DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival

Abstract

Abstract Species with complex life cycles are susceptible to environmental stressors across life stages, but the carryover and latent effects between stages remain understudied. For species with biphasic life histories, such as pond‐breeding amphibians, delayed effects of aquatic conditions can influence terrestrial juveniles and adults directly or indirectly, usually mediated through fitness correlates such as body size. We collected adult southern toads ( Anaxyrus terrestris ) from 2 source populations—a natural reference wetland and a metal‐contaminated industrial wetland—and exposed their offspring to 2 aquatic stressors (a metal contaminant, copper [Cu], and a dragonfly predator cue) in outdoor mesocosms ( n  = 24). We then reared metamorphs in terraria for 5 mo to examine delayed effects of early life stage environmental conditions on juvenile performance, growth, and survival. Larval exposure to Cu, as well as having parents from a contaminated wetland, resulted in smaller size at metamorphosis—a response later negated by compensatory growth. Although Cu exposure and parental source did not affect larval survival, we observed latent effects of these stressors on juvenile survival, with elevated Cu conditions and metal‐contaminated parents reducing postmetamorphic survival. Parental source and larval Cu exposure affected performance at metamorphosis through carryover effects on body size but, 1more » mo later, latent effects of parental source and larval predator exposure directly (i.e., not via body size) influenced performance. The carryover and latent effects of parental source population and aquatic Cu level on postmetamorphic survival and juvenile performance highlight the importance of conducting studies across life stages and generations. Environ Toxicol Chem 2018;37:2660–2669. © 2018 SETAC« less

Authors:
ORCiD logo [1];  [1];  [1]
  1. Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL); Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Savannah River Ecology Laboratory (SREL), Aiken, SC (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1819197
Alternate Identifier(s):
OSTI ID: 1466081
Grant/Contract Number:  
FC09-07SR22506
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Toxicology and Chemistry
Additional Journal Information:
Journal Volume: 37; Journal Issue: 10; Journal ID: ISSN 0730-7268
Publisher:
SETAC
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Copper; Amphibians; Ecotoxicology; Latent; Carryover

Citation Formats

Rumrill, Caitlin T., Scott, David E., and Lance, Stacey L. Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival. United States: N. p., 2018. Web. doi:10.1002/etc.4228.
Rumrill, Caitlin T., Scott, David E., & Lance, Stacey L. Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival. United States. https://doi.org/10.1002/etc.4228
Rumrill, Caitlin T., Scott, David E., and Lance, Stacey L. Mon . "Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival". United States. https://doi.org/10.1002/etc.4228. https://www.osti.gov/servlets/purl/1819197.
@article{osti_1819197,
title = {Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival},
author = {Rumrill, Caitlin T. and Scott, David E. and Lance, Stacey L.},
abstractNote = {Abstract Species with complex life cycles are susceptible to environmental stressors across life stages, but the carryover and latent effects between stages remain understudied. For species with biphasic life histories, such as pond‐breeding amphibians, delayed effects of aquatic conditions can influence terrestrial juveniles and adults directly or indirectly, usually mediated through fitness correlates such as body size. We collected adult southern toads ( Anaxyrus terrestris ) from 2 source populations—a natural reference wetland and a metal‐contaminated industrial wetland—and exposed their offspring to 2 aquatic stressors (a metal contaminant, copper [Cu], and a dragonfly predator cue) in outdoor mesocosms ( n  = 24). We then reared metamorphs in terraria for 5 mo to examine delayed effects of early life stage environmental conditions on juvenile performance, growth, and survival. Larval exposure to Cu, as well as having parents from a contaminated wetland, resulted in smaller size at metamorphosis—a response later negated by compensatory growth. Although Cu exposure and parental source did not affect larval survival, we observed latent effects of these stressors on juvenile survival, with elevated Cu conditions and metal‐contaminated parents reducing postmetamorphic survival. Parental source and larval Cu exposure affected performance at metamorphosis through carryover effects on body size but, 1 mo later, latent effects of parental source and larval predator exposure directly (i.e., not via body size) influenced performance. The carryover and latent effects of parental source population and aquatic Cu level on postmetamorphic survival and juvenile performance highlight the importance of conducting studies across life stages and generations. Environ Toxicol Chem 2018;37:2660–2669. © 2018 SETAC},
doi = {10.1002/etc.4228},
journal = {Environmental Toxicology and Chemistry},
number = 10,
volume = 37,
place = {United States},
year = {Mon Jul 09 00:00:00 EDT 2018},
month = {Mon Jul 09 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The larval legacy: cascading effects of recruit phenotype on post-recruitment interactions
journal, November 2010


