Prolonged Alteration of Neonate Traits Following Maternal Exposure to Fishing-Capture Stress During Late Pregnancy in a Chondrichthyan Species

Abstract

For animals discarded after fishing capture (unwanted bycatch), the effects of fishing-capture stress can extend beyond immediate or delayed death, causing long-term, sub-lethal effects such as injuries and physiological, behavioral, immune, energetic, and reproductive consequences. Given the importance of successful reproduction for population recruitment, investigating reproductive impairment is essential, even more so for animals with low reproductive rates such as chondrichthyans. However, data for these species are lacking, even though the poor conservation status of many chondrichthyan populations and the threats from overexploitation and discard require a better understanding of fishing-capture stress consequences. In this study, we investigated the reproductive consequences of trawling and air exposure stress when experienced by southern fiddler rays (Trygonorrhina dumerilii) during late pregnancy, with a focus on neonatal traits. Compared with neonates from unstressed mothers, neonates born from mothers subjected to capture simulation had significantly lower body mass and yolk sac volume at birth, showed a granulocyte-to-lymphocyte ratio indicative of a stressed condition, reduced growth, altered burying behavior, reduced boldness, and swam for shorter distances after a simulated predator attack. Smaller size and lower growth rate might expose neonates to a higher rate of predation, and similarly, the altered burying and swimming behaviors may reduce their ability to escape from predators. Decreased boldness could impact neonate survival by reducing their ability to compete and obtain food and resources. Further investigations are needed, but these initial results suggest that capture stress suffered by pregnant rays may alter traits and survival of their offspring with consequences for recruitment and population abundance.

Influence of female reproductive state and of fishing‐capture stress on the oxygen uptake rate of a viviparous elasmobranch

“…Similarly, it is unlikely the Ṁ O 2 decline originated from the fact the animals habituated to the respirometer and were less stressed on their second respirometry trial. Indeed, elephant fish, Callorhinchus milii , does not show habituation to the respirometer over three Ṁ O 2 measurement trials (Finotto, 2021). Additionally, spending up to 3 h in a respirometry chamber does not elicit a significant stress response in C. melanopterus (Bouyoucos et al, 2018), which is even a more sensitive species than T. dumerilii (Dapp et al, 2015).…”

“…Moreover, a reduced investment in maintenance of pregnancy might reduce the quality of the uterine environment due to the accumulation of toxic metabolites produced by the embryos that the mother cannot remove (Hamlett et al, 2005; Thibault & Schultz, 1978; Webb & Brett, 1972). We did not investigate recovery, but metabolic decline persisted for up to 24 h after osmotic stress in M. antarcticus and school sharks ( Galeorhinus galeus ; Morash et al, 2016; Tunnah et al, 2016) and up to 7 days after capture stress in C. milii (Finotto, 2021). Given the rapid development of T. dumerilii embryos (Marshall et al, 2007), even short‐term maternal energetic disruptions potentially severely impact embryonic development.…”

“…However, a fecundity estimates was available for each female from the ultrasound performed at collection. Additionally, neonate TL at birth is positively correlated with maternal size and siblings have similar coloration patterns (Finotto et al, 2021). Based on these variables, we are confident that all neonates were assigned to the correct mother.…”

“…Indeed, induced premature parturition is commonly reported (Adams et al, 2018) and when pregnant southern fiddler rays ( Trygonorrhina dumerilli ) experienced trawling simulation, both neonatal and maternal consequences were detected (Finotto et al, 2021; Guida et al, 2017). The neonates had reduced body size and internal‐residual yolk sac, altered behaviors, and a stressed physiological condition (indicated by higher values of the granulocyte to lymphocyte ratio; Van Rijn & Reina, 2010); moreover, compared to unstressed animals, stressed females had a larger decrease in body mass postpartum (Finotto et al, 2021; Guida et al, 2017). These observations seem to indicate that capture might affect females' body condition and/or energy allocation to pregnancy.…”

Ecological vulnerability of the chondrichthyan fauna of southern Australia to the stressors of climate change, fishing and other anthropogenic hazards

“…There is also evidence of impairment of reproductive vitality in pregnant animals after escape or release following fishing‐capture stress (Guida et al., 2017), which is likely to affect the reproductive output. Furthermore, the effects of capture stress can be intergenerational or transgenerational (Finotto et al., 2021).…”