Abstract
Agricultural drainage ditches help remove excess water from fields and provide habitat for wildlife. Drainage ditch management, which includes various forms of vegetation clearing and sediment dredging, can variably affect the ecological function of these systems. To determine whether ditch conditions following dredging/vegetation clearing management affected the survival, growth, and development of embryos and tadpoles of northern leopard frogs (Lithobates pipiens), we conducted three field studies using in situ cages over 2 years. We measured nutrients, pesticides, and other water quality properties in vegetated/unmanaged (i.e., no clearing or dredging) and newly cleared/dredged (i.e., treeless, then dredged), clay-bottomed drainage ditches in a river basin in Eastern Ontario, Canada. Nutrients, atrazine, and total neonicotinoid concentrations were generally lower at the cleared/dredged sites, whereas glyphosate was at higher concentrations. In contrast, water-quality variables measured in situ, particularly temperature, dissolved oxygen, and turbidity, tended to be higher in the cleared/dredged sites. Total phosphorous and total organic carbon concentrations at all sites were above the recommended limits for amphibian assays. No significant differences were detected in the survival, hatching success, or development of embryos among the ditch management treatments, but premature hatching was observed at one vegetated/unmanaged site where high specific conductivity may have been formative. We found the cleared/dredged sites supported earlier tadpole growth and development, likely as a result of the higher water temperatures. Increased temperature may have offset other growth/development stressors, such as those related to water chemistry. However, the long-term consequences of these differences on amphibian populations requires further study.
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Data Availability
The datasets generated during and/or analysed during the current study are available as Supplementary Information.
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Not applicable.
Change history
22 May 2021
On page 11, the sentence that ends “in waters with salinity 5/ or higher, and mortality increased with salinity levels (17% mortality at 1/ to 79% mortality at 30/).” the ‘5/’ and ‘1/’ and ‘30/’ should be ‘5‰’ and ‘1‰’ and ‘30‰’.
References
Allaway C (2006) Combined nitrogen retention in an agricultural river system. University of Ottawa
Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution (NY) 57:872–882
Anderson JC, Dubetz C, Palace VP (2015) Neonicotinoids in the Canadian aquatic environment: a literature review on current use products with a focus on fate, exposure, and biological effects. Sci Total Environ 505:409–422. https://doi.org/10.1016/J.SCITOTENV.2014.09.090
Barton DR, Taylor WD, Biette RM (1985) Dimensions of Riparian buffer strips required to maintain trout habitat in Southern Ontario Streams. North Am J Fish Manag 5:364–378. https://doi.org/10.1577/1548-8659(1985)5%3c364:dorbsr%3e2.0.co;2
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bernabò I, Guardia A, Macirella R et al (2016) Effects of long-term exposure to two fungicides, pyrimethanil and tebuconazole, on survival and life history traits of Italian tree frog (Hyla intermedia). Aquat Toxicol 172:56–66. https://doi.org/10.1016/j.aquatox.2015.12.017
Berven KA, Gill DE (1983) Interpreting geographic variation in life-history traits. Am Zool Am Zool 23:85–97
Biggs J, von Fumetti S, Kelly-Quinn M (2017) The importance of small waterbodies for biodiversity and ecosystem services: implications for policy makers. Hydrobiologia 793:3–39. https://doi.org/10.1007/s10750-016-3007-0
Bracewell S, Verdonschot RC, Schafer RB et al (2019) Qualifying the effects of single and multiple stressors on the food web structure of Dutch drainage ditches using a literature review and conceptual models. Sci Total Environ 684:727–740. https://doi.org/10.1016/j.scitotenv.2019.03.497
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644
CCME - Canadian Council of Ministers of the Environment (2007) Canadian water quality guidelines for protection of aquatic life: Imidacloprid. In: Canadian environmental quality guidelines, 1999. Canadian Council of Ministers of the Environment, Winnipeg, p 12
