Influence of starvation on the critical swimming behaviour of the Senegalese sole (Solea senegalensis) and its relationship with RNA/DNA ratios during ontogeny

Authors

  • Ana M. Faria Eco-Ethology Research Unit, Instituto Superior de Psicologia Aplicada - Centre of Marine Sciences, University of Algarve
  • Teja Muha University of Ljubljana, Biotehnical faculty
  • Elvira Morote Institut de Ciències del Mar (CSIC)
  • M. Alexandra Chícharo Centre of Marine Sciences, University of Algarve

DOI:

https://doi.org/10.3989/scimar.2011.75n1087

Keywords:

Senegalese sole, Solea senegalensis, feeding treatment, starvation, RNA/DNA ratio, critical swimming speed, Ucrit, ontogeny

Abstract


Food availability can affect larval survival directly through starvation and indirectly through the effects on larval growth rate, swimming performance and vulnerability to predators. In the present study we evaluate the effects of starvation on growth, nutritional condition and swimming behaviour of the Senegalese sole (Solea senegalensis) throughout ontogeny (8 to 14 days after hatching). Biochemical analysis (RNA/DNA ratios) and behavioural experiments (critical swimming speed, Ucrit) were conducted on larvae reared under 3 feeding treatments: fed ad libitum, deprived of food for 48 hours and deprived of food for 96 hours. Growth was significantly affected by feeding treatment, while only slight decreases in RNA/DNA ratio and swimming performance were registered. Late stage larvae of the three feeding treatments had slower critical speeds than the pre-flexion and flexion stages, which is probably related to the benthic lifestyle acquired by the species at the end of the larval period. These physiological and behavioural changes are in accordance with previous results, which show that flatfish larvae are more resistant to starvation than pelagic species and that they become less active later in development.

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References

Armsworth, P.R. – 2001. Directed Motion in the Sea: Efficient Swimming by Reef Fish Larvae. J. Theor. Biol., 210: 81-91. doi:10.1006/jtbi.2001.2299 PMid:11343432

Bailey, K.M. – 1984. Comparison of laboratory rates of predation on five species of marine fish larvae by three planktonic invertebrates; effect of larval size on vulnerability. Mar. Biol., 79(Suppl. 3): 303-309. doi:10.1007/BF00393262

Bailey, K.M. and E.D. Houde. – 1989. Predation on eggs and larvae of marine fishes and the recruitment problem. Adv. Mar. Biol., 25: 1-83. doi:10.1016/S0065-2881(08)60187-X

Bentle, L.A., S. Dutta and J. Metcoff. – 1981. The sequential enzymatic determination of DNA and RNA. Anal Biochem., 116: 5-16. doi:10.1016/0003-2697(81)90314-6

Bergeron, J.-P. – 1982. L’aspartate transcarbamylase, indice de croissance des organismes marins: perspectives et Limites. Publs. Cent. natn. Exploit. Oceans (CNEXO) (Ser Act. Colloques) 14: 177-19.

Billerbeck, J.M., T.E. Lankford Jr. and D.O. Conover. – 2001. Evolution of intrinsic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution, 55(9): 1873-1881. PMid:11681742

Blaxter, J.H.S. – 1986. Development of sense organs and behaviour of teleost larvae with special reference to feeding and predator avoidance. Trans. Am. Fish. Soc., 115: 98-115.

Blaxter, J.H.S. and G. Hempel. – 1963. The influence of egg size on herring larvae (Clupea harengus L.). J. Cons. int. Explor Mer, 28: 211-240.

Blaxter, J.H.S. and M.E. Staines. – 1971. Food searching potential in marine fish larvae. In: D.J. Crisp (ed.), Proceedings 4th European Marine Biology Symposium, pp. 467-481. Cambridge University Press, Cambridge,

Booman, C.I., A. Folkvord and J.R. Hunter. – 1991. Responsiveness of starved northern anchovy Engraulis mordax larvae to predatory attacks by adult anchovy. Fish. Bull. (U.S.), 89(Suppl. 4): 707-711.

Brett, J.R. – 1964. The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Board. Can., 21: 1183-1226.

