The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Rahman, Md Moshiur ^a   Turchini, Giovanni M ^b   Gasparini, Clelia ^a   Norambuena, Fernando ^b   Evans, Jonathan P ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

OMEGA 3 FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; COPULATION; COURTSHIP; DIET SUPPLEMENTATION; FOOD COMPOSITION; GUPPY; LIFE HISTORY TRAIT; MALE; NONHUMAN; SEXUAL BEHAVIOR; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TESTIS; ANALYSIS OF VARIANCE; ANIMAL; COLOR; DIET; DRUG EFFECTS; FEMALE; PHYSIOLOGY; PIGMENTATION; POECILIA; SPERMATOZOON; SWIMMING; TIME;

ANALYSIS OF VARIANCE; ANIMALS; COLOR; DIET; FATTY ACIDS, OMEGA-3; FEMALE; MALE; PIGMENTATION; POECILIA; SEXUAL BEHAVIOR, ANIMAL; SPERM MOTILITY; SPERMATOZOA; SWIMMING; TIME FACTORS;

EID: 84928010095     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105856     Document Type: Article

References (121)

1. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16: 254-260. (Pubitemid 32288153)
2. Krause ET, Naguib M (2014) Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata). Evol Ecol 28: 263-275.
3. Hylander S, Grenvald JC, Kiorboe T (2014) Fitness costs and benefits of ultraviolet radiation exposure in marine pelagic copepods. Funct Ecol 28: 149-158.
4. Archambault JM, Cope WG, Kwak TJ (2014) Survival and behaviour of juvenile unionid mussels exposed to thermal stress and dewatering in the presence of a sediment temperature gradient. Freshwat Biol 59: 601-613.
5. Hastings RP, Bauman JM, Baker EA, Scribner KT (2013) Post-hatch dispersal of lake sturgeon (Acipenser fulvescens, Rafinesque, 1817) yolk-sac larvae in relation to substrate in an artificial stream. J Appl Ichthyol 29: 1208-1213.
6. Luszczek-Trojnar E, Drag-Kozak E, Szczerbik P, Socha M, Popek W (2014) Effect of long-term dietary lead exposure on some maturation and reproductive parameters of a female Prussian carp (Carassius gibelio B.). Environ Sci Pollut Res 21: 2465-2478.
7. Wang H, Zhu XW, Wang HZ, Qiang J, Xu P, et al. (2014) Joint effect of temperature, salinity and pH on the percentage fertilization and hatching of Nile tilapia (Oreochromis niloticus) . Aquacult Res 45: 259-269.
8. Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68: 203-220.
9. Boland MP, Lonergan P, O'Callaghan D (2001) Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55: 1323-1340. (Pubitemid 32327974)
10. Pike TW, Blount JD, Lindstroem J, Metcalfe NB (2010) Dietary carotenoid availability, sexual signalling and functional fertility in sticklebacks. Biol Lett 6: 191-193.
11. Gage MJG, Cook PA (1994) Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera: Pyralidea). Funct Ecol 8: 594-599. (Pubitemid 2147243)
12. Lewis Z, Sasaki H, Miyatake T (2011) Sex starved: do resource-limited males ensure fertilization success at the expense of precopulatory mating success? Anim Behav 81: 579-583.
13. Zahavi A (1975) Mate selection - selection for a handicap. J Theor Biol 53: 205-214.
14. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16: R755-R765. (Pubitemid 44691806)
15. Iwasa Y, Pomiankowski A (1999) Good parent and good genes models of handicap evolution. J Theor Biol 200: 97-109. (Pubitemid 29481594)
16. Hooper RE, Tsubaki Y, Siva-Jothy MT (1999) Expression of a costly, plastic secondary sexual trait is correlated with age and condition in a damselfly with two male morphs. Physiol Entomol 24: 364-369.
17. Cotton S, Fowler K, Pomiankowski A (2004) Condition dependence of sexual ornament size and variation in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera : Diopsidae). Evolution 58: 1038-1046. (Pubitemid 38673791)
18. Devigili A, Kelley JL, Pilastro A, Evans JP (2013) Expression of pre- and postcopulatory traits under different dietary conditions in guppies. Behav Ecol 24: 740-749.