Christin MS, Ménard L, Giroux I et al (2013) Effects of agricultural pesticides on the health of Rana pipiens frogs sampled from the field. Environ Sci Pollut Res 20:601–611. https://doi.org/10.1007/s11356-012-1160-1
Collins SJ, Fahrig L (2017) Responses of anurans to composition and configuration of agricultural landscapes. Agric Ecosyst Environ 239:399–409. https://doi.org/10.1016/j.agee.2016.12.038
Collins SJ, Bellingham L, Mitchell GW, Fahrig L (2019) Life in the slow drain: Landscape structure affects farm ditch water quality. Sci Total Environ 656:1157–1167. https://doi.org/10.1016/j.scitotenv.2018.11.400
Crane M, Burton GA, Culp JM et al (2007) Review of aquatic in situ approaches for stressor and effect diagnosis. Integr Environ Assess Manag 3:234–245. https://doi.org/10.1897/IEAM_2006-027.1
Curran-Everett D (2013) Explorations in statistics: The analysis of ratios and normalized data. Am J Physiol Adv Physiol Educ 37:213–219. https://doi.org/10.1152/advan.00053.2013
Dalton RL, Pick FR, Boutin C, Saleem A (2014) Atrazine contamination at the watershed scale and environmental factors affecting sampling rates of the polar organic chemical integrative sampler (POCIS). Environ Pollut 189:134–142. https://doi.org/10.1016/j.envpol.2014.02.028
Dalton RL, Boutin C, Pick FR (2015a) Nutrients override atrazine effects on riparian and aquatic plant community structure in a North American agricultural catchment. Freshw Biol 60:1292–1307. https://doi.org/10.1111/fwb.12563
Dalton RL, Boutin C, Pick FR (2015b) Determining in situ periphyton community responses to nutrient and atrazine gradients via pigment analysis. Sci Total Environ 515–516:70–82. https://doi.org/10.1016/j.scitotenv.2015.01.023
De Solla SR, Pettit KE, Bishop CA et al (2002) Effects of agricultural runoff on native amphibians in the Lower Fraser River Valley, British Columbia, Canada. Environ Toxicol Chem 21:353–360
Dollinger J, Dagès C, Bailly JS et al (2015) Managing ditches for agroecological engineering of landscape. A review. Agron Sustain Dev 35:999–1020. https://doi.org/10.1007/s13593-015-0301-6
Edge CB, Gahl MK, Pauli BD et al (2011) Exposure of juvenile green frogs (Lithobates clamitans) in littoral enclosures to a glyphosate-based herbicide. Ecotoxicol Environ Saf 74:1363–1369. https://doi.org/10.1016/j.ecoenv.2011.04.020
Evans RO, Bass KL, Burchell MR et al (2007) Management alternatives to enhance water quality and ecological function of channelized streams and drainage canals. J Soil Water Conserv 62:308–320
Feng S, Kong Z, Wang X et al (2004) Acute toxicity and genotoxicity of two novel pesticides on amphibian, Rana N. Hallowell. Chemosphere 56:457–463. https://doi.org/10.1016/j.chemosphere.2004.02.010
Fiener P, Auerswald K (2003) Effectiveness of grassed waterways in reducing runoffand sediment delivery from agricultural watersheds. Environ Qual 32:927–936
Flora C, Kröger R (2014) Use of vegetated drainage ditches and low-grade weirs for aquaculture effluent mitigation: II. Suspended sediment. Aquac Eng 60:68–72. https://doi.org/10.1016/j.aquaeng.2014.04.007
Gomez-Mestre I, Wiens JJ, Warkentin KM (2008) Evolution of adaptive plasticity: risk-sensitive hatching in neotropical leaf-breeding treefrogs. Ecol Monogr 78:205–224. https://doi.org/10.1890/07-0529.1
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190. https://doi.org/10.2307/3890061
Green JW, Springer TA, Holbech H (2018) Statistical analysis of ecotoxicity studies, 1st edn. Wiley, Hoboken
Haramura T (2016) Hatching plasticity in response to salinity levels in a rhacophorid frog inhabiting a coastal area. J Zool 299:125–131. https://doi.org/10.1111/jzo.12323
Harris M, Bogart J (1997) A cage for evaluation of in situ water quality using frog eggs and tadpoles. Herpetol Rev 28:134–135
Harris ML, Bishop CA, Struger J et al (1998) The functional integrity of northern leopard frog (Rana pipiens) and green frog (Rana clamitans) populations in orchard wetlands. II. Effects of pesticides and eutrophic conditions on early life stage development. Environ Toxicol Chem 17:1351–1363. https://doi.org/10.1897/1551-5028(1998)017%3c1351:TFIONL%3e2.3.CO;2
