Pheromones and ovarian growth in the African catfish Clarias gariepinus

J.H. van Weerd

Research output: Thesisinternal PhD, WU

Abstract

<p>Pheromones are defined as 'substances which are secreted to the outside by an individual and received by a second individual of the same species, in which they release a specific reaction'. In teleost fish, pheromones play a role in a variety of social interactions. Sex pheromones are involved in reproduction of several teleosts species, including the African catfish <em>Clarias gariepinus.</em> They regulate spawning behavior and endocrine events leading to reproduction. Most, if not all reports in literature describing the action of sex pheromones in teleosts pertain to advanced phases of the reproductive cycle. In those phases, sex pheromones influence oocyte maturation and ovulation in females, and spermiation in males. Furthermore, they play a role in mediating attraction of prospective mates and in triggering spawning behavior and release of gametes. To date, all teleost sex pheromones identified are steroids and steroid glucuronides, derivatives of reproductive hormones, with the exception of prostaglandins. In <em>C.</em><em>gariepinus</em> the presence of males enhances ovarian growth in pubertal females under hatchery conditions and in wild-caught adult females kept in ponds. This phenomenon led to the assumption that sex pheromones are also involved in the early phases of the reproductive cycle of <em>C. gariepinus, i.e.</em> ovarian development and possibly also of the testes and seminal vesicles. Experiments described in the present thesis were carried out to validate this hypothesis, the rationale being that findings might be applied to other fish species which do not or rarely reach the stage of ovarian growth in captivity.<p>In juvenile <em>C. gariepinus,</em> males stimulate ovarian development of females. Chemical and tactile stimuli are relevant to the process, whereas the other cues investigated are not (visual, auditory, electric). Also in adult female <em>C. gariepinus</em> which had entered the stage of recrudescence, <em>i.e.</em> ovarian development after induced maturation, ovulation and stripping of eggs, is influenced by stimuli from males. Chemical cues in holding water are perceived by the sense of smell, since females deprived of their sense of smell (anosmia) do not respond. Metabolites which are known to negatively influence ovarian growth and which are inevitably present in holding water, do not affect the female response. Hence, the chemical cues are indeed pheromones, and their male origin is strongly suggested by the fact that female holding-water has no effect. Male tactile stimuli do not play a role in ovarian development of adult <em>C. gariepinus.</em> The importance of tactile stimuli, which may actually encompass a combination of signals of different types (gustatory, mechanical) may be different in pubertal and adult <em>C. gariepinus.</em><p>In pubertal female <em>C. gariepinus,</em> ovarian growth is parallelled by changes in plasma levels of estradiol-17β(the female sex steroid) and vitellogenin (the femalespecific precursor of yolk proteins) and is reflected in increases in diameter and relative proportion of vitellogenic oocytes within the ovary. The effects were less clear in adult females during recrudescence, presumably as a consequence of their short gonadal cycle. Male stimuli cause changes in levels of estradiol-17β, vitellogenin, and ovarian development, and temporal shifts in the pattern of vitellogenesis. These are most pronounced in pubertal <em>C.</em><em>gariepinus.</em> It seems likely, that male stimuli trigger these changes through the olfactory-brain-pituitarygonad axis. The effect of stimulation of ovarian development is seen in an increase in both the diameter and the relative proportion of exogenous vitellogenic: oocytes, indicating both an enhanced vitellogenesis and an increased recruitment of oocytes into the stage of vitellogenesis. Monitoring the effect of stimulation on the basis of the parameters mentioned above does not lead to earlier detection of actual stimulation than with the use of gonadosomatic: index or oocyte development. However, it may make sacrifice of fish unnecessary.<p>An experiment aiming at investigating the interaction between the sexes with respect to emission of stimuli was hampered by the fact that anosmia in males depressed development of testes and seminal vesicles. Nevertheless, the experiment indicated that not only male tactile and olfactory cues stimulate ovarian development, but that also male olfactory cues stimulate gonadal development of other males. Tactile stimuli from females do not influence, or perhaps even tend to curb gonadal development of males, suggesting the existence of a female inhibitory cue. The emission of 'female-directed' olfactory cues by males is not modified by females, but the emission of 'male-directed' olfactory cues is, suggesting two types of male olfactory cues, differentially influenced.<p>Several of the experiments suggest that the male gonad is involved, directly or indirectly, in the ovarian growth stimulating effect of holding water, since male, but not female holding water is effective. Extirpation of testes, seminal vesicles or both, however, did not abolish the effect of holding water. Still-circulating androgens in operated fish may have been effectively converted to pheromonal steroid glucuronides, leading to holding water concentrations above the detection threshold of females.<p>Holding water was analyzed by gas chromatography and mass spectrometry and was found to contain several of the steroids and steroid glucuronides known to act as pheromones in later stages of the reproductive cycle of <em>C.</em><em>gariepinus. This</em> holding water originated from a mixed-sex group of adult male and female <em>C.</em><em>gariepinus.</em> A provisional calculation learned that the concentration in holding water of the glucuronide of one steroid in particular, 5β-pregnane-3α,17α-diol-20-one, of presumed male origin, approached the detection threshold of the olfactory epithelium.<br/>It is concluded that in <em>C.</em><em>gariepinus,</em> pheromones of male origin stimulate ovarian development, through the olfactory-brain-pituitary-gonad axis. Emission of pheromones and gonadal development are modulated by interaction between the sexes. The question whether male pheromones are of gonadal origin could not be answered conclusively. Holding water with the capacity to stimulate ovarian development contains steroids and steroid glucuronides. The actual involvement in stimulation of ovarian development of these compounds, however, awaits experimental confirmation.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
Supervisors/Advisors
  • Huisman, E.A., Promotor
  • Goos, H.J.T., Promotor, External person
Award date21 Dec 1990
Place of PublicationS.l.
Publisher
Publication statusPublished - 1990

Keywords

  • Siluridae
  • reproduction
  • excretory system
  • reproductive organs
  • urogenital system
  • sexual behaviour
  • Clarias gariepinus

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