Periodic gonadal activity and protracted mating in elasmobranch fishes
Abstract
Temporal patterns of gonad development are determined by environmental cues that regulate hormonal cycles and ultimately affect a population's mating system. Annual periodicity of gonad histology is essentially unknown for the more than 450 species of batoid elasmobranchs. Temporal periodicity in spermatogenic activity and ova production in the Atlantic stingray (Dasyatis sabina) were examined by histology over a consecutive 20 month period. Gonadosomatic index (GSI) shows three distinct phases associated with structural changes at the cellular level. Testes in the inactive phase occur from March through July, have a low GSI, and are represented only by germinal (SI) and early spermatocyst (SII) stages. The enlargement phase begins in mid-August, followed by rapid testicular growth that peaks in October. Testicular recrudescence is characterized by a decline in the proportion of early stage spermatocysts (SI, II) and a sequential maturation of cells to the spermatocyte (SIII), spermatid (SIV), immature sperm (SV), and mature spermatozoa (SVI) stages. The measure of absolute spermatogenic production (ASP) is maximum from about August through January. The diminution phase is characterized by a decrease in male GSI from October through April associated with a reduced tissue biomass and predominance of early spermatogenic stages. The annual succession of peaks in sperm formation indicates continuous spermatogenesis through the fall-winter and shows that peak sperm production lags maximum GSI by approximately 3-4 months. Further, seminal vesicle diameter peaks in February, which also lags maximum GSI by 4 months. Egg growth in females is a periodic process of 5-6 months duration that involves vitellogenesis of 2-4 oocytes. Maximum ova diameter increases after mid-September, peaks in March (x̄ = 10.62 mm), and covaries with the increase in female GSI. Despite the brief period of ovulation and fertilization in March-April, fresh mating scars and sperm in the lower reproductive tract of females confirm a protracted mating period from October through April-May. Thus, mating begins in the population at least 7 months prior to ovulation and fertilization. Current evidence indicates this protracted mating period is not explained by female sperm storage or arrested embryonic development. We suggest the protracted mating period serves some currently undetermined function such as induction of steroidogenesis, oocyte growth, or ovulation in females.