Joint Effects of Fragmentation and Mercury Contamination on Marsh Periwinkle (Littoraria irrorata) Movement.
Habitat fragmentation
Hidden Markov models
Mercury
Movement
Multiple stressors
Journal
Environmental toxicology and chemistry
ISSN: 1552-8618
Titre abrégé: Environ Toxicol Chem
Pays: United States
ID NLM: 8308958
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
revised:
07
03
2022
received:
03
02
2022
accepted:
20
04
2022
pubmed:
28
4
2022
medline:
29
6
2022
entrez:
27
4
2022
Statut:
ppublish
Résumé
There are different ways contaminants can interact and enhance the effects of habitat fragmentation, such as modifying the movement of organisms. The present study tested the hypothesis that mercury exacerbates the effects of fragmentation by affecting the movement of the marsh periwinkle Littoraria irrorata and reducing the probability of snails crossing fragmented microlandscape experimental systems. How these changes could affect the search efficiency of organisms in the long term was assessed using hidden Markov models and random walks simulations. Bayesian nonlinear models were used to analyze the effects of fragmentation and contamination on the mean speed and mean directional change of organisms. Snail movement for control and two mercury-exposure treatments were recorded in microlandscapes with six different levels of habitat cover and three landscape replicates. The results indicated that exposed organisms had lower probabilities of crossing the landscape, reduced speed, and shifts in step length distributions. Both mercury exposure and habitat fragmentation affected the movement of the marsh periwinkle. Mercury exacerbated the effects of habitat fragmentation by affecting the cognition (e.g., route planning, orientation, and spatial learning) and movement of L. irrorata. Hence, the interaction of these stressors could further reduce the functional connectivity of landscapes and reduce the search efficiency of organisms. Environ Toxicol Chem 2022;41:1742-1753. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
Substances chimiques
Mercury
FXS1BY2PGL
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1742-1753Informations de copyright
© 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
Références
Adams, E. M., & Frederick, P. C. (2008). Effects of methylmercury and spatial complexity on foraging behavior and foraging efficiency in juvenile white ibises (Eudocimus albus). Environmental Toxicology and Chemistry, 27, 1708-1712.
Alexander, H. M., Foster, B. L., Ballantyne, F., Collins, C. D., Antonovics, J., & Holt, R. D. (2012). Metapopulations and metacommunities: Combining spatial and temporal perspectives in plant ecology. Journal of Ecology, 100, 88-103.
Anderson, E. P., Jenkins, C. N., Heilpern, S., Maldonado-Ocampo, J. A., Carvajal-Vallejos, F. M., Encalada, A. C., Rivadeneira, J. F., Hidalgo, M., Cañas, C. M., Ortega, H., Salcedo, N., Maldonado, M., & Tedesco, P. A. (2018). Fragmentation of Andes-to-Amazon connectivity by hydropower dams. Science Advances, 4, 1-7.
Araújo, C. V., Martinez-Haro, M., Pais-Costa, A. J., Marques, J. C., & Ribeiro, R. (2016). Patchy sediment contamination scenario and the habitat selection by an estuarine mudsnail. Ecotoxicology, 25, 412-418.
Araújo, C. V., Silva, D. C., Gomes, L. E., Acayaba, R. D., Montagner, C. C., Moreira-Santos, M., Ribeiro, R., & Pompêo, M. L. (2018). Habitat fragmentation caused by contaminants: Atrazine as a chemical barrier isolating fish populations. Chemosphere, 193, 24-31.
Bartumeus, F., da Luz, M. G. E., Viswanathan, G. M., & Catalan, J. (2005). Animal search strategies: A quantitative random-walk analysis. Ecology, 86, 3078-3087.
Beland, M., Biggs, T. W., Roberts, D. A., Peterson, S. H., Kokaly, R. F., & Piazza, S. (2017). Oiling accelerates loss of salt marshes, southeastern Louisiana. PLoS One, 12, Article e0181197.
Bernot, R. J., Kennedy, E. E., & Lamberti, G. A. (2005). Effects of ionic liquids on the survival, movement, and feeding behavior of the freshwater snail, Physa acuta. Environmental Toxicology and Chemistry, 24, 1759-1765.
Best, J. (2018). Anthropogenic stresses on the world's big rivers. Nature Geoscience, 7, 7-21.
Billings, S. A., & Gaydess, E. A. (2008). Soil nitrogen and carbon dynamics in a fragmented landscape experiencing forest succession. Landscape Ecology, 23, 581-593.
Bingham, F. O. (1972). The influence of environmental stimuli on the direction of movement of the supralittoral gastropod Littorina irrorata. Bulletin of Marine Science, 22, 309-335.
