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Timing of oviposition influences the effects of a non-native grass on amphibian development

Oecologia volume 194, pages 113–122 (2020)Cite this article

Abstract

Land-use change can alter the energy dynamics in aquatic systems by changing the subsidies that form the nutrient base within them. However, experimental evaluations of subsidy change often fail to consider how effects, such as differences in individual growth and survival, may differ under varying ecological contexts experienced in the field. We used a mesocosm approach to investigate how litter (Native Prairie or Non-Native Tall-Fescue Grass) surrounding wetlands and timing of oviposition affected larval amphibian development. We found that survival differed between litter types in the Early-Oviposition treatment, with nearly 100% mortality in Fescue treatments. Conversely, survival  was similar across litter types in the Late Oviposition treatment (~ 43%), and larvae in Late-Fescue treatments metamorphosed more quickly and were larger post-metamorphosis than larvae in Prairie treatments. Follow-up experiments confirmed that low dissolved oxygen (DO) was responsible for high mortality in Early-Fescue treatments; high quantities of Fescue resulted in a microbial bloom that reduced DO to < 2 mg/L for several days, resulting in low hatching success. This effect was eliminated in treatments with supplemental aeration. Finally, we confirmed that experimentally observed DO patterns also occurred in the field. Context (i.e., timing of inundation relative to amphibian breeding) is critical to understanding the effects of subsidies on amphibian populations; early and explosively breeding species may experience catastrophic mortality due to DO depletion; whereas, species that breed later may experience enhanced fitness of recruits. Considering the effects of non-native species across different ecological contexts is necessary for elucidating the extent of their impacts.

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Data availability

The datasets generated during the current study are available as an electronic supplement with this manuscript.

References

  • Adams CK, Saenz D (2012) Leaf litter of invasive Chinese tallow (triadica sebifera) negatively affects hatching success of an aquatic breeding anuran, the southern leopard frog (Liithobates sphenocephalus). Can J Zool 90:991–998

    CAS  Google Scholar 

  • Aerts R, de Caluwe H (1997) Initial litter respiration as indicator for long-term leaf litter decomposition of Carex species. Oikos 80:353–361

    Google Scholar 

  • Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA, Power M (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152

    Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater. In: Eaton AE, Clesceri LS, Rice EW, Greenberg AE, Franson MAH (eds), 21st edn, American Public Health Association, Washington

  • Baecher JA, Vogrinc PN, Guzy JC, Kross CS, Willson JD (2018) Herpetofaunal communities in restored and unrestored remant tallgrass prairie and associated wetlands in Northwest Arkansas, USA. Wetlands 38:157–168

    Google Scholar 

  • Battle JM, Golladay SW (2001) Hydroperiod influence on breakdown of leaf litter in cypress-gum wetlands. Am Midl Nat 146:128–145

    Google Scholar 

  • Bradford DF (1983) Winterkill, oxygen relations, and energy metabolism of a submerged dormant amphibian, Rana mucosa. Ecology 64:1171–1183

    Google Scholar 

  • Burggren WW, West NH (1982) Changing respiratory importance of gills, lungs, and skin during metamorphosis in the bullfrog Rana catesbeiana. Respir Physiol 47:151–164

    CAS  PubMed  Google Scholar 

  • Cabrera-Guzmán E, Crossland MR, Brown GP, Shine R (2013) Larger body size at metamorphosis enhances survival, growth, and performance of young cane toads (Rhinella marina). PLoS ONE 8:e701772. https://doi.org/10.1371/journal.pone.0070121

    Article  CAS  Google Scholar 

  • Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639

    Google Scholar 

  • Carpenter SR, Cole JJ, Hodgson JR, Kitchell JF, Pace ML, Bade D, Cottingham KL, Essington TE, Houser JN, Schindler DE (2001) Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71:163–186

    Google Scholar 

  • Cherney JH (2007) Tall fescue for forage production. Forage Information. Purdue University. https://www.agry.purdue.edu/ext/forages/publications/ay98.htm

  • Cohen JS, Maerz JC, Blossey B (2012) Traits, not origin, explain impacts of plants on larval amphibians. Ecol Appl 22:218–228

    PubMed  Google Scholar 

  • Comer PJ, Hak JC, Kindscher K, Muldavin E, Singhurst J (2018) Continent-scale landscape conservation design for temperate grasslands of the Great Plains and Chihuahuan Desert. Nat Areas J 38:196–211

    Google Scholar 

  • Development Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Earl JE, Semlitsch RD (2013) Spatial subsidies, trophic state, and community structure: examining effects of leaf litter on ponds. Ecosystems 16:639–651

    Google Scholar 

  • Earl JE, Castello PO, Cohagen KE, Semlitsch RD (2014) Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export. Oecologica 175:209–218