19. Rahman MM, Kelley JL, Evans JP (2013) Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecol Evol 3: 2197-2213.
20. Jennions MD, Backwell PRY (1998) Variation in courtship rate in the fiddler crab Uca annulipes: is it related to male attractiveness? Behav Ecol 9: 605-611. (Pubitemid 28554083)
21. Kotiaho JS (2000) Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol 48: 188-194.
22. Engqvist L, Sauer KP (2003) Influence of nutrition on courtship and mating in the scorpionfly Panorpa cognata (Mecoptera, insecta). Ethology 109: 911-928. (Pubitemid 37488887)
23. Cerolini S, Mantovani C, Bellagamba F, Mangiagalli MG, Cavalchini LG, et al. (1995) Effect of restricted and ad-libitum feeding on semen production and fertility in broiler breeder males. Brit Poultry Sci 36: 677-682.
24. Selvaraju S, Sivasubramani T, Raghavendra BS, Raju P, Rao SBN, et al. (2012) Effect of dietary energy on seminal plasma insulin-like growth factor-I (IGF-I), serum IGF-I and testosterone levels, semen quality and fertility in adult rams. Theriogenology 78: 646-655.
25. Gasparini C, Devigili A, Dosselli R, Pilastro A (2013) Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits. Ecol Evol 3: 4940-4953.
26. Ward PI, Simmons LW (1991) Copula duration and testes size in the yellow dung fly, Scathophaga stercoraria (L.): the effects of diet, body size, and mating history. Behav Ecol Sociobiol 29: 77-85.
27. Parker GA (1970) Sperm competition and its evolutionary effect on copula duration in fly Scatophaga stercoraria. J Insect Physiol 16: 1301-1328.
28. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton.
29. Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122: 765-788.
30. Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271: 771-783. (Pubitemid 38491262)
31. Yasui Y (1997) A "good-sperm" model can explain the evolution of costly multiple mating by females. Am Nat 149: 573-584.
32. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75: 21-64. (Pubitemid 30135849)
33. Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry: An introduction. 5th edition Blackwell Science Ltd, Oxford.
34. Kishimoto Y, Agranoff BW, Radin NS, Burton RM (1969) Comparison of the fatty acids of lipids of subcellular brain fractions. J Neurochem 16: 397-404.
35. Carlson SE, Werkman SH, Tolley EA (1996) Effect of long-chain n-3 fatty acid supplementation on visual acuity and growth of preterm infants with and without bronchopulmonary dysplasia. Am J Clin Nutr 63: 687-697. (Pubitemid 26126586)
36. Watts JL, Phillips E, Griffing KR, Browse J (2003) Deficiencies in C20 polyunsaturated fatty acids cause behavioral and developmental defects in Caenorhabditis elegans fat-3 mutants. Genetics 163: 581-589. (Pubitemid 36314541)
37. Enslen M, Milon H, Malnoë A (1991) Effect of low intake of n-3 fatty acids during development on brain phospholipid fatty acid composition and exploratory behavior in rats. Lipids 26: 203-208.
38. de Wilde MC, Hogyes E, Kiliaan AJ, Farkas T, Luiten PGM, et al. (2003) Dietary fatty acids alter blood pressure, behavior and brain membrane composition of hypertensive rats. Brain Res 988: 9-19. (Pubitemid 37304014)
39. Wathes DC, Abayasekara DRE, Aitken RJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77: 190-201. (Pubitemid 47173600)
40. Surai PF, Blesbois E, Grasseau I, Chalah T, Brillard JP, et al. (1998) Fatty acid composition, glutathione peroxidase and superoxide dismutase activity and total antioxidant activity of avian semen. Comp Biochem Phys B 120: 527-533. (Pubitemid 28386765)
41. Poulos A, Sharp P, D J, White I, Fellenberg A (1986) The occurrence of polyenoic fatty acids with greater than 22 carbon atoms in mammalian spermatozoa. Biochem J 240: 891-895. (Pubitemid 17010012)
42. Lenzi A, Picardo M, Gandini L, Dondero F (1996) Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum Reprod Update 2: 246-256. (Pubitemid 26355413)
43. Izquierdo MS, Fernández-Palacios H, Tacon AGJ (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197: 25-42. (Pubitemid 32442664)
44. Grubert MA, Dunstan GA, Ritar AJ (2004) Lipid and fatty acid composition of pre- and post-spawning blacklip (Haliotis rubra) and greenlip (Haliotis laevigata) abalone conditioned at two temperatures on a formulated feed. Aquaculture 242: 297-311. (Pubitemid 39584100)
45. Hazel JR (1995) Thermal adaptation in biological-membranes - is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19-42.