Buckley, L.J, E. Caldarone and T.-L. Ong. – 1999. RNA–DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia, 401: 265-277. doi:10.1023/A:1003798613241

Buckley, L.J., S.I. Turner, T.A. Halavik, A.S. Smigielski, S.M. Drew and G.C. Laurence. – 1984. Effects of temperature and food availability on growth, survival and RNA-DNA ratio of larval sand lance (Ammodytes americanus). Mar. Ecol. Prog. Ser., 15: 91-97. doi:10.3354/meps015091

Caldarone, E.M., M. Wagner, J.S. Onge-Burnes and L.J. Buckley. – 2001. Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Ref Doc 01-11, Northeast Fisheries Science Center, Woods Hole, MA.

Caldarone, E.M., J.M. St. Onge-Burns and L.J. Buckley. – 2003. Relationship of RNA/DNA ratio and temperature to growth in larvae of Atlantic cod Gadus morhua. Mar. Ecol. Prog. Ser., 262: 229-240. doi:10.3354/meps262229

Caldarone, E.M., C.M. Clemmesen, E. Berdalet, T. Miller, A. Folkvord, G.J. Holt, M.P. Olivar and I.M. Suthers. – 2006. Inter-calibration of four spectro-fluorometric protocols for measuring RNA/DNA ratios in larval and juvenile fish. Limnol. Oceanogr. Methods, 4: 153-163.

Chick, J.H. and M.J. Van den Avyle. – 2000. Effects of feeding ration on larval swimming speed and responsiveness to predator attacks: implications for cohort survival. Can. J. Fish. Aquat. Sci., 57: 106-115. doi:10.1139/cjfas-57-1-106

Clark, D.L., J.M. Leis, A.C. Hay and T. Trnski. – 2005. Swimming ontogeny of larvae of four temperate marine fishes. Mar. Ecol. Prog. Ser., 292: 287-300. doi:10.3354/meps292287

Chícharo, M.A. – 1997. Starvation percentages in field caught Sardina pilchardus larvae off southern Portugal. Sci. Mar. 61 (4): 507-516.

Chicharo, M.A., E. Esteves, A.M.P. Santos, A. dos Santos, A. Peliz and P. Ré. – 2003. Are sardine larvae caught off northern Portugal in winter starving? An approach examining nutritional conditions. Mar. Ecol. Prog. Ser., 257: 303-309. doi:10.3354/meps257303

Clemmesen, C.M. – 1987. Laboratory studies on RNA/DNA ratios of starved and fed herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae. J. Cons. int. Explor. Mer, 43: 122-128.

Clemmesen, C.M. – 1994. The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar. Biol., 118: 377-382. doi:10.1007/BF00350294

Clemmesen, C.M., R. Sanchez, C. Wongtschowski. – 1997. A regional comparison of the nutritional condition of SW Atlantic anchovy larvae, Engraulis anchoita, based on RNA/DNA contents. Arch. Fish. Mar. Res., 45: 17-43.

Cushing, D.H. – 1975. The natural mortality of the plaice. J. Cons. Int. Explor. Mer. 36 (Suppl. 2): 150-157.

Dudley, B., N. Tolimieri, J. Montgomery. – 2000. Swimming ability of the larvae of some reef fishes from New Zealand waters. Mar. Fresh. Res. 51: 783-787. doi:10.1071/MF00062

Faria, A., A. Ojanguren, L.A. Fuiman and E.J. Gonçalves. – 2009. Ontogeny of Critical Swimming speed of wild-caught and laboratory- reared larvae of red Drum (Scieanops ocellatus). Mar. Ecol. Prog. Ser., 384: 221-230. doi:10.3354/meps08018

Fisher, R., D.R. Bellwood and S.D. Job. – 2000. Development of swimming abilities in reef fish larvae. Mar. Ecol. Prog. Ser., 202: 163-173. doi:10.3354/meps202163

Fisher, R., J.M. Leis, D.L. Clark and S.K. Wilson. – 2005. Critical swimming speeds of late-stage coral reef fish larvae: Variation within species, among species and between locations. Mar. Biol., 147: 1201-1212. doi:10.1007/s00227-005-0001-x

Fuiman, L.A. and D.R. Ottey. – 1993. Temperature effects on spontaneous behaviour of larval and juvenile red drum Sciaenops ocellatus, and implications for foraging. Fish. Bull., 91: 23-35.