Harris ML, Bishop CA, McDaniel TV (2001) Assessment of rates of deformity in wild frog populations using in situ cages: a case study of leopard frogs (Rana pipiens) in Ontario, Canada. Biomarkers 6:52–63. https://doi.org/10.1080/135475001452797
Hartel T, Bǎncilǎ R, Cogǎlniceanu D (2011) Spatial and temporal variability of aquatic habitat use by amphibians in a hydrologically modified landscape. Freshw Biol 56:2288–2298. https://doi.org/10.1111/j.1365-2427.2011.02655.x
Hayek L-AC, Heyer WR, Gascon C (2001) Frog morphometries: a cautionary tale. Alytes 18:153–177
Hayes T, Haston K, Tsui M et al (2002) Herbicides: feminization of male frogs in the wild. Nature 419:895–896. https://doi.org/10.1038/419895a
Hayes T, Haston K, Tsui M et al (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): Laboratory and field evidence. Environ Health Perspect 111:568–575. https://doi.org/10.1289/ehp.5932
Hayes TB, Case P, Chui S et al (2006) Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ Health Perspect 114:40–50. https://doi.org/10.1289/ehp.8051
Hecnar S, M’Closkey R (1996) Amphibian species richness and distribution in relation to pond water chemistry in south-western Ontario, Canada. Freshw Biol 36:7–15. https://doi.org/10.1046/j.1365-2427.1996.00054.x
Herzon I, Helenius J (2008) Agricultural drainage ditches, their biological importance and functioning. Biol Conserv 141:1171–1183. https://doi.org/10.1016/j.biocon.2008.03.005
Hogan NS, Duarte P, Wade MG et al (2008) Estrogenic exposure affects metamorphosis and alters sex ratios in the northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. Gen Comp Endocrinol 156:515–523. https://doi.org/10.1016/j.ygcen.2008.03.011
Howe CM, Berrill M, Pauli BD et al (2004) Toxicity of glyphosate based pesticides to four North American frog species. Env Toxicol Chem 23:1928–1938. https://doi.org/10.1897/03-71
Johnson MS, Aubee C, Salice CJ et al (2017) A review of ecological risk assessment methods for amphibians: comparative assessment of testing methodologies and available data. Integr Environ Assess Manag 13:601–613. https://doi.org/10.1002/ieam.1881
Karraker NE, Gibbs JP, Vonesh JR (2008) Impacts of road deicing salt on the demography of vernal pool-breeding amphibians. Ecol Appl 18:724–72434. https://doi.org/10.1890/07-1644.1
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Langlois VS, Carew AC, Pauli BD et al (2010) Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms. Environ Health Perspect 118:552–557. https://doi.org/10.1289/ehp.0901418
Lee-Jenkins SY, Robinson SA (2018) Effects of neonicotinoids on putative escape behavior of juvenile wood frogs (Lithobates sylvaticus) chronically exposed as tadpoles. Environ Toxicol Chem Chem 37:3115–3123. https://doi.org/10.1002/etc.4284
Maisonneuve C, Rioux S (2001) Importance of riparian habitats for small mammal and herpetofaunal communities in agricultural landscapes of southern Québec. Ecosyst Environ 83:165–175
Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927. https://doi.org/10.1016/j.envpol.2009.05.015
Marian M, Pandian T (1985) Effect of temperature on development, growth and bioenergetics of the bullfrog tadpole Rana tigrina. J Therm Biol 10:157–161. https://doi.org/10.1016/0306-4565(85)90020-8
Mazerolle MJ (2005) Drainage ditches facilitate frog movements in a hostile landscape. Landsc Ecol 20:579–590. https://doi.org/10.1007/s10980-004-3977-6
Moore LJ, Fuentes L, Rodgers JH et al (2012) Relative toxicity of the components of the original formulation of Roundup to five North American anurans. Ecotoxicol Environ Saf 78:128–12833. https://doi.org/10.1016/j.ecoenv.2011.11.025
Morrissey CA, Mineau P, Devries JH et al (2015a) Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ Int 74:291–303. https://doi.org/10.1016/j.envint.2014.10.024
Nakagawa S, Cuthill I (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605. https://doi.org/10.1111/j.1469-185X.2007.00027.x
Needelman BA, Kleinman PJA, Allen AL (2007) Improved management of agricultural drainage ditches for water quality protection: an overview. J Soil Water Conserv 62:171–178
Newman RA (1998) Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level. Oecologia 115:9–16. https://doi.org/10.1007/s004420050485