Density dependence in the terrestrial life history stage of two anurans
journal, July 2007


Larval amphibians learn to match antipredator response intensity to temporal patterns of risk
journal, June 2008

  • Ferrari, M. C. O.; Messier, F.; Chivers, D. P.
  • Behavioral Ecology, Vol. 19, Issue 5
  • DOI: 10.1093/beheco/arn056

Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival
journal, May 2007


Competition Among Immatures Affects Their Adult Fertility: Population Dynamics
journal, October 1985

  • Prout, Timothy; McChesney, Frances
  • The American Naturalist, Vol. 126, Issue 4
  • DOI: 10.1086/284436

Interactive and cumulative effects of multiple human stressors in marine systems
journal, December 2008


Reproduction, Embryonic Development, and Maternal Transfer of Contaminants in the Amphibian Gastrophryne carolinensis
journal, May 2006

  • Hopkins, William Alexander; DuRant, Sarah Elizabeth; Staub, Brandon Patrick
  • Environmental Health Perspectives, Vol. 114, Issue 5
  • DOI: 10.1289/ehp.8457

Carryover effects in amphibians: Are characteristics of the larval habitat needed to predict juvenile survival?
journal, September 2013

  • Earl, Julia E.; Semlitsch, Raymond D.
  • Ecological Applications, Vol. 23, Issue 6
  • DOI: 10.1890/12-1235.1

Adult Recruitment in Chorus Frogs: Effects of Size and Date at Metamorphosis
journal, April 1987


Do effects of mercury in larval amphibians persist after metamorphosis?
journal, August 2011


A Life‐History Perspective on Short‐ and Long‐Term Consequences of Compensatory Growth
journal, December 2005

  • Mangel, Marc; Munch, Stephan B.
  • The American Naturalist, Vol. 166, Issue 6
  • DOI: 10.1086/444439

Biological carryover effects: linking common concepts and mechanisms in ecology and evolution
journal, March 2014

  • O'Connor, Constance M.; Norris, D. Ryan; Crossin, Glenn T.
  • Ecosphere, Vol. 5, Issue 3
  • DOI: 10.1890/ES13-00388.1

Effects of Larval Density on Postmetamorphic Spadefoot Toads (Spea hammondii)
journal, February 2001

  • Morey, Steven; Reznick, David
  • Ecology, Vol. 82, Issue 2
  • DOI: 10.2307/2679876

Determinants of size at metamorphosis in an endangered amphibian and their projected effects on population stability
journal, November 2014

  • Searcy, Christopher A.; Snaas, Helen; Shaffer, H. Bradley
  • Oikos, Vol. 124, Issue 6
  • DOI: 10.1111/oik.01775

Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs
journal, July 2010


Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species
journal, September 2013

  • Hartmann, Aaron C.; Marhaver, Kristen L.; Chamberland, Valérie F.
  • Ecology, Vol. 94, Issue 9
  • DOI: 10.1890/13-0161.1

Field Evidence for a Cost of Behavioral Antipredator Response in a Larval Amphibian
journal, April 1992


Patterns of natural selection on size at metamorphosis in water frogs.
text, January 2003


Thrice as easy to catch! Copper and temperature modulate predator‐prey interactions in larval dragonflies and anurans
journal, April 2015

  • Hayden, Mairin T.; Reeves, Mari K.; Holyoak, Marcel
  • Ecosphere, Vol. 6, Issue 4
  • DOI: 10.1890/ES14-00461.1

Predicting the consequences of carry-over effects for migratory populations
journal, November 2005


Carry-over effects as drivers of fitness differences in animals: Carry-over effects in animal populations
journal, August 2010


Interactive effects of maternal and dietary mercury exposure have latent and lethal consequences for amphibian larvae
journal, April 2011

  • Bergeron, Christine M.; Hopkins, William A.; Todd, Brian D.
  • Environmental Science & Technology, Vol. 45, Issue 8
  • DOI: 10.1021/es104210a

Larval carry-over effects from ocean acidification persist in the natural environment
journal, September 2013