46. Stubbs CD, Smith AD (1984) The modification of mammalian polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779: 89-137. (Pubitemid 14199577)
47. Connor WE, Lin DS, Wolf DP, Alexander M (1998) Uneven distribution of desmosterol and docosahexaenoic acid in the heads and tails of monkey sperm. J Lipid Res 39: 1404-1411. (Pubitemid 28332474)
48. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton, NJ.
49. Karino K, Haijima Y (2004) Algal-diet enhances sexual ornament, growth and reproduction in the guppy. Behaviour 141: 585-601. (Pubitemid 38946970)
50. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16: 294-300. (Pubitemid 40112975)
51. Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25: 393-401.
52. Grether GF (2000) Carotenoid limitation and mate preference evolution: A test of the indicator hypothesis in guppies (Poecilia reticulata) . Evolution 54: 1712-1724.
53. Kolluru GR, Grether GF, Dunlop E, South SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behav Ecol 20: 131-137.
54. Rick IP, Mehlis M, Esser E, Bakker TCM (2014) The influence of ambient ultraviolet light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Oecologia 174: 393-402.
55. Simmons LW (2012) Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus. Behav Ecol 23: 168-173.
56. Anderson JT, Wagner MR, Rushworth CA, Prasad K, Mitchell-Olds T (2014) The evolution of quantitative traits in complex environments. Heredity 112: 4-12.
57. Harpaz S, Slosman T, Segev R (2005) Effect of feeding guppy fish fry (Poecilia reticulata) diets in the form of powder versus flakes. Aquacult Res 36: 996-1000. (Pubitemid 41009353)
58. Brown TD, Francis DS, Turchini GM (2010) Can dietary lipid source circadian alternation improve omega-3 deposition in rainbow trout? Aquaculture 300: 148-155.
59. Bozynski CC, Liley NR (2003) The effect of female presence on spermiation, and of male sexual activity on 'ready' sperm in the male guppy. Anim Behav 65: 53-58. (Pubitemid 36198777)
60. Gasparini C, Peretti AV, Pilastro A (2009) Female presence influences sperm velocity in the guppy. Biol Lett 5: 792-794.
61. Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55: 1002-1015. (Pubitemid 32550568)
62. Nicoletto PF (1993) Female sexual-response to condition-dependent ornaments in the guppy, Poecilia reticulata. Anim Behav 46: 441-450.
63. Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153: 183-200. (Pubitemid 29139435)
64. Gardiner DM (1978) Utilization of extracellular glucose by spermatozoa of two viviparous fishes. Comparative Biochemistry and Physiology Part A: Physiology 59: 165-168.
65. Matthews IM, Evans JP, Magurran AE (1997) Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proc R Soc Lond B 264: 695-700.
66. Wilson-Leedy JG, Ingermann RL (2007) Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67: 661-672. (Pubitemid 46026865)
67. Billard R, Cosson MP (1990) The energetics of fish sperm motility. Controls of sperm motility: biological and clinical aspects (eds C. Gagnon), pp. 153-173. CRC Press Inc., Florida.
68. Evans JP (2009) No evidence for sperm priming responses under varying sperm competition risk or intensity in guppies. Naturwissenschaften 96: 771-779.
69. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
70. Norambuena F, Lewis M, Hamid NKA, Hermon K, Donald JA, et al. (2013) Fish oil replacement in current aquaculture feed: is cholesterol a hidden treasure for fish nutrition? Plos One 8: 1-9.
71. R Development Core Team (2014) R: a language and environment for statistical computing, version 3.1.0. R Foundation for Statistical Computing, Vienna, Austria. Available: http://cran.r-project.org/. Accessed 2014 Aug 4.
72. Langsrud Ø (2003) ANOVA for unbalanced data: Use Type II instead of Type III sums of squares. Stat Comput 13: 163-167.
73. Kemp DJ, Reznick DN, Grether GF, Endler JA (2009) Predicting the direction of ornament evolution in Trinidadian guppies (Poecilia reticulata). Proc R Soc Lond B 276: 4335-4343.
74. Ritschard M, Brumm H (2012) Zebra finch song reflects current food availability. Evol Ecol 26: 801-812.
75. Blay S, Yuval B (1997) Nutritional correlates of reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Anim Behav 54: 59-66. (Pubitemid 27309129)
76. Schatral A (1993) Diet influences male-female interactions in the bushcricket Requena verticalis (Orthoptera: Tettigoniidae). J Insect Behav 6: 379-388.
