Metabolic responses of adult lion\u2019s paw scallops Nodipecten subnodosus exposed to acute hyperthermia in relation to seasonal reproductive effort

Rosa L Salgado-García,Ilie S Racotta,Alma R Rivera-Camacho,Marcial Arellano-Martínez,Claudia I Maytorena-Verdugo,M Teresa Sicard,Edouard Kraffe

doi:10.1038/s41598-020-59242-6

Abstract

In marine ectotherms, reproduction is an energetically expensive process that affects their thermal window tolerance. For most species, the impacts of hyperthermia during gametogenesis have still not been addressed. Our aim was to assess the metabolic response of adult Nodipecten subnodosus scallops to thermal challenges at early development (spring) and advanced gonad maturation (summer). Scallops collected in both seasons were exposed to acute hyperthermia (26 and 30 °C, 24 h), maintaining a group of scallops at acclimation temperature (22 °C) as a control condition. During the summer, relatively low activity of hexokinase (HK), as well as low levels of ATP and GTP were found in the adductor muscle, suggesting a shift in energy investment for reproduction, although arginine phosphate (ArgP) levels were higher in summer scallops. Hyperthermia (30 °C) induced an increased energy expenditure reflected by a transitory enhanced oxygen consumption (VO2) and relatively high activities of HK and arginine kinase (AK). Moreover, a slight decrease in adenylic energy charge (AEC) was partially compensated by a decrease in ArgP. An increase in nucleotide by-products inosine monophosphate (IMP) and hypoxanthine (HX) indicated a thermal stress at 30 °C. Some of the responses to acute hyperthermia were more pronounced at advanced maturation stages (summer scallops), indicating a possible lack of energy balance, with possible implications in animals challenged to global warming scenario.

Highlights

In marine ectotherms, reproduction is an energetically expensive process that affects their thermal window tolerance
An increase in gonad size (GSI, gonadal mass index (GMI)) and more advanced gonadal development were identified in summer scallops, in accordance with previous studies analysing reproduction of N. subnodosus at Magdalena Bay and in the Ojo de Liebre Lagoon on the Baja California Peninsula[27,37]
Additional studies are needed to explore the direct seasonal influence in field scallops and the effects of acclimation to laboratory conditions such as being fed ad libitum and constant temperature. These results support the hypothesis that N. subnodosus scallops display a seasonal pattern in energy metabolism related to gonad maturation

Summary

Introduction

Reproduction is an energetically expensive process that affects their thermal window tolerance. Our aim was to assess the metabolic response of adult Nodipecten subnodosus scallops to thermal challenges at early development (spring) and advanced gonad maturation (summer). Scallops collected in both seasons were exposed to acute hyperthermia (26 and 30 °C, 24 h), maintaining a group of scallops at acclimation temperature (22 °C) as a control condition. Summer mortality events occur when the temperature approaches the critical thermal limit of a species, mainly affecting mature and post spawning animals, in which any increase in energy demand may lead to metabolic stress[18]. Thermal tolerance of juvenile lion’s paw scallops have been determined, with a lethal temperature of 32 °C26, but no studies on the effects of high temperature in combination with a related biological trait, such as reproductive effort, on adult scallops exist

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