    Google Scholar 

  • Entrekin SA, Tank TL, Rosi-Marshall EJ, Hoellein TJ, Lamberti GA (2008) Responses in organic matter accumulation and processing to an experimental wood addition in three headwater streams. Freshw Biol 53:1642–1657

    CAS  Google Scholar 

  • Feder ME (1983a) Responses to acute aquatic hypoxia in larvae of the frog Rana berlandieri. J Exp Biol 104:79–95

    Google Scholar 

  • Feder ME (1983b) Effect of hypoxia and body size on the energy metabolism of lungless tadpoles, Bufo woodhousei, and air-breathing anuran larvae. J Exp Zool 228:11–19

    Google Scholar 

  • Fish D, Carpenter SR (1982) Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63:283–288

    Google Scholar 

  • Foster D, Swanson F, Aber J, Burke I, Brokaw N, Tilman D, Knapp A (2003) The importance of land-use legacies to ecology and conservation. Bioscience 53:77–88

    Google Scholar 

  • Fuell AK, Entrekin SA, Owen GS, Owen SK (2013) Drivers of leaf decomposition in two wetland types in the Arkansas River Valley, USA. Wetlands 33:1127–1137

    Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Hall RO, Meyer JL (1998) The trophic significance of bacteria in detritus-based stream food web. Ecology 79:1995–2012

    Google Scholar 

  • Hall RO, Wallace JB, Eggert SL (2000) Organic matter flow in stream food webs with reduced detrital resource base. Ecology 81:3445–3463

    Google Scholar 

  • Hammerson GM Parris (2004) Lithobates areolatus. The IUCN Red List of Threatened Species 2004:e.T58546A11799946. https://doi.org/10.2305/IUCN.UK.2004.RLTS.T58546A11799946.en

  • Henwood WD (2010) Toward a strategy for the conservation and protection of the world’s temperate grasslands. Great Plains Res 20:121–134

    Google Scholar 

  • Knutson MG, Richardson WB, Reineke DM, Gray BR, Parmelee JR, Weick SE (2004) Agricultural ponds support amphibian populations. Ecol Appl 14:669–684

    Google Scholar 

  • Leroux SJ, Loreau M (2008) Subsidy hypothesis and strength of trophic cascades across ecosystems. Ecol Lett 11:1147–1156

    PubMed  Google Scholar 

  • Maerz JC, Brown CJ, Chapin CT, Blossey B (2005) Can secondary compounds of an invasive plant affect larval amphibians? Funct Ecol 19:970–975

    Google Scholar 

  • Maerz JC, Cohen JS, Blossey B (2010) Does detritus quality predict the effect of native and nonnative plants on the performance of larval amphibians? Freshw Biol 55:1694–1704

    Google Scholar 

  • Mallin MA, Johnson VL, Ensign SH, MacPherson TA (2006) Factors contributing to hypoxia in rivers, lakes, and streams. Limnol Oceanogr 51:690–701

    CAS  Google Scholar 

  • Meyer JL (1994) The microbial loop in flowing waters. Microb Ecol 28:195–199

    CAS  PubMed  Google Scholar 

  • Miller JH (2003) Nonnative invasive plants of southern forests: a field guide to identification and control, vol 62. US Department of Agriculture, Forest Service, Southern Research Station

    Google Scholar 

  • Pace ML, Cole JC, Carpenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC, Bade DL, Kritzberg DL, Bastviken D (2004) Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–243

    CAS  PubMed  Google Scholar 

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316

    Google Scholar 

  • Rogalski MA, Skelly DK (2012) Positive effects of nonnative invasive Phragmites australis on larval bullfrogs. PLoS ONE 7(8):e44420. https://doi.org/10.1371/journal.pone.0044420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosemond AD, Mulholland PJ, Elwood JW (1993) Top-down and bottom-up control of stream periphyton growth: effects of nutrients and herbivores. Ecology 74:1264–1280

    Google Scholar 

  • Rubbo MJ, Kiesecker JM (2004) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525

    Google Scholar 

  • Rubbo MJ, Belden LK, Kiesecker JM (2006) Differential responses of aquatic consumers to variations in leaf-litter inputs. Hydrobiologia 605:37–44

    Google Scholar 

  • Sacerdote AB, King RB (2009) Dissolved oxygen requirements for hatching success of two ambystomatid salamanders in restored ephemeral wetlands. Wetlands 29:1202–1213

    Google Scholar 

  • Samson FB, Knopf FL (1994) Prairie conservation in North America. Bioscience 44:418–421

    Google Scholar 

  • Samson FB, Fl Knopf, Ostlie WR (2004) Great plains ecosystems: past, present, and future. Wildl Soc Bull 32:6–15

    Google Scholar 

  • Semlitsch RD (1983) Growth and metamorphosis of larval red salamanders (Pseudotriton ruber) on the coastal plain of South Carolina. Ecology 39:48–52