77. van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, et al. (2003) Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol 16: 273-281. (Pubitemid 36261058)
78. Head ML, Wong BBM, Brooks R (2010) Sexual display and mate choice in an energetically costly environment. Plos One 5: e15279.
79. Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. Journal of Avian Biolology 31: 559-566.
80. Tibbetts EA (2010) The condition dependence and heritability of signaling and nonsignaling color traits in paper wasps. Am Nat 175: 495-503.
81. Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263: 1415-1421.
82. Gilchrist BM, Green J (1960) The Pigments of Artemia. Proc R Soc Lond B 152: 118-136.
83. Krinsky NI (1965) The carotenoids of the brine shrimp, Artemia salina. Comp Biochem Physiol 16: 181-187.
84. Yonekura L, Nagao A (2007) Intestinal absorption of dietary carotenoids. Mol Nutr Food Res 51: 107-115. (Pubitemid 46144766)
85. Lakshminarayana R, Baskaran V (2013) Influence of olive oil on the bioavailability of carotenoids. Eur J Lipid Sci Technol 115: 1085-1093.
86. Prince MR, Frisoli JK (1993) Beta-carotene accumulation in serum and skin. Am J Clin Nutr 57: 175-181. (Pubitemid 23039888)
87. Parker RS (1996) Carotenoids .4. Absorption, metabolism, and transport of carotenoids. FASEB J 10: 542-551.
88. Erdman JW, Bierer TL, Gugger ET (1993) Absorption and transport of carotenoids. Ann N Y Acad Sci 691: 76-85. (Pubitemid 24099382)
89. San-Jose LM, Granado-Lorencio F, Fitze PS (2012) Dietary lipids reduce the expression of carotenoid-based coloration in Lacerta vivipara. Funct Ecol 26: 646-656.
90. Martin GB, Walkden-Brown SW (1995) Nutritional influences on reproduction in mature male sheep and goats. J Rep Fer S 49: 437-449.
91. Schillo KK (1992) Effects of dietary energy on control of luteinizing hormone secretion in cattle and sheep. J Anim Sci 70: 1271-1282.
92. Dunn TG, Moss GE (1992) Effects of nutrient deficiencies and excesses on reproductive efficiency of livestock. J Anim Sci 70: 1580-1593.
93. Al-Daraji HJ, Al-Mashadani HA, Al-Hayani WK, Al-Hassani AS, Mirza HA (2010) Effect of n-3 and n-6 fatty acid supplemented diets on semen quality in Japanese quail (Coturnix coturnix japonica). Int J Poult Sci 9: 656-663.
94. Robbins WA, Xun L, FitzGerald LZ, Esguerra S, Henning SM, et al. (2012) Walnuts improve semen quality in men consuming a western-style diet: randomized control dietary intervention trial. Biol Reprod 87: 1-8.
95. Simmons LW, Kotiaho JS (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56: 1622-1631.
96. Perry JC, Rowe L (2010) Condition-dependent ejaculate size and composition in a ladybird beetle. Proc R Soc Lond B 277: 3639-3647.
97. Rogers-Bennett L, Dondanville RF, Moore JD, Vilchis LI (2010) Response of red abalone reproduction to warm water, starvation, and disease stressors: implications of ocean warming. J Shellfish Res 29: 599-611.
98. Parker GV, Thwaites CJ (1972) Effects of undernutrition on libido and semen quality in adult merino rams. Aust J Agric Res 23: 109-115.
99. Sexton KJ, Renden JA, Marple DN, Kemppainen RJ (1989) Effects of adlibitum and restricted feeding on semen quantity and quality, bodycomposition, and blood-chemistry of caged broiler breeder males. Poultry Sci 68: 569-576.
100. Buckner RE, Renden JA, Savage TF (1986) The effect of feeding programs on reproductive traits and selected blood chemistries of caged broiler breeder males. Poultry Sci 65: 85-91.
101. Estienne MJ, Harper AF, Crawford RJ (2008) Dietary supplementation with a source of omega-3 fatty acids increases sperm number and the duration of ejaculation in boars. Theriogenology 70: 70-76.
