Relations to Energy and Abundance

142 Pages·2014·15.66 MB·English

by  R. Ehnes

Allometry – Relations to
Energy and Abundance
ZurErlangungdesGradeseinesDoctorrerumnaturalium(Dr.rer.nat.)
genehmigteDissertationvonDipl.Biol.RoswithaB.EhnesausFulda
Januar2014—Darmstadt—D17
FachbereichBiologie
AGBrose
Allometry–RelationstoEnergyandAbundance
Vom Fachbereich Biologie genehmigte Dissertation von Dipl. Biol. Roswitha B.
EhnesausFulda
1. Gutachten: Prof. Dr. UlrichBrose
2. Gutachten: Prof. Dr. NicoBlüthgen
TagderEinreichung: 16. Oktober2013
TagderPrüfung: 12. Dezember2013
Januar2014—Darmstadt—D17
Wir sind so gerne in der freien Natur, weil diese keine Meinung über uns hat.
— Friedrich Nietzsche
i
Contents
1 AimsandScope 1
2 Introduction 2
2.1 Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.2 Body-masseffect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3 Temperatureeffect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.4 AllometricScaling–currentDebate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2.5 MetabolicTheoryofEcologyforendothermsandectotherms? . . . . . . . . . . . . . . 12
2.6 Foodbalancesmetabolicdemand . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
2.7 Diversityofinvertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
2.8 Communityenergyuse. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
2.9 Investigatinganimalsinthesoil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
2.10 Shortoutline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
2.11 Contributionstothepublications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
3 Temperature,predator-preyinteractionstrengthandpopulationstability 20
3.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
3.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
3.3 MaterialandMethods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
3.3.1 Respirationandingestionexperiments . . . . . . . . . . . . . . . . . . . . . . . . 22
3.3.2 Statisticalanalysisofexperimentaldata. . . . . . . . . . . . . . . . . . . . . . . . 23
3.3.3 Longterminteractionstrength . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
3.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
3.4.1 Respirationandingestionexperiments . . . . . . . . . . . . . . . . . . . . . . . . 25
3.4.2 Ingestionefficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
3.4.3 Short-terminteractionstrength . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
3.4.4 Predictionoflong-terminteractionstrength . . . . . . . . . . . . . . . . . . . . . 30
3.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
3.5.1 Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
3.5.2 Body-masseffectsoningestion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
3.5.3 Temperature effects on ingestion, ingestion efficiencies and interaction
strengths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
3.5.4 Temperatureeffectsonpopulationstability. . . . . . . . . . . . . . . . . . . . . . 33
3.6 Caveats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
3.7 Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4 Warmingupthesystem: higherpredatorfeedingratesbutlowerenergeticefficien-
cies 36
4.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
4.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
4.3 Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
4.3.1 Experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
ii
4.3.2 Statisticalanalyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
4.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
4.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
4.6 Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46
5 Phylogeneticgrouping,curvatureandmetabolicscalinginterrestrialinvertebrates 47
5.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
5.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
5.3 Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
5.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
5.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
5.6 Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
5.7 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
6 Respiration rates, assimilation efficiencies and maintenance consumption rates de-
pendonconsumertypes: energeticimplicationsofenvironmentalwarming 58
6.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
6.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
6.3 Materialsandmethods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
6.3.1 Datasets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
6.3.2 Statisticalanalyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
6.3.3 Simulationofmaintenanceconsumptionrates. . . . . . . . . . . . . . . . . . . . 62
6.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
6.4.1 Respirationrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
6.4.2 Assimilationefficiencies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
6.4.3 Maintenanceconsumptionrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
6.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
6.6 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
7 Positive correlation between density and parthenogenetic reproduction in oribatid
mites(Acari)supportsthestructuredresourcetheoryofsexualreproduction 69
7.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
7.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
7.3 MaterialsandMethods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
7.3.1 Regionalscale. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
7.3.2 Globalscale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
7.3.3 Statisticalanalysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
7.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
7.4.1 Regionalscale. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
7.4.2 Globalscale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
7.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
7.5.1 Parthenogeneticreproductioninoribatidmites . . . . . . . . . . . . . . . . . . . 75
7.5.2 Regionalscale. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
7.5.3 Globalscale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
7.5.4 Thestructuredresourcetheoryofsexualreproductionasanintegrativetheory 77
7.6 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
iii
8 Lackofenergeticequivalenceinforestsoilinvertebrates 79
8.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
8.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
8.3 Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
8.4 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
8.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
8.6 Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
8.7 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92
9 GeneralDiscussion 93
10 GeneralSummary 98
11 Zusammenfassung 100
Bibliography 102
ListofFigures 124
ListofTables 127
12 Appendix 128
13 Acknowledgements/Danksagung 130
14 CurriculumVitae 133
iv
1 Aims and Scope
The species in assemblages are linked by interactions. Many of these are trophic interactions,
indicating who eats what and thus, also, the flow of energy through the system. These feed-
ing interactions constitute the food web and are themselves determined by the attributes of the
interactingorganisms.