Oda FH, Batista VG, Gambale PG et al (2016) Anuran species richness, composition, and breeding habitat preferences: a comparison between forest remnants and agricultural landscapes in Southern Brazil. Zool Stud 55:1–14. https://doi.org/10.6620/ZS.2016.55-34
OECD (2009) Test No. 231: amphibian metamorphosis assay. In: OECD guidelines for the testing of chemicals. OECD, Paris
OECD (2015) Test No. 241: The Larval amphibian growth and development assay (LAGDA). OECD iLibrary 227:1–19. https://doi.org/10.1787/9789264242340-en
Pappas E, Smith D (2007a) Effects of dredging an agricultural drainage ditch on water column herbicide concentration, as predicted by fluvarium techniques. J Soil Water Conserv 62:262–268
Pohl J, Örn S, Norrgren L, Carlsson G (2015) Toxicological evaluation of water from stormwater ponds using Xenopus tropicalis embryos. Wetl Ecol Manag 23:1091–1098. https://doi.org/10.1007/s11273-015-9444-0
R Core Team (2017) R: a language and environment for statistical computing, 3.5.1
Relyea R, Jones D (2009) The toxicity of roundup original max to 13 species of larval amphibians. Environ Toxicol Chem 28:2004–2008
Riha V, Berven K (1991) An analysis of latitudinal variation in the larval development of the wood frog (Rana sylvatica). Copeia 1991:209–221. https://doi.org/10.2307/1446264
Robinson SA, Richardson SD, Dalton RL et al (2017) Sublethal effects on wood frogs chronically exposed to environmentally relevant concentrations of two neonicotinoid insecticides. Environ Toxicol Chem 36:1101–1109. https://doi.org/10.1002/etc.3739
Robinson SA, Richardson SD, Dalton RL et al (2019) Assessment of sublethal effects of neonicotinoid insecticides on the life-history traits of 2 frog species. Environ Toxicol Chem 38:1967–1977. https://doi.org/10.1002/etc.4511
Robinson SA, Young SD, Brinovcar C et al (2020) Ecotoxicity assessment and bioconcentration of a highly brominated organophosphate ester flame retardant in two amphibian species. Chemosphere 260:127631. https://doi.org/10.1016/j.chemosphere.2020.127631
Rodney SI, Teed RS, Moore DRJ (2013) Estimating the toxicity of pesticide mixtures to aquatic organisms: a review. Hum Ecol Risk Assess 19:1557–1575. https://doi.org/10.1080/10807039.2012.723180
Rudolf VHW, Rödel MO (2007) Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evol Ecol 21:121–142. https://doi.org/10.1007/s10682-006-0017-9
Ruthsatz K, Peck MA, Dausmann KH et al (2018) Patterns of temperature induced developmental plasticity in anuran larvae. J Therm Biol 74:123–132. https://doi.org/10.1016/j.jtherbio.2018.03.005
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Semlitsch RD, Scott DE, Pechmann HK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192. https://doi.org/10.2307/1943173
Shi Y-B (2000) Amphibian metamorphosis: from morphology to molecular biology. Wiley-Liss, Bethesda
Shigaki F, Schmidt JP, Kleinman PJA et al (2009) Nitrogen fate in drainage ditches of the coastal plain after dredging. J Environ Qual 38:2449–2457. https://doi.org/10.2134/jeq2008.0268
Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83:983–992. https://doi.org/10.1890/0012-9658(2002)083[0983:FCATPO]2.0.CO;2
Smalling KL, Reeves R, Muths E et al (2015) Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture. Sci Total Environ 502:80–90. https://doi.org/10.1016/j.scitotenv.2014.08.114
Smith DC (1987) Adult recruitment in Chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350. https://doi.org/10.2307/1939265
Smith D, Huang C (2010) Assessing nutrient transport following dredging of agricultural drainage ditches. Trans ASABE 53:429–436
Smith DR, Pappas EA (2007) Effect of ditch dredging on the fate of nutrients in deep drainage ditches of the Midwestern United States. J Soil Water Conserv 62:252–261
Smith DR, Warnemuende EA, Haggard BE, Huang C (2006) Dredging of drainage ditches increases short-term transport of soluble phosphorus. J Environ Qual 35:611. https://doi.org/10.2134/jeq2005.0301
Sparling D, Linder G, Bishop C (2000) Ecotoxicology of amphibians and reptiles, 1st edn. Society of Environmental Toxicology and Chemistry, Pensacola
Sunohara MD, Topp E, Wilkes G et al (2012) Impact of riparian zone protection from cattle on nutrient, bacteria, f-coliphage, cryptosporidium, and giardia loading of an intermittent stream. J Environ Qual 41:1301–1314. https://doi.org/10.2134/jeq2011.0407