Bouton, S. N., Frederick, P. C., Spalding, M. G., & McGill, H. (1999). Effects of chronic, low concentrations of dietary methylmercury on the behavior of juvenile great egrets. Environmental Toxicology and Chemistry, 18, 1934-1939.
Bürkner, P. C. (2017). brms: An R package for Bayesian multilevel models using Stan. Journal of Statistical Software, 80, 1-28.
Cabecinhas, A. S., Novais, S. C., Santos, S. C., Rodrigues, A. C., Pestana, J. L., Soares, A. M., & Lemos, M. F. (2015). Sensitivity of the sea snail Gibbula umbilicalis to mercury exposure-Linking endpoints from different biological organization levels. Chemosphere, 119, 490-497.
Chevalier, J., Harscoët, E., Keller, M., Pandard, P., Cachot, J., & Grote, M. (2015). Exploration of Daphnia behavioral effect profiles induced by a broad range of toxicants with different modes of action. Environmental Toxicology and Chemistry, 34, 1760-1769. https://doi.org/10.1002/etc.2979
Cutter, J. W. (1988). Snail barrier (US Patent No. 4756116 A). US Patent and Trademark Office.
Deegan, L. A., Johnson, D. S., Warren, R. S., Peterson, B. J., Fleeger, J. W., Fagherazzi, S., & Wollheim, W. (2012). Coastal nutrient enrichment as a driver of salt marsh loss. Nature, 490, 388-392.
Doerr, E. D., & Doerr, V. A. (2005). Dispersal range analysis: Quantifying individual variation in dispersal behaviour. Oecologia, 142, 1-10.
Doerr, V. A., Barrett, T., & Doerr, E. D. (2011). Connectivity, dispersal behaviour and conservation under climate change: A response to Hodgson et al. Journal of Applied Ecology, 48, 143-147.
Edelhoff, H., Signer, J., & Balkenhol, N. (2016). Path segmentation for beginners: An overview of current methods for detecting changes in animal movement patterns. Movement Ecology, 4, 1-21.
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487-515.
Failon, C. M., Wittyngham, S. S., & Johnson, D. S. (2020). Ecological associations of Littoraria irrorata with Spartina cynosuroides and Spartina alterniflora. Wetlands, 40, 1317-1325.
Focks, A. (2014). Why we need landscape ecotoxicology and how it could be advanced-An academic perspective. Environmental Toxicology and Chemistry, 33, 1193-1194.
Garner, T. R., Hart, M. A., Sweet, L. E., Bagheri, H. T., Morris, J., Stoeckel, J. A., & Roberts, A. P. (2017). Effects of deepwater horizon oil on the movement and survival of marsh periwinkle snails (Littoraria irrorata). Environmental Science & Technology, 51, 8757-8762.
Gelman, A., Jakulin, A., Pittau, M. G., & Su, Y. S. (2008). A weakly informative default prior distribution for logistic and other regression models. Annals of Applied Statistics, 2, 1360-1383.
Haddad, N. M. (1999). Corridor and distance effects on interpatch movements: A landscape experiment with butterflies. Ecological Applications, 9, 612-622.
Haddad, N. M., Brudvig, L. A., Clobert, J., Davies, K. F., Gonzalez, A., Holt, R. D., Lovejoy, T. E., Sexton, J. O., Austin, M. P., Collins, C. D., Cook, W. M., Damschen, E. I., Ewers, R. M., Foster, B. L., Jenkins, C. N., King, A. J., Laurance, W. F., Levey, D. J., Margules, C. R., … Townshend, J. R. (2015). Habitat fragmentation and its lasting impact on earth's ecosystems. Science Advances, 1, 1-9.
Hamilton, P. V. (1977). Daily movements and visual location of plant stems by Littorina irrorata (Mollusca: Gastropoda). Marine and Freshwater Behaviour and Physiology, 4, 293-304.
Hamilton, P. V., & Winter, M. A. (1982). Behavioural responses to visual stimuli by the Littorina irrorata. Animal Behavior, 30, 752-760.
Hasselrot, B., & Grennfelt, P. (1987). Deposition of air pollutants in a wind-exposed forest edge. Water, Air, and Soil Pollution, 34, 135-143.
Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Tchamitchian, A., & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336, 348-350.
Hester, A. J., & Hobbs, R. J. (1992). Influence of fire and soil nutrients on native and non-native annuals at remnant vegetation edges in the Western Australian wheatbelt. Journal of Vegetation Science, 3, 101-108.
Holloman, E. L., & Newman, M. C. (2012). Expanding perceptions of subsistence fish consumption: Evidence of high commercial fish consumption and dietary mercury exposure in an urban coastal community. Science of the Total Environment, 416, 111-120.
