HOW TRAITS ARE INTERRELATED THROUGH. Survival. Fecundity. Survival and fecundity both depend on Feeding. To eat. To survive.
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1 --5 What is a key trait? A property that is a main determinant of an individual s fitness HOW TRAITS ARE INTERRELATED THROUGH TRADE-OFFS IN ZOOPLANKTON* m m. mm.5 mm. mm Commonly used fitness measures: Net reproductive rate Survival R lxmxdx Fecundity.5 mm. mm.5 mm.5 mm Thomas Kiørboe Centre for Ocean Life, DTU Aqua Survival and fecundity both depend on Fundamental missions What is a usefull trait? What is common between these organisms? Foram feeding on copepods feeeding copepod To eat To survive To reproduce Coutesey Lombard. mm. mm Wing snail with mucus net mm cm ing hydromedusa Gilmer & harbison Mar Biol 9; Kiørboe et al. PNAS 9; Hansson & Kiørboe LO 5 What is a trade off? The costs and benefits of a certain trait. mm EAT mm EATEN Traits are interrelated through trade-offs Conflicts between missions Survival reproduction Copepod nauplius capturing a prey As it jumps, the nauplius itself is perceived by a predator Behavioral interaction Growth Bruno et al. PlosOne, Kjellerup & Kiørboe Biol Lett Both movies in SloMo Energy allocation Litchman et al. JPR
2 --5 Outline Zooplankton feeding traits Three principal feeding modes. Taxa trascending feeding traits. Behavioral trade offs a. Survival (Predation risk) b. Reproduction Cruise current (Hovering). Energy allocation tradeoffs a. Maintenance (survival) vs. Growth & reproduction. Synthesis Kjellerup & Kiørboe Biol Lett Keyword: Taxa-transeding; Mechanistic; Rationalize & Generalize Passive feeding modes Kiørboe Biol Rev Active feeding modes All movies in SloMo :-: Diversity of ambush feeders: Taxa transcending Diversity of current feeders: taxa transcending Choanoflagellate (Video: LT Nielsen) Apendicularian (Video: F Lombard) Foram feeding on copepods feeeding copepod.5 mm Coutesey Lombard. mm. mm 5 µm Wing snail with mucus net mm Copepod SloMo Doliolid cm ing hydromedusa Gilmer & harbison Mar Biol 9; Kiørboe et al. PNAS 9; Hansson & Kiørboe LO 5 Tiselius et al LO µm Kiørboe JPR 7 mm Trade-offs: efficiency The principal feeding modes differ in efficiency Cruise All movies in SloMo : -: current (Hovering) efficiency The basis for the conclusion and generalisation:. Mechanistic understanding of encounter mechanisms Hover & Cruise rate Kjellerup & Kiørboe Biol Lett g C/mg C/h ik LOW Kiørboe Biol Rev Volume of water scanned per unit time HIGH Nielsen & Kiørboe in prep Nielsen & Kiørboe ISME J 5 Tiselius et al. LO J Body mass, mg C. Theoretical analysis of corresponding encounter models. Experimental tesgting of predictions Kiørboe ICB Kiørboe Biol Rev
3 --5 All in SloMo ~ x 5 Trade-offs: Risk and cost of feeding behavior and fluid signals Four propulsion modes Propulsion and feeding are partly related Breast stroke Hovering and swimming (active feeders) Swimming (ambush feeders) Jumping.5 mm SloMo :.5 mm SloMo :5 (reposition jump) LOW Cruise current (hovering) HIGH Cruising Kiørboe et al. Proc. Roy Soc B ; Kiørboe & Jiang J Roy Soc Interface. mm.5 mm SloMo : SloMo : Diversity of breast strokers: Taxa transcending Diverse organisms and diverse machineries Cladoceran Nauplius Flagellate Diversity of cruisers: Taxa transcending Pushers and pullers Rotifer Copepod pusher Puller.5 mm SloMo : Ciliate. mm SloMo : m SloMo ca.: Guasto et al. PRL. mm Dinoflagellate SloMo : 5 m SloMo : Dinoflagellate m SloMo : m m SloMo : Fluid disturbances Flow and vorticity fields Crusing flagellate Junping copepod Extension of flow field: temporal variation Area with imposed velocities > U* (= Predator encounter cross section) Oxyrrhis marina. Crusing rotifere Hovering nauplius S. mm/s, mm... Time, ms SloMo : Kiørboe et al. PNAS U* =. mm/s SloMo: Kiørboe et al. PNAS
