,
London.
Stich, H.-B. & Lampert,W. (1981) Predatorevasion as an
explanation ofdiurnalverticalmigrationby zooplankton. Nature, 293, 396-398.
Stich, H.-B. & Lampert,W. (1984) Growthand reproduction of migratingand non-migratingDaphnia species
under simulated food and temperatureconditions of
diurnal verticalmigration.Oecologia, 61, 192-196.
Swift, M.C. (1976) Energetics of vertical migrationin
Chaoborus trivittatuslarvae. Ecology, 57, 900-914.
Vuorinen, I. (1987) Vertical migration of Eurytemora
(Crustacea, Copepoda): a compromisebetween riskof
predation and decreased fecundity.Journalof Plankton Research, 9, 1037-1046.
Wolf, H.G. & Mort, M.A. (1986) Interspecifichybridization underlies phenotypic variabilityin Daphnia
populations. Oecologia, 68, 507-511.
Wright,D., O'Brien, W.J.& Vinyard,G.L. (1980) Adaptive
value of vertical migration:a simulation model argument forthe predation hypothesis. In Evolution and
Ecology of Zooplankton Communities (ed. W.C. Kerfoot),pp. 138-147. UniversityPress of New England,
Hanover, New Hampshire.
Zaret,T.M. (1980) Predation and FreshwaterCommunities. Yale UniversityPress, New Haven.
Zaret, T.M. & Suffern,J.S. (1976) Vertical migrationin
zooplankton as a predator avoidance mechanism.
Limnologyand Oceanography, 21, 804-813.
Received 17 March 1988; revised 9 May 1988; accepted
17June 1988
This content downloaded on Fri, 8 Mar 2013 14:24:20 PM
All use subject to JSTOR Terms and Conditions