Diel Vertical Migration of Zooplankton in Lakes and Oceans: causal explanations and adaptive significances

360 Pages·2010·9.44 MB·English

by  Joop Ringelberg (auth.)

Diel Vertical Migration of Zooplankton
in Lakes and Oceans
Joop Ringelberg
Diel Vertical Migration
of Zooplankton in Lakes
and Oceans
Causal Explanations and Adaptive
Significances
123
JoopRingelberg
Stationsstraat90
3881AGPutten
Netherlands
[email protected]
ISBN978-90-481-3092-4 e-ISBN978-90-481-3093-1
DOI10.1007/978-90-481-3093-1
SpringerDordrechtHeidelbergLondonNewYork
LibraryofCongressControlNumber:2009936304
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Plate1 DaphniagaleataxhyalinefromLakeMaarsseveen(notethatthecompoundeyehasbeen
turnedinaventraldirection).ThehybridsplayedanimportantroleinthestudyofDVMinthelake
andinthelaboratoryexperimentsoftheDepartmentofAquaticEcology,UniversityofAmsterdam.
(PhotographbyMichaelaBrehm,CentreforLimnology,Nieuwersluis,theNetherlands.)
v
Preface
Whatevertheorymaybeadvancedtoexplaindiurnalmigration,
theunderlyingreactionsinvolvedmustbedemonstratedconclu-
sively in the laboratory before the explanation can be finally
accepted
GeorgeL.Clarke1933p.434
In oceans and lakes, zooplankton often make diel vertical migrations (DVM),
descendingatdawnandcomingupagaininlateafternoonandevening.Thesmall
animals cover distances of 10–40 m in lakes or even a few hundred metres in the
open oceans. Although not as spectacular as migrations of birds or the massive
movementsoflargemammalsovertheAfricansavannas,thenumbersinvolvedare
verylargeandthebiomassexceedthebulkoftheAfricanherds.Forexample,inthe
Antarcticoceansswarmsof“Krill”maycoverkilometresacross,withthousandsof
individualspercubicmetre.TheseEuphausiidsarefoodforwhales,themostbulky
animalsonearth.
Zooplanktonarekeyspeciesinthepelagicfoodweb,intermediarybetweenalgae
and fish, and thus essential for the functioning of the pelagic community. Prey for
many,theyhaveevolveddiversestrategiesofsurvivalandDVMisthemostimpor-
tantone.Mostfisharevisuallyhuntingpredatorsandneedahighlightintensityto
detecttheoftentransparentanimals.Bymovingdown,thewell-litsurfacelayersare
avoidedbuttheyhavetocomeupagainatnighttofeedonalgae.Thisdescription
istoosimple,however,becauseatrade-offbetweenadecreasedpredationandless
foodispresent.Thusbenefitsmaybesmallerthancosts.Thatdependsoncircum-
stances,ofcourse,whichimpliesthattheindividualhasto“decide”whentomigrate
and how deep. During evolutionary time, a physiological–behavioural mechanism
must have been selected for with information from the environment as decisive
input. This topic is hardly touched upon in the hundreds of articles that appeared
in more than a century of research. For decennia the simple hypothesis that zoo-
planktonfolloweda“preferred”lightintensitywhenmovingupanddownwiththe
setting and rising of the sun reigned. In the last 30 years the aspect of predator
avoidancegotmostattentionasifbythatthefinalexplanationwasgiven.Andfew
authorsareconcernedwithcausalmechanismsanddecision-making.
Inthisbook,thephysiological–behaviouralmechanismsarecentraltopics.Light
intensitychangestriggercomplexphotobehaviour,guidingtheanimalsintoatimely
vii
viii Preface
descentandaprudentascent.Photobehaviourhasnoobviousrelationwithadaptive
goalsandintheopinionofsomeis,therefore,notimportant.However,withoutlight
intensitychanges DVMwould not occur. Causal mechanisms were predominantly
studied in Daphnia, but the results can be applied to many migrating species in
lakesaswellasoceans.Thecruciallightchangesofdawnandduskareessentially
the same, everywhere and always (yes, I know of seasons and latitudes). About
the causal explanations presented in this book, the last word is not said. It never
isinscience.Buttheyarepresentlythebestexplanations.Overtheyearsofstudy,
themechanismshavebecomecomplicatedandcannotbecomprehendedbyreading
summaries of the original articles only. I try to give a comprehensive picture now.
Ultimateaspectsarenotshunnedbutaslongasspeculationsarealargepartofthe
literature,mentioningoftheseaspectshadtobemodest.Clarke’sdictumalsoholds
fortheultimatelevelofinvestigations.