    Google Scholar 

  • Semlitsch RD (1987) Relationship of pond drying to reproductive success of the salamander Ambystoma talpoideum. Copeia 1987:61–69

    Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192

    Google Scholar 

  • Sleper DA, West CP (1996) Tall Fescue. In: Moser LE, Buxton DR, Casler MD (eds) Cool-season forage grasses. American Society of Agronomy; Crop Science, Society of America; Soil Science Society of America, Madison, pp 471–502

    Google Scholar 

  • Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350

    Google Scholar 

  • Stephens JP, Berven KA, Tiegs SD (2013) Anthropogenic changes to leaf litter input affect the fitness of a larval amphibian. Freshw Biol 58:1631–1646

    CAS  Google Scholar 

  • Stoler AB, Relyea RA (2011) Living in the litter: the influence of tree leaf litter on wetland communities. Oikos 120:862–872

    Google Scholar 

  • Stream Solute Workshop (1990) Concepts and methods for assessing solute dynamics in stream ecosystems. J N Am Benthol Soc 9:95–119

    Google Scholar 

  • Trauth SE, Robison HW, Plummer MV (2004) The amphibians and reptiles of arkansas. The University of Arkansas Press, Fayetteville, pp 166–167

    Google Scholar 

  • Watling JI, Hickman CR, Lee E, Wang K, Orrock JL (2011a) Extracts of the invasive Lonicera maackii increase mortality and alter behavior of amphibian larvae. Oecologia 165:153–159

    CAS  PubMed  Google Scholar 

  • Watling JI, Hickman CR, Orrock JL (2011b) Predators and invasive plants affect performance of amphibian larvae. Oikos 120:735–739

    Google Scholar 

  • Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594

    Google Scholar 

  • Wilcox HS, Wallace JB, Meyer JL, Benstead JP (2005) Effects of labile carbon addition on a headwater stream food web. Limnol Oceanogr 50:1300–1312

    CAS  Google Scholar 

  • Williams BK, Rittenhouse TAG, Semlitsch RD (2008) Leaf litter input mediates tadpole performance across forest canopy treatments. Oecologia 155:377–384

    PubMed  Google Scholar 

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Acknowledgements

Funding for this project was partially provided by the National Science Foundation (NSF DBI 1659857) and the University of Arkansas, as well as Prairie Biotic Research and the Arkansas Audubon Society Trust. We thank Mackenzie Bramlett, Jessika Dorcas, Logan Estes, Dr. Jackie Guzy, Kelly Halloran, Micalea Klaus, David Reed, Meredith Swartwout, and Phil Vogrinc for help in vegetation and data collection. We thank Dr. Jennifer Mortensen for assisting in data analysis in the egg hatching experiment and data collection. Thank you to Erik Pollock and Lindsey Conaway, from the University of Arkansas Stable Isotope Laboratory, for running nutrient analyses. We also thank Dr. Hal Halvorson for running preliminary nutrient tests. Thank you to Drs Steve Beaupre, Jeff Briggler, and Dan Magoulick for project guidance and comments on early versions of this manuscript. Additionally, we thank Ethan Royal and three reviewers for their comments that improved this manuscript. For site access and support, we thank the City of Fayetteville and Woolsey Wet Prairie Sanctuary, especially Jeff Hickle and Bruce Shackleford.

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Authors and Affiliations

  1. University of Arkansas, Fayetteville, AR, 72704, USA

    Chelsea S. Kross, Philip L. Mariage & John D. Willson

  2. Stephen A. Forbes Biological Station, Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Havana, IL, 62644, USA

    Chelsea S. Kross

  3. Lyon College, Batesville, AR, 72501, USA

    Allyn K. Dodd

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  1. Chelsea S. Kross
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Contributions

CSK and JDW conceived the ideas and designed methodology; CSK, AKD, and PLM collected the data; CSK and AKD analyzed the data, CSK led the writing of the manuscript, comments from JDW improved the manuscript. All authors gave final approval for publication.

Corresponding author

Correspondence to Chelsea S. Kross.

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The authors declare they have no conflict of interest.

Animal rights

All applicable institutional and national guidelines for the care and use of animals and were approved and followed (IACUC protocol #’s 15033 and 17079).

Additional information

Communicated by Howard Whiteman.

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Kross, C.S., Dodd, A.K., Mariage, P.L. et al. Timing of oviposition influences the effects of a non-native grass on amphibian development. Oecologia 194, 113–122 (2020). https://doi.org/10.1007/s00442-020-04744-3

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  • DOI: https://doi.org/10.1007/s00442-020-04744-3

Keywords

  • Agriculture
  • Dissolved oxygen
  • Grasslands
  • Microbial respiration
  • Lithobates