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Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels

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Abstract
During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels' bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.
Keywords
eel, maternal transfer, bone loss, metals, spawning migration, EUROPEAN EEL, ENERGY-METABOLISM, CALCIUM, FISH, TELEOST, CADMIUM, EGGS, IMPAIRMENT, ROSTRATA, SKELETON

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MLA
Freese, Marko et al. “Bone Resorption and Body Reorganization During Maturation Induce Maternal Transfer of Toxic Metals in Anguillid Eels.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116.23 (2019): 11339–11344. Print.
APA
Freese, M., Rizzo, L. Y., Pohlmann, J.-D., Marohn, L., Witten, P., Gremse, F., Rütten, S., et al. (2019). Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(23), 11339–11344.
Chicago author-date
Freese, Marko, Larissa Yokota Rizzo, Jan-Dag Pohlmann, Lasse Marohn, Paul Witten, Felix Gremse, Stephan Rütten, et al. 2019. “Bone Resorption and Body Reorganization During Maturation Induce Maternal Transfer of Toxic Metals in Anguillid Eels.” Proceedings of the National Academy of Sciences of the United States of America 116 (23): 11339–11344.
Chicago author-date (all authors)
Freese, Marko, Larissa Yokota Rizzo, Jan-Dag Pohlmann, Lasse Marohn, Paul Witten, Felix Gremse, Stephan Rütten, Nihan Güvener, Sabrina Michael, Klaus Wysujack, Twan Lammers, Fabian Kiessling, Henner Hollert, Reinhold Hanel, and Markus Brinkmann. 2019. “Bone Resorption and Body Reorganization During Maturation Induce Maternal Transfer of Toxic Metals in Anguillid Eels.” Proceedings of the National Academy of Sciences of the United States of America 116 (23): 11339–11344.
Vancouver
1.
Freese M, Rizzo LY, Pohlmann J-D, Marohn L, Witten P, Gremse F, et al. Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2019;116(23):11339–44.
IEEE
[1]
M. Freese et al., “Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 23, pp. 11339–11344, 2019.
@article{8619419,
  abstract     = {{During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels' bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.}},
  author       = {{Freese, Marko and Rizzo, Larissa Yokota and Pohlmann, Jan-Dag and Marohn, Lasse and Witten, Paul and Gremse, Felix and Rütten, Stephan and Güvener, Nihan and Michael, Sabrina and Wysujack, Klaus and Lammers, Twan and Kiessling, Fabian and Hollert, Henner and Hanel, Reinhold and Brinkmann, Markus}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{eel,maternal transfer,bone loss,metals,spawning migration,EUROPEAN EEL,ENERGY-METABOLISM,CALCIUM,FISH,TELEOST,CADMIUM,EGGS,IMPAIRMENT,ROSTRATA,SKELETON}},
  language     = {{eng}},
  number       = {{23}},
  pages        = {{11339--11344}},
  title        = {{Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels}},
  url          = {{http://dx.doi.org/10.1073/pnas.1817738116}},
  volume       = {{116}},
  year         = {{2019}},
}

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