I do not treat the literature exhaustively. There are excellent reviews where the
manyresultsandopinionsarepresentedobjectively,withoutmuchcomment.Ihad
tomakechoicesfromthelargenumberofarticlesbecauseItriedtoscrutinisewhat
was implied and to compare with the principles and philosophy of the book. Did
I violate the principle of being objective? It is up to critical readers to say so.
Comparedtoothertopicsinbiology,IthinkthatDVMresearchhasnotmademuch
progressand,afterthestimulatingimpulseofrealisinghowimportantpredatorsare,
isslowingdownagain.
The set-up of the book is perhaps a bit unusual and needs explanation.
Traditionally, descriptions of ecological phenomena and relevant environmental
factors precede the presentation of mechanisms and explanations. Because most
readerswillbefamiliarwithDVM,Istartwiththeunderlyingphysiologyofstim-
ulusperceptionandtheresultingbehaviour(Chapters1,2,3,4and5)asobtained
with laboratory experiments. That opened a way to think about the role of essen-
tial“light”and“temperature”as“biologicalfactors”(Chapter6).Iamawareofthe
independent existence of physical factors but I also recognise that each individual
perceivesandprocessesabioticfactorsinawaythatdependsonaspecies-specific
physiology.Processingoccurspredominantlyinthecentralnervoussystemandthe
factorgetsnewbiologicalproperties.
ThebookcontinueswithDVM,asencounteredinthefield(Chapters8,9and10).
Ilookedforstudieswithextensiveanddetaileddata.Thereafter,inChapter11,the
conclusionsfromtheexperimentswereintegratedwithfielddatainafinalvalidation
ofideas.
Diel vertical migration is multifaceted with, amongst others, consequences
for population dynamics, food web structure and community composition. In
Chapter12, the development of a Daphnia population during a period of migra-
tionwaspresentedandinthelastchaptertheinformationflowassuperimposedon
thematerialflowinatritrophicfoodchainwaspresented.
DVMcannotbestudiedwithoutdedicatedcolleagues.Tenyearsofuniquefield
work in Lake Maarsseveen would have been impossible without the organisation
and control of Ben Flik and the talent for being able to fix everything by Dick
Lindenaar. Koen Royackers participated in the first years and Erik van Gool in
Preface ix
the last years. Niels Daan helped when the size and distribution of the 0+ fish
population had to be estimated. An intensive acoustic study in the lake by Annie
Duncan,BrianQuiliiam(RoyalHollowayUniversityofLondon)andJanKubecka
(HydrobiologicalInstitute,CeskeBudejovice,CzechRepublic)contributedmuchto
ourknowledgeofthejuvenilefishpopulationinthelake.Ididnotalwayshavethe
time to participate in the field study because of duties at the university. Moreover,
my attention was also focused on photobehaviour experiments, in the last years
together with Erik van Gool. We had long discussions before we understood (do
we?) “decision-making” in Daphnia. DVM starts long before sunrise and occurs
predominantlyaftersunset.Inearlysummer,nightsareshortandtheneedtosleep
was not always felt on these weekly days at the lake. We were among friends, I
think.
Drafts of some chapters were read by Jan Verheijen, Erik van Gool, Koos
Vijverberg,NielsDaanandOttoSiebeckforcriticalcommentsonseveralchapters.
For30yearsBenFlikplayedacentralroleintheorganisationofourDepartment
of Aquatic Ecology, University of Amsterdam. His friendship was often of great
helptome.
Finally,Ithankmysonanddaughtersforsupportandunremittinglove.