4 --5 Peak extension of flow field Feeders generate larger flow fields than swimmers log(s.5 mm/s, mm ) Feeders (cruise, hover) Swimmers (Jumpers and breast strokers) ( feeders) Log Re P. intermedius T. longicornis naupl A. tonsa naupl O. davisae fem O. davisae male A. tonsa cop M. rubrum A. tonsa cop M. lucens Dinoflagellates T. longicornis naupl B. pliciatilis T. longicornis cop Swimmers Feeders Kiørboe et al. PNAS Spatial attenuation of flow fields During peak of power stroke (closed symbols) u, m s Oithona davisae male ~ r -.. r, mm u,m s- - Acartia tonsa nauplius ~ r -.. r, mm Kiørboe et al. PNAS Spatial attenuation More examples Jump: - Breast stroke: A B C D Swimming - ~ r - ~ r -.5. (ambush).5..5 ~ r - ~ r E F G. H ~ r -.5 ~ r - ~ r - 5. ~ r - ~ r ~ r - and swimming (Hover, Cruise) ~ r - ~ r- Hover: Cruise: - r, mm A. tonsa jump (A); O.davisae jump (B); Podon swim (C); A. tonsa naupli swim (D); Metridia cruising (E); Dinoflagellate cruising (F), Temora nauplius feeding current; Temora copepodit hovering Kiørboe et al. PNAS U, m s - Idealized models Hovering (feeding current) (negatively boyant) F tether = Excess weight F feeding current Ffeeding current STOKESLET Only red forces act on the water R - R - R - Crusing (Neutrally boyant) F swim F drag F drag = F swim STRESSLET Kiørboe et al. PRSB Jumping (Jump) F drag =F swim IMPULSIVE STRESSLET Breast stroke: Quadropole Breast stroke swimming: appendages follow streamlines of a potential dipole (quadropole) R - Bulk properties of flow Spatial flow attenuation from idealized, taxa transcending models Predicted streamlines observed streamlines Breast swimming nauplius Behaviour Purpose Model Attenuation Hovering Stokeslet R Cruising & locomotion Stresslet R (Jumping) Locomotion Impulsive stresslet R (Breast stroking) Locomotion Quadropole (potential dipole) R Kiørboe et al. PNAS ; Andersen et al. PRE 5 we can rationalize and therefore generalize the observed fluid disturbances
5 --5 tradeoffs Predation risk estimated from simple generic fluid mechanical models Log (Detection distance, mm) Predation risk Cruise Hovering. Mean body length, mm l O /mg C/h Brun unpublished.5 Respiration.5 Hover & Cruise.. -5 Active - - Prosome length, mm Body mass, mg C Kiørboe et al. Proc Roy Soc B Fecundity...5 tradeoff: Experimental testing Rheotactic predator feeding on active and passively feeding nauplii Active feeder predation rate (n nauplii predator - d - ) behavior specific predation rate - 5 Active vs. Passive feeding modes Prey concentration (n nauplii L - ) THE MORTALITY RISK OF THE ACTIVE FEEDER IS T. longicornis O. davisae MUSCH HIGHER THAN THAT OF THE PASIVE FEEDER Someren Gréve and Almeda unpublished feeder, swimming, and predation risk Experimental testing: Large copepod feeding on nauplii Trait based models Examples of trait based models of zooplankton Active feeder predation rate (n nauplii predator - d - ) behavior specific predation rate - Active vs. Passive 5 Prey concentration (n nauplii L - ) C. hamatus O. nana SAME RESULT FOR DIFFERENT SET OF PREY Someren Gréve et al unpublished feeder Kaisia Kenitz: Seasonal succssion of zooplankton feeding traits Fi Prowe: Global distribution of zooplankton feeding traits Trait biogeography Field data that allow testing of models Traits are interrelated through trade-offs Conflicts between missions feeding trait Active feeding trait Survival reproduction Brun et al in prep Behavioral interaction Energy allocation Growth Litchman et al. JPR 5
