Abstract
An appropriate approach to assess the effect of toxicants on aquatic animals is to monitor behavioral endpoints, as they are a link between physiological and ecological processes. A group that can be exposed long-term to low toxic concentrations is benthic macroinvertebrates, as their mobility in aquatic ecosystems is relatively limited. Therefore, the study of behavioral long-term effects in this group is suitable from an ecological point of view, as behavioral effects can appear before mortality. During the last decades there has been an increase in ammonia concentrations in freshwater ecosystems, threatening aquatic animals. The present study focuses on the long-term effects (40 days) of nonionized ammonia on the behavioral activity of the aquatic snail Potamopyrgus antipodarum. One control and three ammonia concentrations (0.02, 0.07, and 0.13 mg N–NH3/L) were used in triplicate, and the activity of snails (as mean time to start normal movement) and immobility were recorded for each treatment after 0, 10, 20, 30, and 40 days of continuous exposure to nonionized ammonia. The results show that P. antipodarum presented a high tolerance to lethal long-term effects of nonionized ammonia, as no animal died during the bioassay. However, the behavioral activity of snails was a very sensitivity endpoint, as a mean nonionized ammonia concentration of 0.07 mg N–NH3/L affected P. antipodarum. The results are discussed and compared with the available literature on long-term effects of ammonia on freshwater macroinvertebrates. Additionally, the ammonia water quality criteria, NOECs, LOECs, and long-term LCs are discussed on the basis of the current available data for freshwater macroinvertebrates.
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References
Abel PD (2000) Water pollution biology, 2nd edn. Taylor & Francis, London
Alabaster JS, Lloyd R (1982) Water quality criteria for freshwater fish, 2nd edn. Butterworths, London
Alleman JE (1998) Purdue University Web Page. Java unionized ammonia calculator. Available at: http://cobweb.ecn.purdue.edu/~piwc/w3_research/free-ammonia/nh3.html
Alonso A (2005) Valoración de la degradación ambiental y efectos ecotoxicológicos sobre la comunidad de macroinvertebrados bentónicos en la cabecera del río Henares. Doctoral dissertation, Universidad de Alcalá, Alcalá de Henares, Spain
Alonso A, Camargo JA (2003) Short-term toxicity of ammonia, nitrite and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bull Environ Contam Toxicol 70:1006–1012. doi:10.1007/s00128-003-0082-5
Alonso A, Camargo JA (2004a) Sub-lethal responses of the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca) to unionized ammonia: a tolerant invading species. Fresen Environ Bull 13:607–615
Alonso A, Camargo JA (2004b) Toxic effects of unionized ammonia on survival and feeding activity of the freshwater amphipod Eulimnogammarus toletanus (Gammaridae, Crustacea). Bull Environ Contam Toxicol 72:1052–1058. doi:10.1007/s00128-004-0350-z
Alonso A, Camargo JA (2006) Ammonia toxicity to the freshwater invertebrates Polycelis felina (Planariidae, Turbellaria) and Echinogammarus echinosetosus (Gammaridae, Crustacea). Fresen Environ Bull 15:1578–1583
Alonso A, Castro-Diez P (2008) What explains the invading success of the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614:107–116. doi:10.1007/s10750-008-9529-3
APHA (American Public Health Association) (1995) Standard methods for the examination of water and wastewater, 19th edn. APHA-AWWA-WPCF, Washington, DC
Borgmann U (1994) Chronic toxicity of ammonia to the amphipod Hyalella azteca; importance of ammonium ion and water hardness. Environ Poll 86:329–335. doi:10.1016/0269-7491(94)90173-2
Burris JA, Bamford MS, Stewart AJ (1990) Behavioural responses of marked snails as indicators of water quality. Environ Toxicol Chem 9:69–76. doi:10.1897/1552-8618(1990)9[69:BROMSA]2.0.CO;2
Calevro F, Campani S, Filippi C, Batistoni R, Deri P, Bucci S, Ragghianti M, Mancino G (1999) Bioassays for testing effects of Al, Cr and Cd using development in the amphibian Pleurodeles waltl and regeneration in the planarian Dugesia etrusca. Aquat Ecosyst Health Manage 2:281–288