Sunohara MD, Gottschall N, Wilkes G et al (2015) Long-term observations of nitrogen and phosphorus export in paired-agricultural watersheds under controlled and conventional tile drainage. J Environ Qual 44:1589–1604. https://doi.org/10.2134/jeq2015.01.0008
Székely D, Denoël M, Székely P, Cogălniceanu D (2017) Pond drying cues and their effects on growth and metamorphosis in a fast developing amphibian. J Zool 303:129–135. https://doi.org/10.1111/jzo.12468
Tavera-Mendoza L, Ruby S, Brousseau P et al (2002) Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ Toxicol Chem 21:527–531. https://doi.org/10.1002/etc.5620210309
Touchon JC, Gomez-Mestre I, Warkentin KM (2006) Hatching plasticity in two temperate anurans: responses to a pathogen and predation cues. Can J Zool 84:556–563. https://doi.org/10.1139/Z06-058
Trudeau VL, Schueler FW, Navarro-Martin L et al (2013) Efficient induction of spawning of northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season. Reprod Biol Endocrinol 11:14. https://doi.org/10.1186/1477-7827-11-14
Valls JH, Mills NE (2007) Intermittent hypoxia in eggs of Ambystoma maculatum: embryonic development and egg capsule conductance. J Exp Biol 210:2430–2435. https://doi.org/10.1242/jeb.003541
Warkentin KM (2011) Plasticity of hatching in amphibians: evolution, trade-offs, cues and mechanisms. Integr Comp Biol 51(1):111–127
Wilbur HM (1977) Density-dependent aspects of growth and metamorphosis in Bufo americanus. Ecology 58:196–200. https://doi.org/10.2307/1935122
Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis: nonnormal distributions of competitive ability reflect selection for facultative metamorphosis. Science 182(4119):1305–1314. https://doi.org/10.1126/science.182.4119.1305
Wilkes G, Brassard J, Edge TA et al (2014) Long-term monitoring of waterborne pathogens and microbial source tracking markers in paired agricultural watersheds under controlled and conventional tile drainage management. Appl Environ Microbiol 80:3708–3720. https://doi.org/10.1128/AEM.00254-14
Wilkes G, Sunohara MD, Topp E et al (2019) Do reductions in agricultural field drainage during the growing season impact bacterial densities and loads in small tile-fed watersheds? Water Res 151:423–438. https://doi.org/10.1016/j.watres.2018.11.074
Williams N, Sweetman J (2019) Distribution and concentration of neonicotinoid insecticides on waterfowl production areas in West Central Minnesota. Wetlands 39:311–319. https://doi.org/10.1007/s13157-018-1090-x
Witschi E (1931) Studies on sex differentiation and sex determination in amphibians. J Exp Zool 58:113–145
Zuur AF, Hilbe JM, Ieno EN (2013) A beginner’s guide to GLM and GLMM with R., Beginner’s. Highland Statistics, Newburgh
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgments
They acknowledge that the study took place on unceded Algonquin Territory. They thank Dr. Vance L. Trudeau (University of Ottawa) for providing the egg masses and France Maisonneuve and Eric Pelletier from ECCC for their assistance with the pesticide concentration data. They also thank Alexandre Thibodeau, Isabella C. Richmond, Jocelyn Mennen, and Kimberly O’Hare for their help in setting up and monitoring the embryo and tadpole field experiments.
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This project was funded by Agriculture and Agri-Food Canada, Environment and Climate Change Canada (SR01-2018 and SR01-2019) and by the Natural Science and Engineering Research Council of Canada (NSERC RGPIN 036751 to FRP).
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by AD, SDY, SAR, JBR, LS, and FRP. AD, SDY, and SAR wrote the first draft of the manuscript. All authors contributed to the final manuscript. FRP, SAR, and DRL provided supervision. All authors read and approved the final manuscript.
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Dyck, A., Robinson, S.A., Young, S.D. et al. The Effects of Ditch Management in Agroecosystems on Embryonic and Tadpole Survival, Growth, and Development of Northern Leopard Frogs (Lithobates pipiens). Arch Environ Contam Toxicol 81, 107–122 (2021). https://doi.org/10.1007/s00244-021-00836-0
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DOI: https://doi.org/10.1007/s00244-021-00836-0