Abstract
Male copepods must swim to find females, but swimming increases the risk of meeting predators and is expensive in terms of energy expenditure. Here I address the trade-offs between gains and risks and the question of how much and how fast to swim using simple models that optimise the number of lifetime mate encounters. Radically different swimming strategies are predicted for different feeding behaviours, and these predictions are tested experimentally using representative species. In general, male swimming speeds and the difference in swimming speeds between the genders are predicted and observed to increase with increasing conflict between mate searching and feeding. It is high in ambush feeders, where searching (swimming) and feeding are mutually exclusive and low in species, where the matured males do not feed at all. Ambush feeding males alternate between stationary ambush feeding and rapid search swimming. Swimming speed and the fraction of time spent searching increase with food availability, as predicted. This response is different from the pattern in other feeding types. The swimming speeds of non-feeding males are predicted and observed to be independent of the magnitude of their energy storage and to scale with the square root of body length in contrast to the proportionality scaling in feeding copepods. Suspension feeding males may search and feed at the same time, but feeding is more efficient when hovering than when cruising. Therefore, females should mainly be hovering and males cruising, which is confirmed by observations. Differences in swimming behaviour between genders and feeding types imply different mortality rates and predict well the observed patterns in population sex ratios. Sex ratios may become so female-biased that male abundances limit population growth, demonstrating that behaviours that are optimal to the individual may be suboptimal to the population.
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References
Acharya L (1995) Sex biased predation on moths by insectivorous bats. Anim Behav 49:1461–1468
Bagøien E, Kiørboe T (2005a) Blind dating – mate finding in planktonic copepods. I. Tracking the pheromone trail of Centropages typicus. Mar Ecol Prog Ser 300:105–115
Bagøien E, Kiørboe T (2005b) Blind dating – mate finding in planktonic copepods. III. Hydromechanica communication in Acartia tonsa. Mar Ecol Prog Ser 300:129–133
Behrens JW, Praebel K, Steffensen JF (2006) Swimming energetics of the Barent Sea Capelin (Mallotus villosus) during the spawning migration period. J Exp Mar Biol Ecol 331:208–216
Berg HC (1993) Random walks in biology. Princeton University Press, Princeton
Bollens SM, Frost BW (1989) Predator-induced diel vertical migration in a planktonic copepod. J Plankton Res 11:1047–1065
Bossert WH, Wilson EO (1963) The analysis of olfactory communication among animals. J Theor Biol 5:443–469
Buskey EJ (1998) Energetic cost of swarming behavior for the copepod Dioithona oculata. Mar Biol 130:425–431
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton
Christensen-Dalsgaard KK, Fenchel T (2003) Increased filtration efficiency of attached compared to free-swimming flagellates. Aquat Microb Ecol 33:77–86
Davis CS, Alatalo P (1992) Effects of constant and intermittent food supply on life-history parameters in a marine copepod. Limnol Oceanogr 37:1618–1639
Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610
Doall MH, Colin SP, Strickler JR, Yen J (1998) Locating a mate in 3D: the case of Temora longicornis. Phil Trans R Soc B 353:681–689
Fenchel T, Jonsson PR (1988) The functional biology of Strombidium sulcatum, a marine oligotrich ciliate (ciliophora, oligotrichina). Mar Ecol Prog Ser 48:1–15
Frost BW, Bollens SM (1992) Variability of diel vertical migration in the marine planktonic copepod Pseudocalanus newmani in relation to its predators. Can J Fish Aquat Sci 49:1137–1141
Gerritsen J (1980) Sex and parthenogenesis in sparse populations. Am Nat 115:718–742
Hedenström A, Alerstam T (1993) Optimal flight speed of birds. Phil Trans R Soc B 348:471–487
Hedenström A, Alerstam T (1996) Skylark optimal flight speeds for flying nowhere and somewhere. Beh Ecol 7:121–126
Hirst AG, Kiørboe T (2002) Mortality of marine planktonic copepods: global rates and patterns. Mar Ecol Prog Ser 230:195–209
Hopkins CCE (1982) The breeding biology of Euchaete norvegica (Boeck) (Copepoda, Calanoida) in Loch Etive, Scotland – assessment of breeding intensity in terms of seasonal cycles in the sex-ratio, spermatophore attachement, and egg-sac production. J Exp Mar Biol Ecol 60:91–102
Ianora A, Poulet SA (1993) Egg viability in the copepod Termora stylifera. Liminol Oceanogr 38:1615–1638
Ikeda T, KannoY, Ozaki K, Shinada A (2001) Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Mar Biol 139:587–596
Johansen JE, Pinhassi J, Blackburn N et al. (2002) Variability in motility characteristics among marine bacteria. Aquat Microb Ecol 28:229–237
Kerfoot WC (1978) Combat between predatory copepods and their prey – Cyclops, Epischura, and Bosmina. Limnol Oceanogr 23:1089–1102
Kiørboe T (2006) Sex, sex-ratios, and the dynamics of pelagic copepod populations. Oecologia 148:40–50
Kiørboe T (2007) Mate finding, mating, and population dynamics in a planktonic copepod Oithona davisae: there are too few males. Limnol Oceanogr 52:1511–1522
Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007
