Testosterone and semen seasonality for the sand tiger shark Carcharias taurus†

Abstract

Understanding the fundamental reproductive biology of a species is the first step toward identifying parameters that are critical for reproduction and for the development of assisted reproductive techniques. Ejaculates were collected from aquarium (n = 24) and in situ (n = 34) sand tiger sharks Carcharias taurus. Volume, pH, osmolarity, sperm concentration, motility, status, morphology, and plasma membrane integrity were assessed for each ejaculate. Semen with the highest proportion of motile sperm was collected between April and June for both in situ and aquarium sand tiger sharks indicating a seasonal reproductive cycle. Overall, 17 of 30 semen samples collected from aquarium sharks from April through June contained motile sperm compared to 29 of 29 of in situ sharks, demonstrating semen quality differences between aquarium and in situ sharks. Sperm motility, status, morphology, and plasma membrane integrity were significantly higher (P < 0.05) for in situ compared to aquarium sand tiger sharks. Testosterone was measured by an enzyme immunoassay validated for the species. Testosterone concentration was seasonal for both aquarium and in situ sharks with highest concentrations measured in spring and lowest in summer. In situ sharks had higher (P < 0.05) testosterone concentration in spring than aquarium sharks. This study demonstrated annual reproduction with spring seasonality for male sand tiger sharks through marked seasonal differences in testosterone and semen production. Lower testosterone and poorer semen quality was observed in aquarium sharks likely contributing to the species’ limited reproductive success in aquariums.

Steroid hormones and chondrichthyan reproduction: physiological functions, scientific research, and implications for conservation

“…Embryos of viviparous species could complete their development through a placental connection, ingestion of unfertilised oocytes or other embryos, yolk sac, or nutritional substances provided in histotrophic and embryotrophic species (Compagno, Dando & Fowler, 2005;Hamlett, 2011;Castro, Sato & Bodine, 2016;Nelson, Grande & Wilson, 2016). However, the number of studies is highly limited in certain groups, with few papers published for some reproductive modes such as oophagy (Carcharodon carcharias; Sulikowski, Williams & Domeier, 2012), embryotrophy (Galeocerdo cuvier; Sulikowski et al, 2016) and adelphophagy (Carcharias taurus; Henningsen et al, 2008;Wyffels et al, 2019).…”

“…3). Minimum and maximum number of specimens were 2-81 for males (Nozu et al, 2017;Wyffels et al, 2019) and 3-94 for females (Nozu et al, 2015;Mylniczenko et al, 2019). All papers with EIA/ELISA as the main analytical method mentioned the antibodies used and constitute 13.6% (n = 8) of the reviewed literature.…”

Reproductive cycle and fecundity of the bonnethead Sphyrna tiburo L. from the northwest Atlantic Ocean

“…Although the physiological significance of some hormones such as T and P 4 remains uncertain in female S. tiburo , a clear role for T in regulating spermatogenesis in males is well supported by results of the present study as well as past research on this species (Gelsleichter et al ., 2002; Manire & Rasmussen, 1997). In all of these cases, plasma T concentrations were shown to progressively increase in male S. tiburo during the period of spermatogenesis, a pattern that has also been observed in males from all other seasonally reproducing elasmobranch species in which circulating T levels have been examined to date ( e.g ., R. terraenovae , Hoffmayer et al ., 2010; H. sabinus , Snelson et al ., 1997; Tricas et al ., 2000; sand tiger shark Carcharias taurus Rafinesque 1810, Henningsen et al ., 2008; Wyffels et al ., 2020; U. halleri , Mull et al ., 2008). The expression of androgen receptor (AR) mRNA and/or presence of AR protein has been demonstrated in multiple cell types in the testis of male S. tiburo including premeiotic germ cells, hormone‐producing Leydig‐like interstitial cells, Sertoli cells in spermatocysts containing elongating spermatids, mature spermatozoa and peritubular myoid cells surrounding spermatocysts containing mature spermatozoa (Tyminski et al ., 2015).…”

Natural environmental conditions and collaborative efforts provide the secret to success for sand tiger shark Carcharias taurus reproduction in aquaria

“…The uterus was remarked to be flat or empty or to contain fluid, egg cases or young and the ovary was either small and quiescent or enlarged with vitellogenic follicles. For males, in May of 2018 and 2019 a semen sample was collected and evaluated using previously described methods (Wyffels et al, 2020). In May 2018, the inseminating male, E16060, had higher sperm concentration and better motility parameters than male E16056 (Table 4).…”