The complexity of such a food web cannot be understood using only a single methodology.
Different concepts must be used to gain insight into the structure of the system. Likewise, the
system cannot be well understood by examining only a single level and several levels have to be
taken into account. I therefore concentrated on several different aspects and attributes of the
organismsinteractinginfoodwebs.
Itisenormouslydemandingtoderivedetaileddescriptionsoffeedinginteractionsbylaboratory
study. However, such studies do provide precise information on the strengths of the interactions.
Obtaining such precise information for large systems of interacting organisms is, unfortunately,
logistically impossible. It is therefore necessary, for large assemblages, to obtain estimations of
interaction strengths. I therefore used different approaches during my thesis. In the laboratory,
I investigated specific feeding interactions and determined how they are driven by predator body
massandbytemperature. Then,Ifocusedonthemetabolicneedsofdifferentinvertebratesdiffer-
entiating their phylogenetic group and feeding type. I then combined these findings with a field
studytotestdifferenttheoriesoffood-webstructure.
1
2 Introduction
Natural ecosystems consist of many organisms, large or small, rare or abundant. How do all
these organisms relate to each other and how is this assemblage structured? The structure of
these species communities can be characterized by the feeding interactions between the species.
The majority of these organisms are heterotrophs feeding on different resources such as plants
(i.e. herbivores), detritus (i.e. detritivores), or other animals (i.e. predators). The question of
theircoexistenceengagesecologistsanditcannotbeansweredreclusivelybyconcentratingonone
individual organism as it involves factors inherent to the many organisms and also depends on
thehabitat. Forexample,eachorganimsneedstotakeupcertainamountsofenergy,accordingto
certain intrinsic factors, and can conversely be fed on by other organisms. These intrinsic factors
includeforexamplebodymassoftheorganism,itsphysiology,feedingtype,phylogeny,andactivity
level(Fig.2.1). However,alsotheenvironmentwithitsspecificpropertiesinfluencestheenergetic
demandofanorganismviatemperatureeffects,orfactorslikehabitattype,possibledisturbances
(human land use), or properties of the occurring resources (for instance their type, body mass
(energeticcontent),availability,orabundance,Fig.2.1).
temperature
habitat type
body mass disturbance
physiology
feeding type
land use
phylogeny
activity level
resource
(type, body mass, availability)
Figure2.1:Factorsthatinfluencethemetabolicdemandofanorganism.Greenbackgroundrepre-
sentstheenvironmentanditsinfluencesontheorganism,theintrinsicfactorsaregiven
insidetheorganism.