Kiørboe T, Møhlenberg F, Hamburger K (1985) Bioenergetics of the planktonic copepod Acartia tonsa: relation between feeding, egg production and respiration, and the composition of specific dynamic action. Mar Ecol Prog Ser 26:85–95
Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philo Trans R Soc B 361:1615–1638
Kokko H, Wong BBM (2007) What determines sex roles in mate searching? Evolution 61:1162–1175
Loose CJ, Dawidowicz P (1994) Trade-offs in diel vertical migration by zooplankton—the cost of predator avoidance. Ecology 75:2255–2263
Mauchline J (1998) The biology of calanoid copepods. Adv Mar Biol 33:1–710
Menden-Deuer S, Grünbaum D (2006) Individual foraging behaviors and population distributions of a planktonic predator aggregating to phytoplankton thin layers. Limnol Oceanogr 51:109–116
Mengl L, Orsi JJ (1991) Selective predation by larval striped bass on native and introduced copepods. Trans Am Fish Soc 120:187–192
Morris MJ, Gust G, Torres JJ (1985) Propulsion efficiency and cost of transport for copepods: a hydromechanical model of crustacean swimming. Mar Biol 86:283–295
Nesbitt BF, Beevor PS, Cole RA, Lester R, Poppi RG (1973) Pheromones of 2 noctuid moths. Nat New Biol 244:208–209
Nihongi A, Lovern SB, Strickler JR (2004) Mate-searching behaviors in the freshwater calanoid copepod Leptodiaptomus ashlandi. J Mar Syst 49:65–74
Norberg Å (1981) Optimal flight speed in young birds when feeding young. J Anim Ecol 50:473–477
Ohman MD, Wood SN (1996) Mortality estimation for planktonic copepods: Pseudocalanus newmani in a temperate fjord. Limnol Oceanogr 41:126–135
Ohtsuka S, Huys R (2001) Sexual dimorphism in calanoid copepods: morphology and function. Hydrobiologia 453/454:441–466
Olsson M, Madsen T, Shine R (1997) Is sperm realy so cheap? Costs of reproduction in male adders, Vipera berus. Proc R Soc Lond Ser B 264:455–459
Ruxton GD, Bailey DM (2005) Searching speeds and energetic feasibility of an obligate whale-scavenging fish. Deep Sea Res Part I 52:1536–1541
Saiz E, Calbet A, Broglio E (2003) Effects of small-scale turbulence on copepods: the case of Oithona davisae. Limnol Oceanogr 48:1304–1311
Salonen K, Sarvala J, Hakala I, Viljanen MI (1976) The relation of energy and organic carbon in aquatic invertebrates. Limnol Oceanogr 21:724–730
Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect. Oikos 87:185–190
Strathmann RR, Grünbaum D (2006) Good eaters, poor swimmers: compromises in larval form. Int Comp Biol 46:312–322
Strickler JR (1982) Calanoid copepods, feeding currents, and the role of gravity. Science 218:158–160
Strickler JR (1998) Observing free-swimming copepods mating. Phil Trans R Soc B 353:671–680
Svensson M (1996) Sexual selection in moths: the role of chemical communication. Biol Rev 71:113–135
Svetlichny LS, Hubareva ES (2005) The energetics of Calanus euxinus: locomotion, filtration of food and specific dynamic action. J Plankton Res 27:671–682
Tiselius P (1992) Behavior of Acartia tonsa in patchy food environments. Limnol Oceanogr 8:1640–1651
Tiselius P, Jonsson PR (1990) Foraging behaviour of 6 Calanoid copepods – observations and hydrodynamic analysis. Mar Ecol Prog Ser 66:23–33
Tiselius P, Jonsson PR, Kaartved S, Olsen EM, Jørstad T (1997) Effects of copepod foraging behavior on predation risk: an experimental study of the predatory copepod Pareuchaeta norvegica feeding on Acartia clausi and A. tonsa (Copepoda). Limnol Oceanogr 42:164–170
Titelman J, Fiksen O (2004) Ontogenetic vertical distribution patterns in small copepods: field observations and model predictions. Mar Ecol Prog Ser 284:49–63
Titelman J, Kiørboe T (2003) Motility of copepod nauplii and implications for food encounter. Mar Ecol Prog Ser 247:123–135
Tsuda A, Miller CB (1998) Mate-finding behaviour in Calanus marshallae Frost. Philo Trans R Soc B 353:713–720
Uye S-I, Matsuda O (1988) Phosphorus content of zooplankton from the Inland Sea of Japan. J Oceanogr Soc Jpn 44:280–286
Uye S-I, Sano K (1995) Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Mar Ecol Prog Ser 118:121–128
Van Duren LAS, Videler JJ (1995) Swimming behavior of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar Ecol Prog Ser 126:153–161
Van Gool E, Ringelberg J (1998) Light-induced migration behaviour of Daphnia modified by food and predator kairomones. Anim Behav 56:741–747
Van Voorhies WA (1992) Production of sperm reduces nematode life-span. Nature 360:456–458
Visser AW, Kiørboe T (2006) Plankton motility patterns and encounter rates. Oecologia 148:538–546
Ware DM (1975) Growth, metabolism, and optimal swimming speed of a pelagic fish. J Fish Res Bd Can 32:33–41
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320
Yen J, Weissburg MJ, Doall MH (1998) The fluid physics of signal perception by mate-tracking copepods. Philo Trans R Soc Lond B 353:387–804
Acknowledgments
This study was supported by the Danish Natural Research Council and the Spanish Ministry of Education and Science. I thank Dr. Enric Saiz and the zooplankton ecology group at Institut de Ciencies del Mar, Barcelona for support and stimulating discussions, Juancho Movilla for technical assistance and Dr. Jordi Sole and Dr. Andy Visser for help with solving equations.
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Communicated by Ulrich Sommer.
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Kiørboe, T. Optimal swimming strategies in mate-searching pelagic copepods. Oecologia 155, 179–192 (2008). https://doi.org/10.1007/s00442-007-0893-x
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DOI: https://doi.org/10.1007/s00442-007-0893-x