Iacarella, J. C., & Helmuth, B. (2012). Body temperature and desiccation constrain the activity of Littoraria irrorata within the Spartina alterniflora canopy. Journal of Thermal Biology, 37, 15-22.
Ims, R. A., & Stenseth, N. C. (1989). Divided the fruitflies fall. Nature, 342, 21-22.
Kabadayi, C., Bobrowicz, K., & Osvath, M. (2018). The detour paradigm in animal cognition. Animal Cognition, 21, 21-35.
Kane, A. S., Salierno, J. D., Gipson, G. T., Molteno, T. C. A., & Hunter, C. (2004). A video-based movement analysis system to quantify behavioral stress responses of fish. Water Research, 38, 3993-4001.
Kater, B. J., Hannewijk, A., Postma, J. F., & Dubbeldam, M. (2000). Seasonal changes in acute toxicity of cadmium to amphipod Corophium volutator. Environmental Toxicology and Chemistry, 19, 3032-3035.
Kitamura, T., & Imafuku, M. (2015). Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes. Proceedings of the Royal Society B: Biological Sciences, 282, Article 20150483. https://doi.org/10.1098/rspb.2015.0483
Kobiela, M. E., Cristol, D. A., & Swaddle, J. P. (2015). Risk-taking behaviours in zebra finches affected by mercury exposure. Animal Behavior, 103, 153-160.
Kölzsch, A., Alzate, A., Bartumeus, F., de Jager, M., Weerman, E. J., Hengeveld, G. M., Naguib, M., Nolet, B. A., & van de Koppel, J. (2015). Experimental evidence for inherent Lévy search behaviour in foraging animals. Proceedings of Royal Society B: Biological Sciences, 282, Article 20150424. https://doi.org/10.1098/rspb.2015.0424
Krabbenhoft, D. P., & Sunderland, E. M. (2013). Global change and mercury. Science, 341, 1457-1458.
Li, Y., Lee, J. M., Chon, T. S., Liu, Y., Kim, H., Bae, M. J., & Park, Y. S. (2013). Analysis of movement behavior of zebrafish (Danio rerio) under chemical stress using hidden Markov model. Modern Physics Letters B, 27, 1-13.
Little, E. E., & Finger, S. E. (1990). Swimming behavior as an indicator of sublethal toxicity in fish. Environmental Toxicology and Chemistry, 9, 13-19. https://doi.org/10.1002/etc.5620090103
Liu, Y., Lee, S. H., & Chon, T. S. (2011). Analysis of behavioral changes of zebrafish (Danio rerio) in response to formaldehyde using self-organizing map and a hidden Markov model. Ecological Modelling, 222, 2191-2201.
Mainville, N., Webb, J., Lucotte, M., Davidson, R., Betancourt, O., Cueva, E., & Mergler, D. (2006). Decrease of soil fertility and release of mercury following deforestation in the Andean Amazon, Napo River Valley, Ecuador. Science of the Total Environment, 368, 88-98.
Maltby, L. (2013). Ecosystem services and the protection, restoration, and management of ecosystems exposed to chemical stressors. Environmental Toxicology and Chemistry, 32, 974-983.
McCloskey, J. T., & Newman, M. C. (1995). Sediment preference in the Asiatic clam (Corbicula fluminea) and viviparid snail (Campeloma decisum) as a response to low-level metal and metalloid contamination. Archives of Environmental Contamination and Toxicology, 28, 195-202.
McGee, B. L., Wright, D. A., & Fisher, D. J. (1998). Biotic factors modifying acute toxicity of aqueous cadmium to estuarine amphipod Leptocheirus plumulosus. Archives of Environmental Contamination and Toxicology, 34, 34-40.
McIntyre, N. E., & Wiens, J. A. (1999). How does habitat patch size affect animal movement? An experiment with darkling beetles. Ecology, 80, 2261-2270.
McLean, D. J., & Skowron Volponi, M. A. (2018). trajr: An R package for characterisation of animal trajectories. Ethology, 124, 440-448.
Metzger, J. P., & Décamps, H. (1997). The structural connectivity threshold: A hypothesis in conservation biology at the landscape scale. Acta Ecologica, 18, 1-12.
Michelot, T., Langrock, R., & Patterson, T. A. (2016). moveHMM: An R package for the statistical modelling of animal movement data using hidden Markov models. Methods in Ecology and Evolution, 7, 1308-1315.
Morales, J. M., & Ellner, S. P. (2002). Scaling up animal movements in heterogeneous landscapes: The importance of behavior. Ecology, 83, 2240-2247.
Nathan, R., Getz, W. M., Revilla, E., Holyoak, M., Kadmon, R., Saltz, D., & Smouse, P. E. (2008). A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy of Sciences of the United States of America, 105, 19052-19059.