Animalcommunitiesconsistofmanyorganismswhichbelongtodifferentspeciesandshowdif-
ferentabundances. Asitisnotaneasytasktodeterminetheenergydemandofoneorganism,itis
nottrivialtodeterminehowmuchenergythewholecommunityneeds. Aspeciesenergydemand
isinfluencedbyseveralfactorstheinterplayofwhichmakesitsassessmentevenmorecomplicated
(HumphriesandMcCann,2013). Whilealotofstudiesonenergydemandormetabolismfocused
on mammals little is known about invertebrates. Communities consist of many species and small
speciesaregenerallymoreabundantthanlargeones. Thesedifferentorganismspossessdifferent
energydemands,feedingtypes,trophiclevelsandabundances. However,allofthemneedto–at
least–balancetheirenergydemands. Thus,everyorganism,basically,needstoabsorbenergy(sun
2
light,plantmaterial,preyorganisms,deadorganicmatter,etc.) formetabolism,growthandrepro-
duction. I concentrated on invertebrate organisms to investigate their energetic demand and the
consequencesofdifferentenergeticneedsofvariousorganisms(differentphylogeneticgroups)for
communities. Invertebratesarepoikilothermicanimalsandthusareoffadifferentmetabolictype
thanmammalsandbirds. Theirbodytemperaturedependsontheenvironmentaltemperatureand
followsenvironmentaltemperaturechanges,butthisdependencycanbemodifiedbythebehaviour
oftheanimal. Thus,bodytemperatureofpoikilothermicanimalsismuchmorevariablethanthat
of mammals or birds. As a consequence of this temperature dependency, the body temperature
of poikilothermic animals can be estimated by measuring environmental temperature. However,
thebiochemicalreactions, thedeterminantsofmetabolismand, therebyenergydemand, proceed
moreeasilyinwarmerenvironments(Arrhenius,1889)andlessactivationenergyisneededwhen
itiswarmer. Furthermore,thelifestageoftheorganismalsohasanimportanteffect: istheanimal
growing or a full-grown adult? Is the animal moving – fast or slow – is it sitting, resting or even
hibernating? Allthesefactorsinfluencemetabolicratesandaccordinglyenergydemand.
Tobeabletoanswerthequestionsofcoexistenceandenergydistributioninnaturalcommunities
severalotherquestionshavetobeansweredfirst. ThequestionsIwanttoanswerinmythesisare:
What determines the metabolic rate and hence, the demand of an organism, is it body mass or
the environmental temperature? Are there applicative models for this description? What further
influenceshavetobeaccountedfor? Inwhatwaydoestheenergeticdemandofanindividualaffect
thestructureofcommunities? Whatistheimpactoftheseenergeticrestrictionsonthedistribution
ofanimalsandmayitbeaffectedbyhumanlanduse?
Some of these questions cannot be answered in the field, because there are no methods for
direct measurement. Thus, we need data from laboratory work to be able to draw conclusions
about what may happen in the field, especially if it is a "field" that is difficult to observe like soil-
animal communities. In the following, I will introduce some theories and models which aim to
explainvariousfactorsthat,puttogether,areabletoexplainthemetabolicconstraintsthatshape
food-webassemblages.
2.1 Metabolism
Everyorganismneedsenergyforsurvival(sustainthevitalfunctions)andfurthermoreforgrowth,
movement, andreproduction. Metabolismisthesumofallprocessesthatalloworganismstoob-
tain energy for their functioning. Thus, metabolic rates can be described as the combined rates
ofenergyuptake,transformationandallocation(Brownetal.,2004;HickmanandWeber,2008).
Phototrophicorganisms(plants,algaeandsomebacteria)useenergyfrom(sun-)light,carbondiox-
ide,andwatertogeneratecarbohydratesandoxygen. Heterotrophicorganismsontheotherhand
usechemical compounds (carbohydrates, lipids, andproteins) andoxygen foraerobic organisms,
to yield energy and set free carbondioxide and water. Nutrients are digested to generate smaller
compoundswhichwillbeprocessedfurther. Thus, passingthroughdifferentmetabolicsteps, like
digestion,glycolysis,tricarboxylicacidcycleandrespiratorychain,resourcesaredigested,energy
rich compounds like ATP (Adenosine-5’-triphosphate) are produced (Hickman and Weber, 2008)
andindigestibleresiduesareexcreted. Energyfromorganiccompoundsaretransferedtoenergy-
richcompoundsinstepwiseenzymaticreactionsforstorageandfortransportationtoallowusage
in different parts. The most important energy-storage compounds are ATP and NADPH (Nicoti-
namide adenine dinucleotide phosphate). The products of the cellular respiration, that needs
carbohydrates and oxygen (for aerobic organisms) are carbondioxide and water (Brown et al.,
3
2004). Theoverallreactionofglucoseandoxygentocarbondioxideandwatercanbesummarized
asfollows:
C H O +6O −→6CO +6H O+energy (2.1)
6 12 6 2 2 2
However, this reaction is not possible in a single reaction, but requires multiple steps. The
differentstepsareassociatedwithspecificcellularcompartmentsineukaryotes.
