Artificial light at night disrupts male dominance relationships and reproductive success in a model fish species

被引:3
作者
Closs, Lauren E. [1 ]
Royan, Muhammad Rahmad [1 ]
Sayyari, Amin [2 ]
Mayer, Ian [2 ]
Weltzien, Finn-Arne [1 ]
Baker, Dianne M. [3 ]
Fontaine, Romain [2 ]
机构
[1] Norwegian Univ Life Sci, Fac Vet Med, Dept Preclin Sci & Pathol, As, Norway
[2] Norwegian Univ Life Sci, Fac Vet Med, Dept Prod Anim Clin Sci, As, Norway
[3] Univ Mary Washington, Dept Biol Sci, Fredericksburg, VA USA
关键词
Dominant; Pituitary; Sperm; Behavior; ALAN; Steroids; ATLANTIC SALMON; SPECTRAL COMPOSITION; CELL-PROLIFERATION; SEXUAL SELECTION; PLASMA-CORTISOL; DIEL CHANGES; LONG-TERM; MEDAKA; BEHAVIOR; STRESS;
D O I
10.1016/j.scitotenv.2023.166406
中图分类号
X [环境科学、安全科学];
学科分类号
08 ; 0830 ;
摘要
Environmental light is perceived and anticipated by organisms to synchronize their biological cycles. Therefore, artificial light at night (ALAN) disrupts both diurnal and seasonal biological rhythms. Reproduction is a complex physiological process involving integration of environmental signals by the brain, and release of endocrine signals by the pituitary that regulate gametogenesis and spawning. In addition, males from many species form a dominance hierarchy that, through a combination of aggressive and protective behavior, influences their reproductive success. In this study, we investigated the effect of ALAN and continuous daylight on the behavior and fitness of male fish within a dominance hierarchy using a model fish, the Japanese medaka. In normal light/ dark cycles, male medaka establish a hierarchy with the dominant males being more aggressive and remaining closer to the female thus limiting the access of subordinate males to females during spawning. However, determination of the paternity of the progeny revealed that even though subordinate males spend less time with the females, they are, in normal light conditions, equally successful at producing progeny due to an efficient sneaking behavior. Continuous daylight completely inhibited the establishment of male hierarchy, whereas ALAN did not affect it. Nonetheless, when exposed to ALAN, subordinate males fertilize far fewer eggs. Furthermore, we found that when exposed to ALAN, subordinate males produced lower quality sperm than dominant males. Surprisingly, we found no differences in circulating sex steroid levels, pituitary gonadotropin levels, or gonadosomatic index between dominant and subordinate males, neither in control nor ALAN condition. This study is the first to report an effect of ALAN on sperm quality leading to a modification of male fertilization success in any vertebrate. While this work was performed in a model fish species, our results suggest that in urban areas ALAN may impact the genetic diversity of species displaying dominance behavior.
引用
收藏
页数:15
相关论文
共 98 条
  • [51] Plasticity of the Reproductive Axis Caused by Social Status Change in an African Cichlid Fish: II. Testicular Gene Expression and Spermatogenesis
    Maruska, Karen P.
    Fernald, Russell D.
    [J]. ENDOCRINOLOGY, 2011, 152 (01) : 291 - 302
  • [52] Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species
    Migaud, H.
    Davie, A.
    Taylor, J. F.
    [J]. JOURNAL OF FISH BIOLOGY, 2010, 76 (01) : 27 - 68
  • [53] The effect of spectral composition and light intensity on melatonin, stress and retinal damage in post-smolt Atlantic salmon, Salmo salar
    Migaud, Herve
    Cowan, Mairi
    Taylor, John
    Ferguson, Hugh W.
    [J]. AQUACULTURE, 2007, 270 (1-4) : 390 - 404
  • [54] Endocrine control of sexual behavior in teleost fish
    Munakata, Arimune
    Kobayashi, Makito
    [J]. GENERAL AND COMPARATIVE ENDOCRINOLOGY, 2010, 165 (03) : 456 - 468
  • [55] High Reproductive Success Despite Queuing - Socio-Sexual Development of Males in a Complex Social Environment
    Mutwill, Alexandra M.
    Zimmermann, Tobias D.
    Reuland, Charel
    Fuchs, Sebastian
    Kunert, Joachim
    Richter, S. Helene
    Kaiser, Sylvia
    Sachser, Norbert
    [J]. FRONTIERS IN PSYCHOLOGY, 2019, 10
  • [56] The dark side of light at night: physiological, epidemiological, and ecological consequences
    Navara, Kristen J.
    Nelson, Randy J.
    [J]. JOURNAL OF PINEAL RESEARCH, 2007, 43 (03) : 215 - 224
  • [57] Reproductive success in wild and hatchery male coho salmon
    Neff, Bryan D.
    Garner, Shawn R.
    Fleming, Ian A.
    Gross, Mart R.
    [J]. ROYAL SOCIETY OPEN SCIENCE, 2015, 2 (08):
  • [58] Using novel methodologies to examine the impact of artificial light at night on the cortisol stress response in dispersing Atlantic salmon (Salmo salar L.) fry
    Newman, Rhian C.
    Ellis, Tim
    Davison, Phil I.
    Ives, Mark J.
    Thomas, Rob J.
    Griffiths, Sian W.
    Riley, William D.
    [J]. CONSERVATION PHYSIOLOGY, 2015, 3
  • [59] Live fast, die young: Behavioural and physiological impacts of light pollution on a marine fish during larval recruitment
    O'Connor, J. J.
    Fobert, E. K.
    Besson, M.
    Jacob, H.
    Lecchini, D.
    [J]. MARINE POLLUTION BULLETIN, 2019, 146 : 908 - 914
  • [60] Ono Y., 1957, Journal of the Faculty of Science Hokkaido University Zoology, V13, P197