Fuiman, L.A. and R.S. Batty. – 1997. What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. J. Exp. Biol., 200: 1745-1755. PMid:9319652

Gadomski, D.M. and J.H. Petersen. – 1988. Effects of food deprivation on the larvae of two flatfishes. Mar. Ecol. Prog. Ser., 44: 103-111. doi:10.3354/meps044103

Grorud-Colvert, K. and S. Sponaugle. – 2006. Influence of condition on behaviour and survival potential of a newly settled coral reef fish, the bluehead wrasse Thalassoma bifasciatum. Mar. Ecol. Prog. Ser., 327: 279-288. doi:10.3354/meps327279

Gwak, W.S. and M. Tanaka. – 2001. Developmental changes in RNA/DNA ratios of fed and starved laboratory-reared Japanese flounder larvae and juveniles, and its application to assessment of nutritional condition for wild fish. J. Fish Biol., 59: 902-915.

Kamler, E., M. Szlamiñska, A. Przybyl, B. Barska, M. Jakubas, M. Kuczyñski and K. Raciborsku. – 1990. Developmental response of carp, Cyprinus carpio, larvae fed different foods or starved. Environ. Biol. Fishes, 29: 303-313. doi:10.1007/BF00001187

Lasker, R., H.M. Feder, G.H. Theilacker and R.C. May. – 1970. Feeding, growth, and survival of Engraulis rnordax larvae reared in the laboratory. Mar. Biol., 5: 345-353.

Laurence, G. – 1972. Comparative swimming abilities of fed and starved larval largemouth bass (Micropterus salmoides). J. Fish. Biol., 4: 73-78. doi:10.1111/j.1095-8649.1972.tb05654.x

Leis, J.M. – 2006. Are larvae of demersal fishes plankton or nekton? Adv. Mar. Biol., 51: 59-141. doi:10.1016/S0065-2881(06)51002-8

Leis, J.M. and R. Fisher. – 2006. Swimming speed of settlement-stage reef-fish larvae measured in the laboratory and in the field: A comparison of critical speed and in situ speed. Proc. 10th Int. Coral Reef Symp., Okinawa: 438-445.

Leis, J.M., A.C. Hay and T. Trnski. – 2006a. In situ ontogeny of behaviour in pelagic larvae of three temperate, marine, demersal fishes. Mar. Biol., 148: 655-669. doi:10.1007/s00227-005-0108-0

Leis, J.M., A.C. Hay, D.A. Clark, I.S. Chen and K.T. Shao. – 2006b. Behavioural ontogeny in larvae and early juveniles of the giant trevally, Caranx ignobilis (Pisces: Carangidae). Fish. Bull., 104: 401-414.

Leis, J.M., A.C. Hay, M.M. Lockett, J.-P. Chen and L.-S. Fang. – 2007. Ontogeny of swimming speed in larvae of pelagic-spawning, tropical, marine fishes. Mar. Ecol. Prog. Ser., 349: 255-267. doi:10.3354/meps07107

Leis, J.M., A.C. Hay and G.J. Howarth. – 2009a. Ontogeny of in situ behaviours relevant to dispersal and population connectivity in larvae of coral-reef fishes. Mar. Ecol. Prog. Ser., 379: 163-179. doi:10.3354/meps07904

Leis, J.M., R.F. Piola, A.C. Hay, C. Wen and K.-P. Kan. – 2009b. Ontogeny of behaviour relevant to dispersal and connectivity in the larvae of two non-reef demersal, tropical fish species. Mar. Fresh. Res., 60: 211-223. doi:10.1071/MF08186

Miller, T.J., L.B. Crowder, J.A. Rice and E.A. Marschall. – 1988. Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can. J. Fish. Aquat. Sci., 45: 1657-1688. doi:10.1139/f88-197

Neilson, J.D., R.I. Perry, P.F. Valerio and K.G. Waiwood. – 1986. Condition of Atlantic cod Gadus morhua larvae after the transition to exogenous feeding: morphometrics, buoyancy and predator avoidance. Mar. Ecol. Prog. Ser., 32(2-3): 229-235. doi:10.3354/meps032229

Olivar, M.P., M. Diaz and M.A. Chicharo. – 2009. Tissue effect on RNA/DNA ratios of marine fish larvae. Sci. Mar., 73S1: 171-182.