At first, in the glycolysis, which takes place in the cytosol, glucose is degraded to pyruvate.
In a second step acetyl-CoA is formed from degraded pyruvate in the mitochondria. The third
part is the tricarboxylic acid cycle, which with its small number of reactions makes up the core
of metabolism (Morowitz et al., 2000) and leads to the creation of energy-rich compounds (ATP,
NADH or NADPH), water, and carbondioxide. During these reactions electrons are transported
acrosstheinnermitochondrialmembranewhichleadstothecreationofaprotongradientacross
the membrane which is then used to synthesize ATP. The nascent energy is stored as energy-rich
molecules. WhileATPisrelativelystableinaphysiologicalenvironment,itcaneasilybehydrolized
inacatalyticcycletosetfreethecontainedenergy.
Thus, a breathing animal ‘consumes’ the amount of oxygen needed for the chemical reactions
and releases the ‘used’ oxygen as carbon dioxide. The oxygen content of the respiratory air is re-
ducedandthecarbondioxidecontentisenrichedcomparedtobeforebreathing. Theconsumption
ofoxygenandtheproductionofcarbondioxideenablesexternalmeasurementofenergyusedbyan
heterotrophic organism. As the stoichiometry of respiratory gas exchange and the rate of oxygen
consumption is fixed, estimating the decrease in oxygen concentration or the increase in carbon-
dioxide concentration will enable calculation of the metabolic demand. Different methods have
been developed for measurement of the oxygen reduction and carbondioxide accumulation. For
the measurements in this thesis an automated electrolytic microrespirometer (Scheu, 1992) has
beenused(Chapter3,4,5).
Basal, standard or resting metabolic rate describe the energy an organism needs for mere sur-
vival. Thus,basalmetabolicrateistheminimumvalueofmetabolicrate. Ifanorganismmoves,the
metabolic rate increases. Two types of metabolic rates above basal metabolic rates are common:
field and maximum metabolic rate. Field metabolic rate can be described as the mean metabolic
rate of an animal that moves and rests alternately. Whereas maximum metabolic rate is a de-
scription for a continuously running (heavily respiring) animal. Therefore, field metabolic rate is
somewhatintermediatebetweenbasalandmaximummetabolicrate,andquitecomplicatedtode-
termine. Causedbythedifficultytocontrolforthemovementofanorganism,metabolicratesare
oftendeterminedfromanimalsatrest. Theserestinganimalsshowarelativelyconstantmetabolic
ratewithoutlargeorabruptfluctuationsandprovideinformationaboutthebasalenergeticneeds
ofaninactiveorganisminthelaboratoryandthus,itsessentialenergydemand.
Measuredoxygenuptakeofanorganismcanbetransferredintoenergeticequivalentsbyusing
therelationshipdescribedbyPeters(1983):
1431.03µgO ≡20.1J (2.2)
2
This conversion allows the estimation of the energy demand of an organism at rest from the
amountofoxygenitusesperunittime. Measuredoxygenuseofanorganismatdifferenttemper-
aturescanbeusedtogainvaluesforbasalmetabolicrateofanindividualwithadeterminedbody
mass. Fromthis,themetabolicrateperunitmassofdifferentorganismscanbecalculatedtoallow
furthercomparison.
4