102. Dolatpanah MB, Towhidi A, Farshad A, Rashidi A, Rezayazdi A (2008) Effects of dietary fish oil on semen quality of goats. Asian Austral J Anim Sci 21: 29-34. (Pubitemid 351353880)
103. Harlioglu MM, Koprucu K, Harlioglu AG, Yonar SM, Duran TC, et al. (2013) Effect of dietary n-3 series fatty acids on sperm production in the freshwater crayfish, Astacus leptodactylus (Eschscholtz) (Astacidae). Aquacult Int 21: 273-282.
104. Pilastro A, Bisazza A (1999) Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc R Soc Lond B 266: 1887-1891. (Pubitemid 29457072)
105. Pitcher TE, Evans JP (2001) Male phenotype and sperm number in the guppy (Poecilia reticulata). Can J Zool 79: 1891-1896. (Pubitemid 34004280)
106. Skinner AMJ, Watt PJ (2007) Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata. Behav Ecol 18: 47-52. (Pubitemid 46026311)
107. Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64: 1634-1643.
108. Rooke JA, Shao CC, Speake BK (2001) Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 121: 315-322. (Pubitemid 32175554)
109. Castenmiller JJM, West CE (1998) Bioavailability and bioconversion of carotenoids. Annu Rev Nutr 18: 19-38. (Pubitemid 28366859)
110. Maldjian A, Pizzi F, Gliozzi T, Cerolini S, Penny P, et al. (2005) Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology 63: 411-421. (Pubitemid 40033965)
111. Samadian F, Towhidi A, Rezayazdi K, Bahreini M (2010) Effects of dietary n-3 fatty acids on characteristics and lipid composition of ovine sperm. Animal 4: 2017-2022.
112. Surai PF, Cerolini S, Speake BK (2000) Effect of supplementing the diet of male chickens with oils rich in n-6 polyunsaturated fatty acids on the fatty acid profiles of the testis and liver. Asian Austral J Anim Sci 13: 1518-1522.
113. Vassallo-Agius R, Watanabe T, Yoshizaki G, Satoh S, Takeuchi Y (2001) Quality of eggs and spermatozoa of rainbow trout fed an n-3 essential fatty acid-deficient diet and its effects on the lipid and fatty acid components of eggs, semen and livers. Fish Sci 67: 818-827. (Pubitemid 33593597)
114. Castellano CA, Audet I, Bailey JL, Chouinard PY, Laforest JP, et al. (2010) Effect of dietary n-3 fatty acids (fish oils) on boar reproduction and semen quality. J Anim Sci 88: 2346-2355.
115. Cerolini S, Pizzi F, Gliozzi T, Maldjiani A, Zaniboni L, et al. (2003) Lipid manipulation of chicken semen by dietary means and its relation to fertility: a review. World Poultry Sci J 59: 65-75. (Pubitemid 36562325)
116. Yan L, Bai X-l, Fang Z-f, Che L-q, Xu S-y, et al. (2013) Effect of different dietary omega-3/omega-6 fatty acid ratios on reproduction in male rats. Lipids Health Dis 12: 1-9.
117. Henrotte E, Kaspar V, Rodina M, Psenicka M, Linhart O, et al. (2010) Dietary n-3/n-6 ratio affects the biochemical composition of Eurasian perch (Perca fluviatilis) semen but not indicators of sperm quality. Aquacult Res 41: 31-38.
118. Scabini V, Fernandez-Palacios H, Robaina L, Kalinowski T, Izquierdo MS (2011) Reproductive performance of gilthead seabream (Sparus aurata L., 1758) fed two combined levels of carotenoids from paprika oleoresin and essential fatty acids. Aquacult Nutr 17: 304-312.
119. Lahnsteiner F, Mansour N, Caberlotto S (2010) Composition and metabolism of carbohydrates and lipids in Sparus aurata semen and its relation to viability expressed as sperm motility when activated. Comp Biochem Phys B 157: 39-45.
120. Azeddine A, Ali AA, Kamal C, Houda A, Mohamed I (2010) Effect of diet (fatty acid and protein) content during spawning season on fertility, eggs and larvae quality of common porgy (Pagrus pagrus, Linnaeus 1758). Agric Biol J North Am 1: 175-184.
121. Yue D, Yan L, Luo H, Xu X, Jin X (2010) Effect of Vitamin E supplementation on semen quality and the testicular cell membranal and mitochondrial antioxidant abilities in Aohan fine-wool sheep. Anim Reprod Sci 118: 217-222.