Nguyen, T. V., Liu, Y., Jung, I. H., Chon, T. S., & Lee, S. H. (2011). Unraveling Markov processes in movement patterns of indicator species in response to chemical stressors. Modern Physics Letters B, 25, 1143-1149.
Niebuhr, B., Wosniack, M. E., Santos, M. C., Raposo, E. P., Viswanathan, G. M., da Luz, M. G. E., & Pie, M. R. (2015). Survival in patchy landscapes: The interplay between dispersal, habitat loss and fragmentation. Scientific Reports, 5, 1-10.
Offerman, H. L., Dale, H. V., Pearson, S. M., Bierregaard, R. O., Jr., & O'Neill, R. V. (1995). Effects of forest fragmentation on neotropical fauna: Current research and data availability. Environmental Reviews, 3, 191-211.
Pardini, R., Souza, S. M., Braga-Neto, R., & Metzger, J. P. (2005). The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape. Biological Conservation, 124, 253-266.
Pearson, S. M., Turner, M. G., Gardner, R. H., & O'Neill, R. V. (1996). An organism-based perspective of habitat fragmentation. In R. C. Szaro & D. W. Johnston (Eds.), Biodiversity in managed landscapes: Theory and practice (pp. 77-95). Oxford University Press.
R Foundation for Statistical Computing. (2020). R: A language and environment for statistical computing.
Roulet, M., Lucotte, M., Farella, N., Serique, G., Coelho, H., Passos, C. S., de Jesus da Silva, E., Scavone de Andrade, P., Mergler, D., Guimarâes, J. R. D., & Amorim, M. (1999). Effects of recent human colonization on the presence of mercury in Amazonian ecosystems. Water, Air, and Soil Pollution, 112, 297-313.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. https://doi.org/10.1038/nmeth.2089
Shirley, T. C., Denoux, G. J., & Stickle, W. B. (1978). Seasonal respiration in the marsh periwinkle, Littorina irrorata. The Biological Bulletin, 154, 322-334.
Silliman, B. R., & Newell, S. Y. (2003). Fungal farming in a snail. Proceedings of the National Academy of Sciences of the United States of America, 100, 15643-15648.
Tankersley, R. A. (1989). The effect of trail-following on the locomotion of the marsh periwinkle Littorina irrorata (mesogastropoda: Littorinidae). Marine Behaviour and Physiology, 15, 89-100. https://doi.org/10.1080/10236248909378721
Tinevez, J.-Y., Perry, N., Schindelin, J., Hoopes, G. M., Reynolds, G. D., Laplantine, E., Bednarek, S. Y., Shorte, S. L., & Eliceiri, K. W. (2017). TrackMate: An open and extensible platform for single-particle tracking. Methods, 115, 80-90. http://fiji.sc/TrackMate
Vitousek, P. M., Mooney, H. A., Lubchenco, J., & Melillo, J. M. (1997). Human domination of earth's ecosystems. Science, 277, 494-499.
Warren, J. H. (1985). Climbing as an avoidance behaviour in the salt marsh periwinkle, Littorina irrorata (Say). Journal of Experimental Marine Biology and Ecology, 89, 11-28.
Wiens, J. A., & Milne, B. T. (1989). Scaling of “landscapes” in landscape ecology, or, landscape ecology from a beetle's perspective. Landscape Ecology, 3, 87-96.
Wiens, J. A., Schooley, R. L., & Weeks, R. D., Jr. (1997). Patchy landscapes and animal movements: Do beetles percolate? Oikos, 78, 257-264.
With, K. A., Cadaret, S. J., & Davis, C. (1999). Movement responses to patch structure in experimental fractal landscapes. Ecology, 80, 1340-1353.
Wu, J., Huang, J., Han, X., Xie, Z., & Gao, X. (2003). Three-Gorges dam-Experiment in habitat fragmentation? Science, 300, 1239-1240.
Xu, X., & Newman, M. C. (2015). Mercury exposure as a function of fish consumption in two Asian communities in coastal Virginia, USA. Archives of Environmental Contamination and Toxicology, 68, 462-475.
Zartman, C. E. (2003). Habitat fragmentation impacts on epiphyllous bryophyte communities in central Amazonia. Ecology, 84, 948-954.
Zengel, S., Montague, C. L., Pennings, S. C., Powers, S. P., Steinhoff, M., Fricano, G., Schlemme, C., Zhang, M., Oehrig, J., Nixon, Z., Rouhani, S., & Michel, J. (2016). Impacts of the deepwater horizon oil spill on salt marsh periwinkles (Littoraria irrorata). Environmental Science & Technology, 50, 643-652.
Zhou, T., & Weis, J. S. (1999). Predator avoidance in mummichog larvae from a polluted habitat. Journal of Fish Biology, 54, 44-57.