Camargo JA, Alonso A (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Intern 32:831–849. doi:10.1016/j.envint.2006.05.002
Cheung SG, Wong LS (1999) Effect of copper on activity and feeding in the subtidal prosobranch Babylonia lutosa (Lamarck) (Gastropoda: Buccinidae). Mar Poll Bull 39:106–111. doi:10.1016/S0025-326X(98)00205-7
Cheung SG, Tai KK, Leung CK, Siu YM (2002) Effects of heavy metals on the survival and feeding behaviour of the sandy shore scavenging gastropod Nassarius festivus (Powys). Mar Poll Bull 45:107–113. doi:10.1016/S0025-326X(01)00324-1
Cold A, Forbes VE (2004) Consequences of a short pulse of pesticide exposure for survival and reproduction of Gammarus pulex. Aquat Toxicol 67:287–299. doi:10.1016/j.aquatox.2004.01.015
Craig S, Laming P (2004) Behaviour of the three-spined stickleback, Gasterosteous aculeatus (Gasterosteidae, Teleostei) in the multispecies freshwater biomonitor: a validation of automated recordings at three levels of ammonia pollution. Water Res 38:2144–2154. doi:10.1016/j.watres.2004.01.021
De Lange HJ, Sperber V, Peeters ETHM (2006a) Avoidance of polycyclic aromatic hydrocarbon-contaminated sediments by the freshwater invertebrates Gammarus pulex and Asellus aquaticus. Environ Toxicol Chem 25:452–457. doi:10.1897/05-413.1
De Lange HJ, Noordoven W, Murk AJ, Lurling M, Peeters ETHM (2006b) Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209–216. doi:10.1016/j.aquatox.2006.03.002
Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effect of pH and temperature. J Fish Res Bd Can 32:2379–2383
Environment Canada (2001) Priority substances assessment report: ammonia in the aquatic environment. Minister of Public Works and Government Services Canada, Ottawa, Ontario
Gerhardt A (2007a) Aquatic behavioral ecotoxicology: prospects and limitations. Hum Ecol Risk Assess 13:481–491. doi:10.1080/10807030701340839
Gerhardt A (2007b) Importance of exposure route for behavioural responses in Lumbriculus variegatus Muller (Oligochaeta: Lumbriculida) in short-term exposures to Pb. Environ Sci Pollut R 14:430–434. doi:10.1065/espr2006.12.371
Gerhardt A, Svensson E, Clostermann M, Fridlund B (1994) Monitoring of behavioral patterns of aquatic organisms with an impedance conversion technique. Environ Intern 20:209–219. doi:10.1016/0160-4120(94)90138-4
Gerhardt A, De Bisthoven LJ, Mo Z, Wang C, Yang M, Wang Z (2002) Short-term responses of Oryzias latipes (Pisces: Adrianichthyidae) and Macrobrachium nipponense (Crustacea: Palaemonidae) to municipal and pharmaceutical waste water in Beijing, China: survival, behaviour, biochemical biomarkers. Chemosphere 47:35–47. doi:10.1016/S0045-6535(01)00223-5
Golding LA, Timperley MH, Evans CW (1997) Non-lethal responses of the freshwater snail Potamopyrgus antipodarum to dissolved arsenic. Environ Monit Assess 47:239–254. doi:10.1023/A:1005796318728
Hickey CW, Martin ML (1999) Chronic toxicity of ammonia to the freshwater bivalve Sphaerium novaezelandiae. Arch Environ Contam Toxicol 36:38–46. doi:10.1007/s002449900440
Hickey CW, Vickers ML (1994) Toxicity of ammonia to nine native New Zealand freshwater invertebrate species. Arch Environ Contam Toxicol 26:292–298. doi:10.1007/BF00203554
Hickey CW, Golding LA, Martin ML, Croker GF (1999) Chronic toxicity of ammonia to New Zealand freshwater invertebrates: a mesocosm study. Arch Environ Contam Toxicol 37:338–351. doi:10.1007/s002449900523
Jones M, Folt C, Guarda S (1991) Characterizing individual, population and community effects of sublethal levels of aquatic toxicants—an experimental case-study using Daphnia. Freshwater Biol 26:35–44. doi:10.1111/j.1365-2427.1991.tb00506.x
Kirkpatrick AJ, Gerhardt A, Dick JTA, Laming P, Berges JA (2006) Suitability of Crangonyx pseudogracilis (Crustacea: Amphipoda) as an early warning indicator in the Multispecies Freshwater Biomonitor. Environ Sci Pollut Res 13:242–250. doi:10.1065/espr2006.06.313
Kramer KJM, Jenner HA, Zwart D (1989) The valve movement response of mussels: a tool in biological monitoring. Hydrobiologia 188–189:433–443
