Aerobic and anaerobic poise of white swimming muscles of the deep-diving scalloped hammerhead shark: comparison to sympatric coastal and deep-water species

Scalloped hammerhead sharks ( Sphyrna lewini ) routinely perform rapid dives to forage on mesopelagic prey. These deep dives consist of intensive swimming followed by recovery periods in the surface mixed layer. Swimming muscle temperature profiles suggest that S. lewini suppresses gill function as a means to reduce convective heat loss during dives into cool water. Such intensive swimming behavior coupled with reduced respiration prompted us to test whether the aerobic and anaerobic metabolic capacities of the white swimming muscle tissue of this species are greater than those of other shark species from the same region. The activities of key enzymes used in aerobic and anaerobic metabolism provide an indirect indicator of the metabolic potential (“poise”) of a tissue. Here we measured the maximal activities [international units (µmol substrate converted to product per min, U) per gram of wet tissue mass at 10°C] of the citric acid cycle enzymes citrate synthase (CS) and malate dehydrogenase (MDH) and glycolytic enzymes pyruvate kinase (PK) and lactate dehydrogenase (LDH) from white swimming muscle of S. lewini . Enzyme activities, and ratios of these enzyme activities that indicate relative indexes of aerobic to anaerobic capacity, were compared to those measured in three sympatric coastal carcharhinid sharks and two deep-dwelling species, Echinorhinus cookei and Hexanchus griseus . This is the first report of swimming-muscle enzyme activity for these deep-dwelling species. In comparison to the other species, S. lewini had significantly higher activities of both LDH and MDH in the white muscle, and a higher MDH/CS ratio. The high LDH activities suggest that the white muscle of S. lewini relies on relatively high rates of anaerobic ATP production, with would result in build up of high lactate levels, during deep foraging dives. High MDH activity in S. lewini white muscle suggests the potential for lactate levels to be rapidly reduced when aerobic conditions are restored while in the surface mixed layer between dives. These biochemical characteristics may enable S. lewini to swim rapidly while suppressing gill function during deep dives and thereby exploit a very different ecological niche from sympatric shark species (e.g., coastal carcharhinids) and hunt more rapidly via faster swimming for deep-water prey compared to species that permanently inhabit deep depths.

Authors

Institutions

Publication Details

Journal
Frontiers in Marine Science
Published
2024-11-11
DOI
https://doi.org/10.3389/fmars.2024.1477553
Citations
1
Primary Topic
Ichthyology and Marine Biology
Type
article
Field-Weighted Citation Impact
0.69

Funders

Controls
|||
ALL TIME
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
article

Aerobic and anaerobic poise of white swimming muscles of the deep-diving scalloped hammerhead shark: comparison to sympatric coastal and deep-water species

Kim N. Holland, Kevin C. Weng, D. Cardenas Garcia, Kathryn A. Dickson et al.
1 citations
Frontiers in Marine Science
Ichthyology and Marine Biology
0.69
article

Aerobic and anaerobic poise of white swimming muscles of the deep-diving scalloped hammerhead shark: comparison to sympatric coastal and deep-water species

Kim N. Holland, Kevin C. Weng, D. Cardenas Garcia, Kathryn A. Dickson, Jeffrey C. Drazen, M Royer, Carl G. Meyer
article en
1 citations

Abstract

Scalloped hammerhead sharks ( Sphyrna lewini ) routinely perform rapid dives to forage on mesopelagic prey. These deep dives consist of intensive swimming followed by recovery periods in the surface mixed layer. Swimming muscle temperature profiles suggest that S. lewini suppresses gill function as a means to reduce convective heat loss during dives into cool water. Such intensive swimming behavior coupled with reduced respiration prompted us to test whether the aerobic and anaerobic metabolic capacities of the white swimming muscle tissue of this species are greater than those of other shark species from the same region. The activities of key enzymes used in aerobic and anaerobic metabolism provide an indirect indicator of the metabolic potential (“poise”) of a tissue. Here we measured the maximal activities [international units (µmol substrate converted to product per min, U) per gram of wet tissue mass at 10°C] of the citric acid cycle enzymes citrate synthase (CS) and malate dehydrogenase (MDH) and glycolytic enzymes pyruvate kinase (PK) and lactate dehydrogenase (LDH) from white swimming muscle of S. lewini . Enzyme activities, and ratios of these enzyme activities that indicate relative indexes of aerobic to anaerobic capacity, were compared to those measured in three sympatric coastal carcharhinid sharks and two deep-dwelling species, Echinorhinus cookei and Hexanchus griseus . This is the first report of swimming-muscle enzyme activity for these deep-dwelling species. In comparison to the other species, S. lewini had significantly higher activities of both LDH and MDH in the white muscle, and a higher MDH/CS ratio. The high LDH activities suggest that the white muscle of S. lewini relies on relatively high rates of anaerobic ATP production, with would result in build up of high lactate levels, during deep foraging dives. High MDH activity in S. lewini white muscle suggests the potential for lactate levels to be rapidly reduced when aerobic conditions are restored while in the surface mixed layer between dives. These biochemical characteristics may enable S. lewini to swim rapidly while suppressing gill function during deep dives and thereby exploit a very different ecological niche from sympatric shark species (e.g., coastal carcharhinids) and hunt more rapidly via faster swimming for deep-water prey compared to species that permanently inhabit deep depths.

Frontiers in Marine ScienceVol. 11
University of Hawaiʻi at Mānoa (US), U.S. National Science Foundation (US), California State University, Fullerton (US), William & Mary (US)
National Science Foundation, U.S. Department of Energy, National Oceanic and Atmospheric Administration, Wind and Water Power Program
Life below water
Openalex Percentile: Top 25%
Ichthyology and Marine Biology
0.69
AI Navigator

Ask Laika to Summarize, Analyze, and Connect papers live on the map.

Summarize Papers & Methodologies

Extract key findings, datasets, and comparative methods across publications.

Benchmark Rankings & Visual Analytics

Rank top research institutions, authors, funders, topics, and journals by Field-Weighted Citation Impact (FWCI) and paper volume with instant charts.

Connect Distant Disciplines

Bridge topological clusters on the map to find hidden collaborative intersections.