Plaut, I. – 2001. Critical swimming speed: its ecological relevance. Comp. Biochem. Physiol. A. Comp. Physiol., 131: 41-50. doi:10.1016/S1095-6433(01)00462-7

Reidy, S.P., S.R. Kerr and J.A. Nelson. – 2000. Aerobic and anaerobic swimming performance of individual Atlantic cod. J. Exp. Biol., 203: 347-357. PMid:10607544

Richard, P., J.-P. Bergeron, M. Boulhic, R. Galois and J. Person-Le Ruyet. – 1991. Effect of starvation on RNA, DNA and protein content of laboratory-reared larvae and juveniles of Solea solea. Mar. Ecol. Prog. Ser., 72: 69-77. doi:10.3354/meps072069

Rooker, J.R. and G.J. Holt. – 1996. Application of RNA/DNA ratios to evaluate the condition and growth of larval and juvenile red drum (Sciaenops ocellatus). Mar. Fresh. Res., 47: 283-290. doi:10.1071/MF9960283

Searcy, S. and S. Sponaugle. – 2001. Selective Mortality during the larval-juvenile transition in two coral reef fishes. Ecology, 82: 2452-2470.

Shepherd, J.G. and D.H. Cushing. – 1980. A mechanism for density- dependent survival of larval fish as the basis of a stock–recruitment relationship. J. Cons. Int. Explor. Mer., 39(Suppl. 2): 160-167.

Skajaa, K. and H.I. Browman. – 2007. The escape response of food-deprived cod larvae (Gadus morhua L.). J. Exp. Mar. Biol. Ecol., 353: 135-144. doi:10.1016/j.jembe.2007.01.014

Sogard, S.M. and B.L. Olla. – 1996. Food deprivation affects vertical distribution and activity of a marine fish in a thermal gradient: potential energy-conserving mechanism. Mar. Ecol. Prog. Ser., 133: 43-55. doi:10.3354/meps133043

Sponaugle, S., K. Grorud-Colvert and D. Pinkard. – 2006. Temperature-mediated variation in early life history traits and recruitment success of the coral reef fish Thalassoma bifasciatum in the Florida Keys. Mar. Ecol. Prog. Ser., 308: 1-15. doi:10.3354/meps308001

Stobutzki, I.C. – 1998. Interspecific variation in sustained swimming ability of late pelagic stage reef fish from two families (Pomacentridae and Chaetodontidae). Coral Reefs, 17, 111-119. doi:10.1007/s003380050104

Stobutzki, I.C. and D.R. Bellwood. – 1994. An analysis of the sustained swimming abilities of pre- and post-settlement coral reef fishes. J. Exp. Mar. Biol. Ecol., 175: 275-286. doi:10.1016/0022-0981(94)90031-0

Stobutzki, I.C. and D.R. Bellwood. – 1997. Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar. Ecol. Prog. Ser., 149: 35-41. doi:10.3354/meps149035

Wagner, M.M., E.G. Durbin and L.J. Buckley. – 1998. RNA/DNA ratios as indicators of nutritional condition in the copepod Calanus finmarchicus. Mar. Ecol. Prog. Ser., 162: 173-181. doi:10.3354/meps162173

Yin, M.C. and J.H.S. Blaxter. – 1986. Morphological changes during growth and starvation of larval cod (Gadus morhua L.) and flounder (Platichthys flesus L.). J. Exp. Mar. Biol. Ecol., 104(1-3): 215-228. doi:10.1016/0022-0981(86)90106-1

Yin, M.C. and J.H.S. Blaxter. – 1987. Escape speeds of marine fish larvae during early development and starvation. Mar. Biol., 96: 459-468. doi:10.1007/BF00397963

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Published

2011-03-30

How to Cite

1.
Faria AM, Muha T, Morote E, Chícharo MA. Influence of starvation on the critical swimming behaviour of the Senegalese sole (Solea senegalensis) and its relationship with RNA/DNA ratios during ontogeny. Sci. mar. [Internet]. 2011Mar.30 [cited 2024Mar.29];75(1):87-94. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1230

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