Mummert AK, Neves RJ, Newcomb TJ, Cherry DS (2003) Sensitivity of juvenile freshwater mussels (Lampsilis fasciola, Villosa iris) to total and unionized ammonia. Environ Toxicol Chem 22:2545–2553. doi:10.1897/02-341
Newton TJ, Allran JW, O’Donnell JA, Bartsch MR, Richardson WB (2003) Effects of ammonia on juvenile unionid mussels (Lampsilis cardium) in laboratory sediment tests. Environ Toxicol Chem 22:2554–2560. doi:10.1897/02-342
Passel HD, Dahm CN, Bedrick EJ (2007) Ammonia modeling for assessing potential toxicity to fish species in the Rio Grande. Ecol Appl 17:2087–2099. doi:10.1890/06-1293.1
Rand GM (1985) Behavior. In: Rand GM, Pretrocelli SR (eds) Fundamentals of aquatic toxicology. Hemisphere, Washington, DC, pp 221–263
Rebelo MF, Rodriguez EM, Santos EA, Ansaldo M (2000) Histopathological changes in gills of the estuarine crab Chasmagnathus granulata (Crustacea-Decapoda) following acute exposure to ammonia. Comp Biochem Physiol 125C:157–164
Richardson J, Williams EK, Kickey CW (2001) Avoidance behaviour of freshwater fish and shrimp exposed to ammonia and low dissolved oxygen separately and in combination. NZ J Mar Freshw Res 35:625–633
Riddell DJ, Culp JM, Baird DJ (2005) Behavioral responses to sublethal cadmium exposure within an experimental aquatic food web. Environ Toxicol Chem 24:431–441. doi:10.1897/04-026R.1
Rosenberg DM, Resh VH (eds) (1993) Freshwater biomonitoring and benthic macroinvertebrates. Chapman & Hall, London
Russo RC (1985) Ammonia, nitrite and nitrate. In: Rand GM, Petrocelli SR (eds) Fundamentals of aquatic toxicology. Hemisphere, Washington, DC, pp 455–471
Schriks M, Van Hoorn MK, Faassen EJ, Van Dam JW, Murk AJ (2006) Real-time automated measurement of Xenopus leavis tadpole behavior and behavioral responses following triphenyltin exposure using the multispecies freshwater biomonitor (MFB). Aquat Toxicol 77:298–305. doi:10.1016/j.aquatox.2005.12.011
Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392. doi:10.1016/j.aquatox.2004.03.016
U.S. Environmental Protection Agency (1986) Quality criteria for water. U.S. EPA, 440/5–86-001. U.S. EPA, Washington, DC
U.S. Environmental Protection Agency (1999) Update of ambient water quality criteria for ammonia. U.S. EPA 822/R-99-014. U.S. EPA, Washington, DC
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750
Wallace WG, Estephan A (2004) Differential susceptibility of horizontal and vertical swimming activity to cadmium exposure in a gammaridean amphipod (Gammarus lawrencianus). Aquat Toxicol 69:289–297. doi:10.1016/j.aquatox.2004.05.010
Wang N, Ingersoll CG, Greer IE, Hardesty DK, Ivey CD, Kunz JL, Brumbaugh WG, Dwyer EJ, Roberts AD, Augspurger T, Kane CM, Neves RJ, Barnhart MC (2007) Chronic toxicity of copper and ammonia to juvenile freshwater mussels (Unionidae). Environ Toxicol Chem 26:2048–2056. doi:10.1897/06-524R.1
Watts MM, Pascoe D, Carroll K (2001) Survival and precopulatory behaviour of Gammarus pulex (L.) exposed to two xenoestrogens. Water Res 35:2347–2352. doi:10.1016/S0043-1354(00)00537-6
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall International, Englewood Cliffs, NJ
Acknowledgments
Funds for this research came from the Ministry of Science and Technology (Research Project REN2001-1008/HID) in Spain. The University of Alcalá provided logistical support. Dr. Álvaro Alonso was supported by predoctoral grants from the Council of Castilla-La Mancha and the University of Alcalá and by a postdoctoral contract from the Spanish Ministry of Science and Innovation at the Water Ecology and Water Quality Management Group of Wageningen University (The Netherlands). Dr. Álvaro Alonso is currently supported by a Juan de la Cierva contract. We are sincerely grateful to Dr. Pilar Castro for correction of the English and for useful comments that improved this work.
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Alonso, Á., Camargo, J.A. Long-Term Effects of Ammonia on the Behavioral Activity of the Aquatic Snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Arch Environ Contam Toxicol 56, 796–802 (2009). https://doi.org/10.1007/s00244-008-9266-7
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DOI: https://doi.org/10.1007/s00244-008-9266-7