  • Hettinger, Annaliese; Sanford, Eric; Hill, Tessa M.
  • Global Change Biology
  • DOI: 10.1111/gcb.12307

A Sensory System at the Interface between Urban Stormwater Runoff and Salmon Survival
journal, April 2007

  • Sandahl, Jason F.; Baldwin, David H.; Jenkins, Jeffrey J.
  • Environmental Science & Technology, Vol. 41, Issue 8
  • DOI: 10.1021/es062287r

Movement ecology of amphibians: A missing component for understanding population declines
journal, January 2014


Patterns of Natural Selection on size at Metamorphosis in Water Frogs
journal, January 2003


What Is Missing in Amphibian Decline Research: Insights from Ecological Sensitivity Analysis
journal, June 2002


Interactions of an Insecticide with Larval Density and Predation in Experimental Amphibian Communities
journal, February 2001


Terrestrial Performance of Juvenile Frogs in Two Habitat Types after Chronic Larval Exposure to a Contaminant
journal, June 2011

  • James, Stacy M.; Semlitsch, Raymond D.
  • Journal of Herpetology, Vol. 45, Issue 2
  • DOI: 10.1670/10-032.1

Exposure to Suboptimal Temperatures during Metamorphosis Reveals a Critical Developmental Window in the Solitary Bee, Megachile rotundata
journal, September 2015

  • Bennett, Meghan M.; Cook, Keeley M.; Rinehart, Joseph P.
  • Physiological and Biochemical Zoology, Vol. 88, Issue 5
  • DOI: 10.1086/682024

EFFECTS OF LARVAL DENSITY ON POSTMETAMORPHIC SPADEFOOT TOADS ( SPEA HAMMONDII )
journal, February 2001


The Effect of Larval Density on Adult Demographic Traits in Ambystoma Opacum
journal, July 1994


The pattern of early growth trajectories affects adult breeding performance
journal, April 2012

  • Lee, Who-Seung; Monaghan, Pat; Metcalfe, Neil B.
  • Ecology, Vol. 93, Issue 4
  • DOI: 10.1890/11-0890.1

Effects of metal and predator stressors in larval southern toads (Anaxyrus terrestris)
journal, June 2016


Within- and among-population level differences in response to chronic copper exposure in southern toads, Anaxyrus terrestris
journal, June 2013


Patterns of Natural Selection on size at Metamorphosis in Water Frogs
journal, April 2003


Maternal Transfer of Contaminants and Reduced Reproductive Success of Southern Toads (Bufo [Anaxyrus] terrestris) Exposed to Coal Combustion Waste
journal, February 2013

  • Metts, Brian S.; Buhlmann, Kurt A.; Tuberville, Tracey D.
  • Environmental Science & Technology, Vol. 47, Issue 6
  • DOI: 10.1021/es303989u

Carryover Aquatic Effects On Survival Of Metamorphic Frogs During Pond Emigration
journal, February 2006

  • Chelgren, Nathan D.; Rosenberg, Daniel K.; Heppell, Selina S.
  • Ecological Applications, Vol. 16, Issue 1
  • DOI: 10.1890/04-0329

Behavioral plasticity mitigates risk across environments and predators during anuran metamorphosis
journal, July 2013


Energetics of metamorphic climax in the southern toad ( Bufo terrestris )
journal, November 2003


Differential Predation on Metamorphic Anurans by Garter Snakes (Thamnophis): Social Behavior as a Possible Defense
journal, August 1978

  • Arnold, Stevan J.; Wassersug, Richard J.
  • Ecology, Vol. 59, Issue 5
  • DOI: 10.2307/1938553

Combined Effects of Virus, Pesticide, and Predator Cue on the Larval Tiger Salamander (Ambystoma tigrinum)
journal, March 2011


Larval experience and latent effects--metamorphosis is not a new beginning
journal, March 2006

  • Pechenik, J. A.
  • Integrative and Comparative Biology, Vol. 46, Issue 3
  • DOI: 10.1093/icb/icj028

Effects of Aquatic Exposure to the Insecticide Carbaryl and Density on Aquatic and Terrestrial Growth and Survival in American Toads
journal, January 2009

  • Distel, Christopher A.; Boone, Michelle D.
  • Environmental Toxicology and Chemistry, Vol. 28, Issue 9
  • DOI: 10.1897/09-026.1

Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae
journal, August 2013