6 --5 Reproduction Flow field Blind dating: Cruise feeder Flow field How do they find one another? Pheromone trail I will show that mate finding strategies depend on feeding behavior Escaping: Probably the fastest in the world Bagøien & Kiørboe MEPS 5 Blind dating: current feeder Pheromone cloud Blind dating: current feeder Pheromone cloud Kiørboe & Bagøien MEPS 5 Kiørboe & Bagøien MEPS 5 How can an ambush feeder ever find a mate? Sex, food and death mortality reproduction tradeoffs Flow field Escaping: Probably the fastest in the world The males sacrifices feeding for part of their time to search for females. When searching they also run elevated predation risk Kiørboe LO 7 Mate finding compromises survival and feeding in males differently for different feeding bahaviors Escaping: Probably the fastest in the world
7 --5 Mate finding and predation risk Experimental test: Different predation mortality risks between sexes Differential mortality and biased sex ratios Observed and predicted sex ratios for ambush, feeding current, and cruiser feeding behaviors >. >.5 >.-. Predation rate, prey per day.5..5 CRUISE FEEDER: no difference Male Female. AMBUSH FEEDER: Higher mortality risk in males 7 5 MALE/FEMALE SEX RATIO.. Family level Species level. CALANIDAE (). OITHONIDAE (). EUCHAETIDAE (). METRIDIIDAE (). PARACALANIDAE (). ONCAEIDAE (). CENTROPAGIDAE (5). TEMORIDAE (5) 9. ACARTIDAE (). CANDACIIDAE () Prey concentration, copepods per L Someren Gréve and Almeda unpublished 5. CLAUSOCALANIDAE (7) 7. PSUDODIAPTOMIDAE (9) N = Kiørboe Oecologia Energy allocation tradeoffs Evolution of ageing Disposable soma theory:. Investment in survival (maintenance) is traded off against investment in growth and reproduction. Large external mortality (relative to total mortality) may push the tradeoff against low investment in maintenance Application to zooplankton:. High risk (feeding, mate finding) behaviors lead to early aging and short life spans, even in the absence of predators, and high fecundity and vice versa Predictions:. feeders: Long lifespan, low fecundity, large male/female difference in lifespan. Active feeders: the opposite tradeoffs Empirical support: Differences in survivorship Survival..... AMBUSH FEEDER Oithona davisae Females Males Time, days CRUISE FEEDER Centropages typicus.. Survivorship measured in lab in absence of predation..... Females Males Kiørboe et al. Ecology 5 Variation in survivorship species of copepods: Longevity varies by factor between species Results behavior and gender are the main determinants of longevity and ageing Log (T) = a + b Mixed + c Sex. Dependent variable Mean longevity Intercept Sex Mixed vs separate Gender Male vs female behaviour Passive vs active Coefficient.7 (9 d). ( %). ( %).5 (+79 %) p value... Ageing shape Intercept behaviour Passive vs active Gender Male vs female Coefficient.7 (.).55 (7 %). ( %) p value..5 Kiørboe et al. Ecology 5 Kiørboe et al. Ecology 5 7
8 --5 Energy allocation The maintenance vs fecundity trade off? Specific fecundity, per day... Active feeding modes (cruise, hover) Passive feeding modes (ambush). Body mass g C Broadcast; Active Sac; Active Sac; TAKE HOME:. Energy acquisition (feeding) is the governing mission from which key traits and tradeoffs should be defined. In zooplankton, mate finding, predation risk, propulsion mode, longevity, ageing, fecundity, and energy allocation are all defined by the feeding behavior. A mechanistic understanding of feeding traits in zooplankton allows us - to rationalize and generalize observations and hence to define key taxa-transcending traits - to quantify tradeoffs. This provides a solid, mechanistic basis for the development of traitbased models Kiørboe et al. Ecology 5 ACKNOWLEDGEMENTS: Funding: Centre for Ocean Life is funded by The Villum Foundation Danish Research Council for Fundamental Research HC Ørsted Foundation Niels Bohr Foundation EU (Marie Curie) Collaborators: Hoshuo Jiang Rodrigo Almeda Hans Sommeren Greve Philipp Brun Espen Bagøien Fi Prowe Lasse Tor Nielsen Peter Tiselius Uffe H Thygesen And others from the Ocean Life teams
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