Putten,theNetherlands JoopRingelberg
Contents
1 Windows:AnIntroduction . . . . . . . . . . . . . . . . . . . . . . 1
1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Individuals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.3 SensoryPhysiologyandBehaviour . . . . . . . . . . . . . . . 3
1.4 TheEcologicalContext. . . . . . . . . . . . . . . . . . . . . . 6
1.5 Finally . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2 SwimminginaStrangeBiotope . . . . . . . . . . . . . . . . . . . . 11
2.1 AStrangeEnvironment. . . . . . . . . . . . . . . . . . . . . . 11
2.2 Small-Scale,“Normal”Swimming . . . . . . . . . . . . . . . . 14
2.2.1 TheFunctionofOscillatingSwimming. . . . . . . . . 19
2.2.2 TheMechanismattheBaseofOscillatingSwimming . 21
2.3 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
3 Light-Induced,ReactiveSwimming . . . . . . . . . . . . . . . . . . 25
3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
3.2 TheStimulusConcept . . . . . . . . . . . . . . . . . . . . . . 26
3.3 VisualThresholds. . . . . . . . . . . . . . . . . . . . . . . . . 29
3.4 ReactionstoInstantaneousChangesinLightIntensity . . . . . 31
3.5 ReactionstoContinuousChangesinLightIntensity. . . . . . . 35
3.5.1 TheStepwiseReactionPattern . . . . . . . . . . . . . 35
3.5.2 TheStimulusStrength–DurationCurve. . . . . . . . . 37
3.5.3 SwimmingSpeedandDisplacementVelocity . . . . . 41
3.6 PhotobehaviourinOtherPlanktonicSpecies. . . . . . . . . . . 43
4 ADecision-MakingMechanism . . . . . . . . . . . . . . . . . . . . 49
4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
4.2 TheInterdependenceofTwoSuccessiveStimuli . . . . . . . . 51
4.3 TheInfluenceofKairomone,FoodandTemperature . . . . . . 52
4.4 Other Kinds of Experiments to Study the Role
ofKairomonesandFood . . . . . . . . . . . . . . . . . . . . . 61
4.5 ADecision-MakingMechanism . . . . . . . . . . . . . . . . . 65
5 MechanisticModels . . . . . . . . . . . . . . . . . . . . . . . . . . 71
5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
xi
xii Contents
5.2 AModelofOscillatingSwimming . . . . . . . . . . . . . . . . 75
5.3 ThePhotobehaviourModel. . . . . . . . . . . . . . . . . . . . 80
5.4 TheDVMModel . . . . . . . . . . . . . . . . . . . . . . . . . 86
6 LightandTemperature . . . . . . . . . . . . . . . . . . . . . . . . 105
6.1 Introduction:TheRelevanceof“BiologicalFactors” . . . . . . 105
6.2 PhysicalAspectsofLightinWater . . . . . . . . . . . . . . . . 107
6.2.1 TheAir–WaterInterface . . . . . . . . . . . . . . . . 107
6.2.2 TheAngularLightDistribution . . . . . . . . . . . . . 109
6.2.3 DownwellingLightAttenuation . . . . . . . . . . . . 110
6.2.4 UltravioletRadiation . . . . . . . . . . . . . . . . . . 113
6.3 The“BiologicalFactor”Light . . . . . . . . . . . . . . . . . . 116
6.4 Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . 122
7 OpticalOrientations . . . . . . . . . . . . . . . . . . . . . . . . . . 129
7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129
7.2 TheStructureofOpticalSenseOrgansofCladocerans
andCopepods . . . . . . . . . . . . . . . . . . . . . . . . . . . 131
7.2.1 TheCompoundEyeof Daphnia . . . . . . . . . . . . 131
7.2.2 TheNaupliusEye . . . . . . . . . . . . . . . . . . . . 136
7.3 TheOrientationofDaphniaintheVerticalPlane . . . . . . . . 138
7.3.1 PinnedAnimals . . . . . . . . . . . . . . . . . . . . . 138
7.3.2 Free-SwimmingDaphnia . . . . . . . . . . . . . . . . 141
7.3.3 TheMechanismofContrastOrientation . . . . . . . . 143
7.4 OpticalOrientationinOtherPlanktonicAnimals . . . . . . . . 149
8 ConsiderationsBeforeGoingintotheField . . . . . . . . . . . . . 161
8.1 GeneralIntroduction . . . . . . . . . . . . . . . . . . . . . . . 161
9 DielVerticalMigrationinLakes . . . . . . . . . . . . . . . . . . . 171
9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171
9.2 TheSeasonalCharacterofMigration . . . . . . . . . . . . . . 172
9.2.1 ANaturalExperiment . . . . . . . . . . . . . . . . . . 175
9.2.2 TheBeginningofthePeriodofDielVertical
Migration . . . . . . . . . . . . . . . . . . . . . . . . 180
9.2.3 TheDevelopmentoftheMigrationAmplitude . . . . . 184
9.3 DielVerticalMigrationCausedbyUVRadiation . . . . . . . . 190
9.3.1 TheDamagingEffectsofUltravioletRadiation . . . . 191
9.3.2 InducedMigrations . . . . . . . . . . . . . . . . . . . 196
9.4 TheInfluenceofFood . . . . . . . . . . . . . . . . . . . . . . 201
9.5 Complications . . . . . . . . . . . . . . . . . . . . . . . . . . 204
9.5.1 ReverseMigrations . . . . . . . . . . . . . . . . . . . 205
9.5.2 Drifts . . . . . . . . . . . . . . . . . . . . . . . . . . 208
9.6 Interpretations . . . . . . . . . . . . . . . . . . . . . . . . . . 210
10 MigrationsintheMarineEnvironment . . . . . . . . . . . . . . . . 217
10.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217